literature review on food safety and hygiene

Food Safety and Hygiene: Current Policies, Quality Standards, and Scope of Artificial Intelligence

• First Online: 02 April 2024

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• Yogita Chavan   ORCID: orcid.org/0009-0008-6199-4703 23 ,
• Kaninika Paul   ORCID: orcid.org/0000-0002-6566-5973 23 &
• Nikhil Kolekar 23  

Part of the book series: Advances in Science, Technology & Innovation ((ASTI))

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Ensuring food safety and hygiene is of supreme importance to protect public health and prevent foodborne illnesses. This chapter explores the current state of food safety policies and quality standards, highlighting their crucial role in regulating the food industry and safeguarding consumers. By analyzing the existing challenges and gaps in traditional approaches, the chapter emphasizes the potential benefits of integrating artificial intelligence (AI) into food safety practices. AI-powered technologies offer a promising scope for revolutionizing food safety and hygiene protocols. The abstract delves into the various AI applications, including automated monitoring systems, E-learning systems, Inspection apps, labeling, and light-based decontamination that can enhance risk assessment, early detection of contamination, and supply chain traceability. Furthermore, this chapter highlights the potential obstacles to adopting AI in this domain, such as data privacy and regulatory concerns. By embracing AI's potential while addressing its limitations, stakeholders can foster a safer food ecosystem, fortify consumer confidence, and cultivate a healthier society.

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Abbreviations

Artificial Intelligence

Artificial Neural Network

Current Good Manufacturing Practices

European Union

Food and Agriculture Organization

Genetic Algorithms

Global Food Safety Initiative

Good Hygienic Practices

Genetically Modified Organisms

Good Manufacturing Practices

Hazards Analysis and Critical Control Points

High Definition

Internet of Things

Learning Vector Quantization

Management Oriented Modeling

Nitrogen, Phosphorous, and Potassium

Sanitary and Phytosanitary Measures

Support Vector Machine

Unmanned Aerial Vehicle

Ultra Violet

World Health Organization

World Trade Organization

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Chavan, Y., Paul, K., Kolekar, N. (2024). Food Safety and Hygiene: Current Policies, Quality Standards, and Scope of Artificial Intelligence. In: Chakraborty, R., Mathur, P., Roy, S. (eds) Food Production, Diversity, and Safety Under Climate Change. Advances in Science, Technology & Innovation. Springer, Cham. https://doi.org/10.1007/978-3-031-51647-4_26

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An Integrative Review of Hygiene Practice Studies in the Food Service Sector

Affiliations.

• 1 Department of Food and Nutrition, University of Ulsan, 93 Daehak-ro, Nam-gu, Ulsan, 44610, South Korea (ORCID: https://orcid.org/0000-0003-3750-1370).
• 2 Department of Hotel Culinary Arts Bakery, Ulsan College, 101 Bong su-ro, Dong-gu, Ulsan, 44022, South Korea.
• PMID: 32692821
• DOI: 10.4315/JFP-19-488

Abstract: This article reviews the recent literature on studies relevant to hygiene practices of food service workers. A total of 32 articles were chosen for evaluation from a systematic search of the published literature from 2014 to 2019. For the assessment of hygiene practices, hand washing as a measurement item and observation as a method were most frequently used. Factors influencing hygiene practices were categorized as internal and external variables. Internal variables included knowledge; psychological factors, such as attitude, risk perception, self-efficacy, and optimistic bias; and food handlers' sociodemographic characteristics, such as work experience and exposure to hygiene training. External variables included characteristics of food premises, such as the size of the operation and number of people served, and organizational factors, such as training. Regarding the recent training literature, attempts to bring in new methodologies and new technologies were found, such as multimedia case studies, cognitive word association, behavior-focused training, wearable technology, and simulation games. Among the theories utilized, knowledge, attitude, and practices were applied most frequently to explain hygiene practices. In particular, this review highlights the important fact that internal and external factors that affect hygiene practices should be considered to maintain good hygiene practices.

Keywords: External variables; Factors influencing hygiene practices; Food service; Hygiene practice; Internal variables; Training.

Copyright ©, International Association for Food Protection.

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Public health risks related to food safety issues in the food market: a systematic literature review

Zemichael gizaw.

Department of Environmental and Occupational Health and Safety, Institute of Public Health, College of Medicine and Health Sciences, University of Gondar, Gondar, Ethiopia

Associated Data

All the extracted data are included in the manuscript.

Food safety in the food market is one of the key areas of focus in public health, because it affects people of every age, race, gender, and income level around the world. The local and international food marketing continues to have significant impacts on food safety and health of the public. Food supply chains now cross multiple national borders which increase the internationalization of health risks. This systematic review of literature was, therefore, conducted to identify common public health risks related to food safety issues in the food market.

All published and unpublished quantitative, qualitative, and mixed method studies were searched from electronic databases using a three step searching. Analytical framework was developed using the PICo (population, phenomena of interest, and context) method. The methodological quality of the included studies was assessed using mixed methods appraisal tool (MMAT) version 2018. The included full-text articles were qualitatively analyzed using emergent thematic analysis approach to identify key concepts and coded them into related non-mutually exclusive themes. We then synthesized each theme by comparing the discussion and conclusion of the included articles. Emergent themes were identified based on meticulous and systematic reading. Coding and interpreting the data were refined during analysis.

The analysis of 81 full-text articles resulted in seven common public health risks related with food safety in the food market. Microbial contamination of foods, chemical contamination of foods, food adulteration, misuse of food additives, mislabeling, genetically modified foods (GM foods), and outdated foods or foods past their use-by dates were the identified food safety–related public health risks in the food market.

This systematic literature review identified common food safety–related public health risks in the food market. The results imply that the local and international food marketing continues to have significant impacts on health of the public. The food market increases internationalization of health risks as the food supply chains cross multiple national borders. Therefore, effective national risk-based food control systems are essential to protect the health and safety of the public. Countries need also assure the safety and quality of their foods entering international trade and ensure that imported foods conform to national requirements.

Food safety is an important issue that affects all of the world’s people. Many countries throughout the world are increasingly interdependent on the availability of their food supply and on its safety. Hence, people all over the world increasingly value food safety; food production should be done safely to maximize public health gains and environmental benefits. Food safety deals with safeguarding the food supply chain from the introduction, growth, or survival of hazardous microbial and chemical agents [ 1 , 2 ].

Unsafe food containing harmful bacteria, viruses, parasites, or chemical substances causes more than 200 diseases—ranging from diarrhea to cancers. An estimated 600 million in the world fall ill after eating contaminated food and 420,000 die every year, resulting in the loss of 33 million disability adjusted life years (DALYs). Children under 5 years of age carry 40% of the food borne disease burden, with 125,000 deaths every year. Diarrheal diseases are the most common illnesses resulting from the consumption of contaminated food, causing 550 million people to fall ill and 230,000 deaths every year [ 3 ].

Food safety is being challenged nowadays by the global dimensions of food supply chains [ 1 , 4 , 5 ]. Foods in the international market may be frauded as different parties such as manufacturers, co-packers, distributors, and others along the chain of distribution involve in the national or international trade [ 6 – 8 ]. Food safety in the food market is one of the key areas of focus in public health, because it affects people of every age, race, gender, and income level around the world. The local and international food marketing continues to have significant impacts on food safety and health of the public. Food supply chains now cross multiple national borders which increase the internationalization of health risks [ 9 – 14 ]. This systematic review of literature was, therefore, conducted to identify common public health risks related to food safety issues in the food market. This review provides evidence to improve food safety in the food market using risk-based food safety strategies. Healthcare providers, researchers, and policy makers may use the results of this systematic literature review to protect the public from undue health effects due to consumption of foods with poor quality and safety.

Research question

What food safety–related public health risks are commonly found in the food market?

Analytical framework

We developed the components of the analytical framework using the PICo (population, phenomena of interest, and context) method. The population for this review was the public over the globe. The phenomenon of interest for this review was public health risks associated with food safety. The context was the food market (such as restaurants, food stores, supermarkets, shops, food processing plants, and street vending). The reviewers sat together to discuss and refine the framework.

Criteria for considering studies for this review

All published and unpublished quantitative, qualitative, and mixed method studies conducted on food safety–related health risks for the general public in the food market were included. Governmental and other organizational reports were also included. Articles published other than English language, citations with no abstracts and/or full texts, duplicate studies, and studies with poor quality were excluded.

Search strategy

We searched published articles/or reports from MEDLINE/ PubMed, EMBASE, CINAHL, Access Medicine, Scopus, Web of Science, Google Scholar, WHO Library, FAO Libraries, and WTO Library. We also searched thesis and dissertations from Worldcat and ProQuest. We used a three step searching. In the first step, we conducted an initial limited search of MEDLINE and analyzed the text words contained in the title and abstract, and of the index terms used to describe articles. Secondly, we searched across all included databases using all identified keywords and index terms. Thirdly, references of all identified articles were searched to get additional studies. The search term we used in the initial searching is presented as follows.

((((("public health"[MeSH Terms] OR ("public"[All Fields] AND "health"[All Fields]) OR "public health"[All Fields]) AND ("risk"[MeSH Terms] OR "risk"[All Fields] OR "risks"[All Fields])) OR (("public health"[MeSH Terms] OR ("public"[All Fields] AND "health"[All Fields]) OR "public health"[All Fields]) AND hazards[All Fields])) OR (("public health"[MeSH Terms] OR ("public"[All Fields] AND "health"[All Fields]) OR "public health"[All Fields]) AND problems[All Fields])) AND ((("food safety"[MeSH Terms] OR ("food"[All Fields] AND "safety"[All Fields]) OR "food safety"[All Fields]) OR ("food quality"[MeSH Terms] OR ("food"[All Fields] AND "quality"[All Fields]) OR "food quality"[All Fields])) OR (("food"[MeSH Terms] OR "food"[All Fields]) AND ("hygiene"[MeSH Terms] OR "hygiene"[All Fields])))) AND (((("food"[MeSH Terms] OR "food"[All Fields]) AND market[All Fields]) OR (("food"[MeSH Terms] OR "food"[All Fields]) AND trade[All Fields])) OR (("food supply"[MeSH Terms] OR ("food"[All Fields] AND "supply"[All Fields]) OR "food supply"[All Fields]) AND chain[All Fields]))

Assessment of methodological quality

Search results from different electronic databases were exported to Endnote reference manager to remove duplication. Two independent reviewers (ZG and BA) screened out articles using titles and abstracts. The reviewers further investigated and assessed full-text articles against the inclusion and exclusion criteria. The reviewers sat together to resolve disagreements during the review. The methodological quality of the included studies was assessed using mixed methods appraisal tool (MMAT) version 2018 [ 15 ]. This method explains the detail of each criterion. The rating of each criterion was, therefore, done as per the detail explanations included in the method. Almost all of the included full-text articles fulfilled the criteria and all the included full-text articles were found to be better quality.

Data extraction

In order to minimize bias, we the reviewers independently extracted data from papers included in the review using JBI mixed methods data extraction form [ 16 ]. The data extraction form was piloted on randomly selected papers and modified accordingly. Eligibility assessment was performed independently by the two reviewers. Information like authors, year of publication, study areas, type of studies, and focus of the study or main messages were extracted.

Synthesis of findings

The included full-text articles were qualitatively analyzed using emergent thematic analysis approach to identify key concepts and coded them into related non-mutually exclusive themes. We then synthesized each theme by comparing the discussion and conclusion of the included articles. Emergent themes were identified based on meticulous and systematic reading. Coding and interpreting the data were refined during the analysis.

The search process

The search strategy identified 2641 titles and abstracts (1890 from PubMed and 751 from other sources) as of 13 June 2019. We obtained 1992 title and abstracts after we removed duplicates. Following assessment by title and abstract, 705 articles were retrieved for more evaluation and 344 articles were assessed for eligibility. Finally, 81 articles were included for systematic literature review based on the inclusion criteria (Fig. ​ (Fig.1 1 ).

Study selection flow diagram

In this review, 81 of 1992 (4%) full-text articles matched the inclusion criteria. The overwhelming majority, 74 of 81 (91%) of the included full-text articles are research articles; 2 (3%) are short communications; 2 (3%) are regulatory papers, 1 (1%) is field inspection; 1 (1%) is research note; and the other 1 (1%) is thesis. Of the included full-text articles, 30 of 81 (37%) are conducted in Asia; 4 of 81 (5%) are conducted in multiple countries in the same region or across regions; and 1of 81 (1%) is not region specific (Fig. ​ (Fig.2 2 ).

Regions where the included full-text articles conducted

All the included full-text articles are published between 1991 and 2018 (35 (43%) between 2011 and 2015; 16 (20%) between 2000 and 2005; 16 (20%) between 2006 and 2010; 12 (15%) between 2016 and 2018; and the rest 2(2%) before 2000).

Food safety–related public health risks identified from the search process

The analysis of 81 full-text articles resulted in seven common public health risks related with food safety in the food market. Microbial contamination of foods, chemical contamination of foods, food adulteration, misuse of food additives, mislabeling, GM foods, and foods past their use-by dates were the identified food safety–related health risks in the food market (Table ​ (Table1 1 ).

Common food safety–related public health risks identified from the search process

Table ​ Table2 2 shows food safety–related public health risks in the food market by country name (countries are categorized into developed and developing based on the United Nations (UN) 2019 list). Among 21 full-text articles included for microbial contamination of foods, 13 (62%) were from developing countries. This may suggest microbial contamination of foods in the food market is a common public health risk in developing countries than the developed. Eight (53%) of 15 articles retrieved for chemical contamination of foods in the food market were from developing countries. The vast majority, 8 of 9 (89%) full-text articles retrieved for food adulteration were from developing countries, which may indicate adulteration of foods is practiced more of in developing countries. Similarly, 8 of 11 (73%) of the full-text articles included for misuse of food additives were from developing countries, which may show misuse of food additives is a common problem in developing countries. For mislabeling, 14 of 17 (82%) and 8 of 17 (47%) of the full-text articles were from developed and developing countries respectively. Four out of six (67%) of full-text articles retrieved for foods past use-by dates were from developing countries. This may show selling of outdated foods is common in developing countries than the developed.

Food safety–related public health risks in the food market by country name (countries are categorized into developed and developing based on the United Nations (UN) 2019 list)

Numbers in the bracket show the number of full-text articles included

a There are studies conducted in two and/or three different countries. In this case, we may count one study twice and /or three times.

b One study was conducted in a general context. So, we did not include it when we categorize studies in regions

Figure ​ Figure3 3 shows comparison of food safety issues in developed and developing countries. A total of 37 and 50 articles were included in this review from developed and developing countries respectively. The comparison of food safety issues among developed countries suggests that mislabeling (38%), microbial contaminations (22%), and chemical contamination (19%) are the commonest food safety issues in the food market. Similarly, the comparison of food safety issues among developing countries suggests that microbial contaminations (26%), chemical contaminations (16%), food adulteration (16%), misuse of additives (16%), and mislabeling (16%) are the commonest food safety issues in the food market.

Comparison of food safety issues in developed and developing countries

Microbial contamination of foods

In this review, 21 of 81 (26%) full-text articles reported the presence of pathogenic microorganisms in different food items in the food market. These studies identified different diseases causing bacteria mainly Salmonella spp., Escherichia coli , Klebsiella spp., Shigella spp., Enterobacter spp., Proteus spp., Citrobacter spp. Staphylococcus aureus , Campylobacter spp., Listeria spp., Vibrio , Alklegens spp., Bacillus cereus , Pseudomonas spp., Clostridium perfringens , Arcobacter spp., and Enterococcus spp. Moreover, different fungus such as Blastomyces, Fusarium spp., Mucor spp., Aspergillus niger , Fusarium avenaceum , Penicillium digitatum , Rhizopus stolonifer , Saccharomyces species, Fusarium solani , Aspergillus flavus , Saccharomyces dairensis , and Saccharomyces exiguus were identified from different food items from food stores or shops. The included studies also reported that some of the microorganisms are resistant to different antimicrobials (Table ​ (Table3). 3 ). The results also show that total coliforms, fecal coliforms, and different fungus were commonly reported in developing countries than developed countries. On the other hand, different Campylobacter species were reported in developed countries than developed countries.

Summary of full-text articles which reported microbial contamination of foods as a public risk in food marketing

Chemical contamination of foods

Fifteen (19%) of the full-text articles included in this review reported that contamination of foods with hazardous chemicals is a major public health concern associated with the food market. Heavy metals (like cadmium, nickel, lead, copper, zinc, iron, mercury, and manganese), pesticide residuals (like dichlorvos, dimethoate, parathion-methyl, pirimiphos-methyl, and parathion), persistent organic pollutants (like dichlorodiphenyltrichloroethane metabolites, polychlorinated biphenyls, perfluorooctanoic acid, endosulfans, and aldrin), organic compounds (like patulin, chloroform, formalin, and urea), volatile organic compounds (like ethyl benzene, o-xylene, and benzene), hydrocarbons (like benzo[a]pyrene and toluene), and other chemical compounds (like calcium carbide and cyanide) are chemical contaminants identified by the full-text articles included in this review. In most cases, the concentration of chemicals exceeded the tolerable limit for consumable food items (Table ​ (Table4 4 ).

Summary of full-text articles which reported chemical contamination of foods as a public risk in food marketing

Food adulteration

In 9 (11%) of full-text articles included in this review, food adulteration has been discussed as a major public health risk associated with food safety issues in the food market. Most of the foodstuffs in the market are adulterated in varying degrees. Chemicals (like urea fertilizer, artificial color flavors, textile dye, formalin, chlorofluorocarbon; DDT powder, sodium bicarbonate, neutralizers, detergents, hydrogen peroxide, caustic soda, sodium chloride, boric acid, ammonium sulfate, sorbitol, metanil yellow, ultramarine blue, rhodamine B., maleic anhydride, copper chlorophyll, dimethyl/diethyl yellow, argemone oil, burnt mobil, and burnt oil); items which are not the genuine component of foods (like potato smash, cow’s fat and intestine in ghee, water in milk, sugar in honey, etc.); poor-quality products; and physical or inert agents (like saw dust and brick powder) are the commonest adulterants added to different food items (Table ​ (Table5 5 ).

Summary of full-text articles which reported food adulteration as a public risk in food marketing

Misuse of food additives

In this systematic review of literature, 11 of 81 (14%) full-text articles showed that misuse of food additives in the food market endangers public health. As reported in the included full-text articles, even though some food colorants and sweeteners are permitted to use such as sunset yellow FCF (SSYFCF), tartrazine, erythrosine, new coccine, ponceau, and saccharin (some may not be permitted based on countries food regulation), their concentration exceeded the prescribed limit. Moreover, use of non-permitted colorants and sweeteners such as rhodamine B, metanil yellow, orange II, malachite green, auramine, quinoline yellow, amaranth, carmoisine, Sudan dyes, and cyclamate (some may be permitted based on countries food regulation) is also commonly reported in the included studies (Table ​ (Table6 6 ).

Summary of full-text articles which reported misuse of food additives as a public risk in food marketing

Mislabeling

Mislabeling of food products has been mentioned as a major public health risk associated with food safety in the food market in 17 of 81 (21%) full-text articles included in this review. All of the 17 studies reported that significant proportion of food samples collected from supermarkets, food stores, shops, and restaurants were genetically identified as entirely different species from that identified on the product labels, and therefore were considered as mislabeled. The studies witnessed that seafood is the most commonly mislabeled food product (Table ​ (Table7 7 ).

Summary of full-text articles which reported mislabeling as a public risk in food marketing

Genetically modified foods

In this systematic review of literature, 4 of 81 (5%) of the included full-text articles discussed that GM foods are becoming an increasing public health risk. Hypertension, stroke, diabetes, obesity, lipoprotein metabolism disorder, Alzheimer’s, Parkinson’s, multiple sclerosis, hepatitis C, end-stage renal disease, acute kidney failure, cancers of the thyroid/liver/bladder/pancreas/kidney, myeloid leukemia, diarrhea, vomiting, difficulty in breathing, respiratory problems, hormonal imbalances and susceptibility to infection or immunosuppression, allergenic or rashes, and chemical toxicity are health problems reported in the included full-text articles (Table ​ (Table8 8 ).

Summary of full-text articles which reported genetically modified foods as a public risk in food marketing

Foods past their use-by dates

Six (7%) of the included full-text articles revealed that outdated or foods past their use-by dates are being sold in food stores, shops, and restaurants which are contributing huge public health and environmental problems (Table ​ (Table9 9 ).

Summary of full-text articles which reported foods past their use-by dates as a public risk in food marketing

This review identified that microbial contamination, chemical contamination, adulteration, misuse of food additives, mislabeling, genetically modified foods, and outdated foods are common public health risks related with food safety issues in the food market. In the food market, food can become contaminated in one country and cause health problems in another. These food safety issues cause exposure of consumers to biological, chemical, and physical hazards [ 91 – 95 ] so that endanger health of the public. The origin of food hazards can be described as a chain which commences on the source and continues with transportation, further processing steps, merchandising events and finally ends with the consumer [ 96 – 100 ]. Overall, this review suggested that food safety–related public health risks are more common in developing countries than developed countries. This can be justified that foods get easily contaminated with microbes due to the poor hygiene and sanitation in developing countries [ 101 – 104 ]. Moreover, hence the regulatory services are weak in developing countries, most food sellers may not comply with food hygiene and safety requirements or standards [ 105 – 107 ]. In developing countries, the legislation enforcement is still weak about administrating the concentration of harmful contaminants in the food [ 108 , 109 ]. In addition, there is inadequate information and technology to detect fake and fraud products [ 110 – 112 ] .

This review identified that microbial contamination of foods in the food market is commonly reported in many studies. Different bacterial species and funguses were the commonest diseases causing pathogens identified [ 17 – 35 , 113 ]. Failure to apply food safety strategies in every stage of the food supply chain, for example bad food handling practices, poor production process, poor agricultural practices, poor transportation system, poor marketing practices, and poor sanitation lead to microbial contamination of foods [ 114 – 118 ]. Moreover, fraud of foods such as adulteration, mislabeling, and selling of spoiled or expired foods are also causing microbial contamination [ 36 , 119 – 122 ]. Microbial contamination of foods causes millions of diseases and thousands of deaths [ 123 ]. This review also shows that total coliforms, fecal coliforms, and different fungus were commonly reported in developing countries than developed countries. This might be due to the fact that fecal contamination of foods and the environment is common in developing countries due to poor sanitation condition [ 124 – 126 ]. Moreover, the temperature and air system of food storage areas are not well regulated in developing countries. This situation creates favorable condition for molds. On the other hand, different Campylobacter species were reported in developed countries. This might be due to the fact that advancement of molecular techniques to identify these microorganisms. Developing countries lack specialized cultivation techniques to culture these organisms [ 127 ]. The standard culture–based technique, which is a predominant detection method in developing countries, is not effective for Campylobacter species [ 128 – 130 ].

Contamination of foods with hazardous chemicals has been reported as a major public health concern associated with the food market in individual studies included in this review [ 37 – 46 , 48 , 131 – 133 ]. The phases of food processing, packaging, transportation, and storage are significant contributors to food contamination [ 109 ]. Food contaminants include environmental contaminants, food processing contaminants, unapproved adulterants and food additives, and migrants from packaging materials. Environmental contaminants are impurities that are either introduced by human or occurring naturally in water, air, or soil. Food processing contaminants include those undesirable compounds, which are formed in the food during baking, roasting, canning, heating, fermentation, or hydrolysis. The direct food contact with packaging materials can lead to chemical contamination due to the migration of some harmful substances into foods. Use of unapproved or erroneous additives may result in food contamination [ 134 – 138 ]. Chemical contamination of foods is responsible millions of cases of poisoning with thousands of hospitalizations and deaths each year [ 139 ].

Nine of the full-text articles included in this review reported that food adulteration is a major public health risk associated with food safety issues in the food market. Chemicals, items which are not the genuine component of foods, poor-quality products, and physical or inert agents are the commonest adulterants added [ 47 , 49 – 56 ]. Food adulteration involves intentional or unintentional addition of useless, harmful, unnecessary chemical, physical, and biological agents to food which decreases the quality of food. It also includes removal of genuine components and processing foods in unhygienic way [ 119 , 140 ]. However, removal of genuine components of food is not considered in this review. Food is adulterated to increase the quantity and make more profit, which is economically motivated adulteration [ 141 – 143 ]. Chemicals which are being used as adulterants have a wide range of serious effects on the health of consumers including cancer [ 119 , 144 – 147 ].

In this systematic review of literature, 11 of the full-text articles reported that misuse of food additives in the food market endangers public health [ 57 – 67 ]. Food additive is any substance not normally consumed as a food by itself; not normally used as a typical ingredient of the food (whether or not it has nutritive value); and added intentionally to food for a technological purpose in the production process for the purpose of maintaining a food’s nutritional quality, for example by preventing the degradation of vitamins, essential amino acids, and unsaturated fats; extending the shelf life of a product, for example by preventing microbial growth; and maintaining and improving a product’s sensory properties, such as texture, consistency, taste, flavor, and color; Being able to provide products [ 148 , 149 ]. Substances generally recognized as safe (GRAS) can be used as food additives [ 150 , 151 ]; however, misuse of substances such as using more than the maximum allowable concentration; using non-permitted substances; and blending of permitted and non-permitted substances together causes health hazards [ 152 , 153 ].

Mislabeling of food products has been mentioned as a major public health risk associated with food safety in the food market in 17 of the full-text articles included in this review [ 68 – 82 , 154 ]. Mislabeling of food products includes false advertising, deliberately or accidentally leaving out ingredients, not listing potential health effects, and claiming a food contains ingredients that it does not for financial gain with the intent of deceiving the consumer regarding what is actually in the package [ 155 ]. These acts of fraud have increased overtime as different parties such as manufacturers, co-packers, distributors, and others along the chain of distribution involve in the national or international trade. Mislabeling leads to cross-contamination, poor food quality, degradation of nutrients, and even adverse effects on human health, serious financial, and legal consequences [ 69 , 154 ].

In this systematic review, we identified that GM foods are becoming an increasing public health risk. The included full-text articles reported that a wide range of health consequences associated with consumption of GM foods [ 83 – 86 ]. Possible hazards of GM foods include the potential for pleiotropic and insertional effects (silencing of genes, changes in their level of expression or, potentially, the turning on of existing genes that were not previously being expressed), effects on animal and human health resulting from the increase of anti-nutrients, potential effects on human health resulting from the use of viral DNA in plants, possible transfer of antibiotic-resistant genes to bacteria in gastrointestinal tract, and possible effects of GM foods on allergic responses [ 156 – 161 ]. However, the health effects of genetically modified foods are still debatable. Different lab-animal-based studies reported that there is no safety difference between GM and non-GM foods or the health concerns are not confirmed well [ 162 – 165 ]. Some others argue that despite the advances in food crop agriculture, the current world situation is still characterized by massive hunger and chronic malnutrition, representing a major public health problem. Biofortified GM crops have been considered an important and complementary strategy for delivering naturally fortified staple foods to malnourished populations [ 164 ].

This review revealed that foods past their use-by dates in the food market are major threats for consumers. This malpractice is more common in less developed countries and rural markets [ 36 , 67 , 87 – 90 ]. Growth of microorganisms in expired foods is very common. Most of these microorganisms are pathogenic and some microorganisms produce toxic substances as they develop [ 36 , 121 , 166 – 169 ].

Limitation of the review

We entirely relied on electronic databases to search relevant articles. We did not include articles available in hard copy. We believed we could get more relevant articles if we had access to hard prints.

This systematic literature review identified common food safety–related public health risks in the food market. The results imply that the local and international food marketing continues to have significant impacts on health of the public. The food market increases internationalization of health risks as the food supply chains cross multiple national borders. Therefore, effective national food control systems are essential to protect the health and safety of the public. Countries have to implement and enforce risk-based food control strategies. Countries need also assure the safety and quality of their foods entering international trade and ensure that imported foods conform to national requirements. Moreover, food producers and retail sectors have to respect the national food safety guideline and have to work to protect the safety of their customers Additional file 1 .

List of full text articles included in the review

The full text articles included in this review are attached as a supplementary file (see supplementary file).

Supplementary information

Acknowledgements.

The author would like to thank The Ohio State University Health Science Library for helping him to access different electronic databases.

Abbreviations

Author’s contribution

The authors read and approved the final manuscript.

The author of this review did not receive funds from any funding institution.

Availability of data and materials

Ethics approval and consent to participate.

Not applicable for systematic reviews.

Consent for publication

This manuscript does not contain any individual person’s data.

Competing interests

The author declares that he has no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information accompanies this paper at 10.1186/s12199-019-0825-5.

In response to increased awareness of foodborne disease in developing countries, the Food and Nutrition Technical Assistance Project (FANTA) Project conducted a literature review to investigate how donors, partners, and programs can reduce this burden at the household level. A full report and a technical brief document interventions to improve food hygiene, identify key actions to prevent foodborne illness, identify research and programming gaps in food hygiene, and identify short- and long-term programmatic recommendations.

Food safety and hygiene: A review

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HACCP: A Practical Approach

Evaluation of food safety problems based on the fuzzy comprehensive analysis method, economic impact of temperature control during food transportation—a covid-19 perspective, hazard analysis critical control point evaluations: a guide to identifying hazards and assessing risks associated with food preparation and storage: frank l. bryan, world health organisation, geneva, 1992, 72 pp, isbn 92-4-154433-3, swfr 15, food-related illness and death in the united states., state of the world’s children, recommended international code of practice : general principles of food hygiene, methodological evaluation of method for dietary heavy metal intake., hazard analysis and critical control point principles and application guidelines, related papers (5), haccp - its need and practices, case studies in food microbiology for food safety and quality, food safety, hazard analysis and critical control point and the increase in foodborne diseases: a paradox, a review of the needs and current applications of hazard analysis and critical control point (haccp) system in foodservice areas, reducing foodborne disease: meeting the food standards agency’s targets, trending questions (3).

Food hygiene plays a crucial role in preventing foodborne illnesses and ensuring food safety, ultimately safeguarding individuals' health from contamination-related diseases and potential hazards.

- Food hygiene practices prevent microbial contamination throughout food production chain. - Lack of food hygiene can lead to foodborne illnesses and death.

- Ensures food safety from production to consumption, preventing foodborne illnesses. - Prevents contamination at all stages of food handling and preparation.

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Good Manufacturing Practices for the 21st Century for Food Processing (2004 Study) Section 2: Literature Review of Common Food Safety Problems and Applicable Controls

August 9, 2004

Table of Contents

This section presents ERG's literature review of preventive controls for microbiological, chemical, and physical food safety problems in the food processing industry. Microbiological safety hazards cause most of the foodborne illnesses and include pathogenic bacteria, viruses, and parasites. Historically, pathogenic bacteria have been the most prevalent food safety hazard, with viral cases following closely behind according to the most recent CDC report on the etiology of foodborne illness (CDC, 2004). Chemical food safety hazards vary widely, but the most common problems cited in the literature include contamination with pesticides, allergens, and natural toxins, including scrombotoxins found in fish and mycotoxins found in crops. Foreign objects, or physical safety hazards, are the least likely to affect large numbers of people and usually are easily recognized.

Many of the microbiological food safety problems discussed in the literature can potentially be addressed by good manufacturing practices (GMPs) codified in 21 CFR 110, such as proper employee hygiene, adequate training, and effective cleaning and sanitizing of the manufacturing equipment and environment. For example, niche environments, which are sites within the manufacturing environment that can harbor bacteria, are a significant cause of post-processing contamination but difficult to reach with average cleaning and sanitizing procedures. Food plants that put in a greater than average effort must identify and eliminate niches by taking apart equipment in order to minimize the risk of post-processing contamination from niche environments. Others take an even more stringent approach by applying a post-package pasteurization method, virtually eliminating the risk of post-processing contamination due to niche environments.

Many chemical food safety problems are also addressed by following good manufacturing practices, such as pest control and proper storage. The rigor of the controls in place varies by plant, however. Further, some food safety problems, such as allergen control, may be better addressed by a Hazard Analysis and Critical Control Point (HACCP) plan in addition to GMPs. Physical hazards may also be better controlled by a HACCP plan. Controls may include foreign body detection systems, such as metal detectors, in addition to putting preventive measures in place.

Table 2-1 summarizes the range of problems associated with each type of hazard as identified in the literature. The following three sections provide a more detailed overview of each hazard and the preventive controls to address each problem, as noted in the literature. Each section also includes a summary flowchart that highlights the potential problems, the relevant CFR section or guidance that addresses each problem, the industry/product covered, and the types of preventive controls typically recommended to eliminate or minimize the type of food safety hazard risk posed. Finally, Section 2.4 discusses other issues to consider when evaluating food safety controls, in addition to GMPs.

2.1 Microbiological Safety

The microbiological safety hazards include pathogenic bacteria, viruses, and parasites. Some of the problems that lead to the contamination of food with these microorganisms at the processor level can be easily remedied with improved employee training programs and effective hygienic practices. Others are more difficult to control, such as post-processing contamination with Listeria monocytogenes , a pathogen that is ubiquitous in the processing environment.

Inefficient hygienic practices among employees . Employee hygiene is paramount to plant sanitation and is one of the leading causes of food contamination (Higgins, 2002). One of the challenges that food processors have to overcome is how to motivate employees to comply with hygienic practices. Training is one step in the process, but is often not enough to ensure employee compliance. Companies have adopted several aids to ensure employee compliance. For example, Atlanta's Buckhead Beef Company requires workers to key in their Social Security Numbers to activate the hand sanitizer dispensers on the plant floor. The company then uses the collected data to impose financial reprisals on employees found to be deficient in hand-sanitizing practices. Other controls include a sensor-equipped towel that prevents the cross-contamination that can occur with hand cranks. These units also count the number of towels dispensed. A signal dispenser that beeps when users have washed their hands sufficiently is also available to ensure adequate hand-washing time.

Language barriers . Current training programs, even those that include Spanish signage and instructional manuals, can be inadequate if the first language of plant employees is one other than English or Spanish. Even Spanish training materials can be problematic due to dialectical differences in translations. Some industry experts therefore recommend a picture-and-symbol approach to training to overcome language barriers (Higgins, 2002).

Table 2-1. Range of Processor-Level Problems by Type of Food Safety Hazard Posed

Ineffective training of employees . Although effective training is crucial to ensuring that sanitation standards are met, it is not clear that current training methods are sufficient. In the third Annual Best Manufacturing Practices Survey conducted by the Food Engineering magazine in 2002, a panel of food manufacturing professionals rated employee training as the lowest among all food safety measures in terms of effectiveness (Gregerson, 2002). Employee training that companies conduct may be too generic. For example, external consultants may not be familiar enough with a plant's operations and requirements to give effective advice. Other impediments to effective training might include training the wrong people, not training enough people, or not providing enough training (Blackburn and McClure, 2002).

Biofilms . Biofilms occur when bacteria form a slime layer upon a surface and provide an environment for pathogens to proliferate. The adhesion of pathogenic bacteria to a biofilm is a food safety hazard because the biofilm can detach and become a significant source of food contamination. Cleaning to remove biofilms prior to sanitation is often sufficient to prevent this problem. However, studies have shown that attached bacteria may survive conventional cleaning methods (Austin and Berferon, as cited in Stopforth et al, 2002). Adequate cleaning prior to sanitizing is therefore paramount to controlling this problem. Further, coating drains and equipment parts with antimicrobial material can counteract biofilms although it does not eliminate the need for proper cleaning and sanitizing (Higgins, 2003).

Niche environments . Niche environments are sites within the manufacturing environment where bacteria can get established, multiply, and contaminate the food processed. These sites may be impossible to reach and clean with normal cleaning and sanitizing procedures. Examples include hollow rollers on conveyors, cracked tubular support rods, the space between close-fitting metal-to-metal or metal-to-plastic parts, worn or cracked rubber seals around doors, and on-off valves and switches (Tompkin, 2002). Tompkin (2002) provides an extensive list of potential niches. Manufacturers must identify and eliminate niches. Microbiological sampling of the environment and equipment can detect a niche. Third-party validation of test results might be useful to further establish confidence in environmental sampling results. Further, sanitary equipment design can help prevent niches (AMI, 2003). Proper maintenance to keep equipment parts from providing potential niches is also essential.

Plant renovations . Outbreaks of listeriosis have been linked to environmental contamination of food caused by plant renovations (FDA/CFSAN, 2001a). While no data were identified in the literature on this issue, plant renovations are likely to require revisions in standard operating procedures (SOPs) to prevent contamination due to changes in processes.

Ineffective use of cleaning agents and disinfectants . Different cleaning agents vary in their ability to remove different soil types (Blackburn and McClure, 2002). Thus, the correct choice of cleaning agent is essential to ensure effective cleaning in a food processing facility. The efficacy of disinfectants is dependent on microbial species, pH, presence of biofilms, temperature, concentration, and contact time (Stopforth et al., 2002; Blackburn and McClure, 2002). Stopforth et al. (2002) found that commonly used disinfectants were not as effective as desired, possibly due to inadequate pre-cleaning steps. While there were no examples in the literature of plants having problems with this issue, the potential for ineffective sanitation is clearly present. Food manufacturers should always confirm the efficacy of their cleaning and disinfection programs with tests from the supplying companies or in-house trials (Blackburn and McClure, 2002).

Lack of sanitary equipment design . Good hygienic design of equipment prevents or minimizes microbiological contamination of food. The materials used for food processing equipment should be easily cleanable. As noted earlier, niche environments are known sources of pathogens; surfaces also deteriorate with age, and this abrasion makes cleaning more difficult (Blackburn and McClure, 2002). For cleaning and sanitation to be effective, all parts of the equipment should be readily accessible. Another way to improve equipment hygiene is to use antimicrobial coatings on equipment parts (Higgins, 2003).

Reactive rather than routine/predictive maintenance . In the Best Manufacturing Practices Survey conducted by Food Engineering magazine in 2001, 56 percent of respondents reported having routine preventive programs (Gregerson, 2002). Only 8.5 percent of respondents noted having predictive maintenance programs; the remaining respondents described their programs as reactive in nature, i.e., "run it 'til it breaks." Reactive maintenance can result in food contamination before a failure is identified. Niches can develop or controls can become defective in processing equipment that is not routinely maintained. For example, in 1994, a Listeria monocytogenes outbreak was linked to the use of defective processing equipment in the production of chocolate milk (FDA/CFSAN, 2001a).

Ineffective application of sanitation principles . It may be difficult for a food processor to apply sanitation principles consistently and effectively to each batch of product. Food processors have found that improving the effectiveness of sanitation principles is dependent on using redundant processing controls (FDA/CFSAN, 1999c). Validation of cleaning processes may also be necessary. Automation that makes it unnecessary for humans to conduct the cleaning, such as robotic spray washers, may also improve sanitation. The extent to which these practices are used in the industry is unclear and should be explored with industry experts.

Internalization of pathogens in fruit . Fruit is usually contaminated by direct or indirect contact with animal feces. Studies have shown that pathogens can infiltrate fruit through damaged or decayed areas or through the flower end of the fruit (FDA/CFSAN, 1999a; FDA/CFSAN, 1999b; FDA/CFSAN, 1999c). While employing best control practices--such as not using dropped fruit, removing damaged fruit, and washing/brushing fruit prior to processing--minimizes these risks, the problem can only be controlled with some certainty by a kill step, such as pasteurization. Other possible controls are listed in the FDA Report of 1997 Inspections of Fresh, Unpasteurized Apple Cider Manufacturers and listed again in the annotated bibliography.

Contamination of raw materials . Many pathogens, like E. coli and Salmonella, enter the food processing environment via raw materials contaminated with those pathogens. A number of studies have shown that methods currently in place to prevent this are not sufficient (FDA/CFSAN, 1999a;

FDA/CFSAN, 1999b; FDA/CFSAN, 1999c; Riordan et al., 2001; Tilden et al., 2002). Raw material contamination can affect any industry, but is more common in industries that use animal-derived products or products at risk of cross-contamination by animal feces. There are numerous preventive controls available to address the hazard. Some controls minimize the risks of raw material contamination (i.e., ensuring that raw material suppliers comply with good agricultural practices) and others (i.e., irradiation, pasteurization) involve a kill-step to eliminate any pathogens.

Post-processing contamination . Products can also be contaminated if the post-processing environment, utensils, or equipment have been contaminated with a pathogen. This issue is especially relevant to the pathogen Listeria monocytogenes , due to its hardiness and pervasiveness in the environment. Effective controls against post-process contamination include eliminating the pathogen from the post-processing environment by using environmental sampling to eliminate niches, effective sanitation, and various in-package pasteurization methods. Use of preservatives, such as nisin, to slow down the growth of Listeria monocytogene are also becoming more common.

Figure 2-1: Microbiological Safety Problems, Related CFR Section or Guidance, Industries Affected, and Sample Preventive Controls Suggested

2.2 Chemical Safety

Chemical safety hazards include intentionally added chemicals (e.g., allergens), unintentionally added chemicals (e.g., cleaners and solvents), and natural toxins (e.g., mycotoxins). Chemicals can also contaminate food through corrosion of metal processing equipment/utensils and residues of cleaning chemicals left on processing equipment. Further, adding too much of an approved ingredient, such as a vitamin in vitamin-fortified products, may compromise the safety of foods.

Raw material contamination with pesticides . FDA has found that roughly 1 percent of sampled domestic produce has pesticide residue in violation of EPA standards (FDA/CFSAN, 2002). While the incidence of contamination is low, consumers remain concerned about pesticide residues. Aside from washing and testing the produce, manufacturers can select produce from organic suppliers to avoid raw material contaminated with pesticides. Other alternative farming systems, such as low-input sustainable agriculture (LISA) and integrated pest management, are also control options at the farm level (Moulton, 1992). These systems, which use much less pesticide than conventional agricultural systems, rely on biological, chemical, cultural, and physical principles and tools to control pests throughout the farming operation. Other preventive control options may include genetic engineering with resistance against pests or developing safer chemicals (Moulton, 1992).

Indiscriminate spraying of facilities against pests. Chemicals can contaminate food if pesticides against insects and rodents are used indiscriminately in a processing facility. Therefore, food experts generally recommend that pest control be performed only by professionals to avoid residues in food (Folks, 2001).

Mistaken identity of pesticides . Food can become contaminated with pesticides if pesticide container labels are misread or when products are stored in containers that have had another use. The best way to control the risk of mistaken identity is to store pesticides away from food ingredients, keep an inventory of pesticides, and store the products in their original containers (Tybor, 1990; Folks, 2001; Bryan, 1997).

Spillage of pesticides or other chemicals . Pesticides should be handled like poisons to avoid potential spillage. Storing chemicals away from food and packaging materials will minimize accidental spillage of pesticides and other chemicals (Tybor, 1990). Further, processors should only use food-grade lubricants and greases in manufacturing.

Corrosion of metal containers/equipment/utensils . Metal poisoning can occur when heavy metals leach into food from equipment, containers, or utensils. When highly acidic foods (e.g., citrus fruits, fruit drinks, fruit pie fillings, tomato products, sauerkraut, or carbonated beverages) come into contact with potentially corrosive materials, the metals can leach into the food (Tybor, 1990). One solution to the problem is to use appropriate, non-corrosive materials in food processing.

Residue from cleaning and sanitizing . If equipment and other food handling materials are not rinsed well, then residue from detergents, cleaning compounds, drain cleaners, polishers, and sanitizers can contaminate a food product. This problem can best be controlled by properly training personnel about cleaning and sanitizing (Folks, 2001; Tybor, 1990).

Accidentally adding too much of an approved ingredient . Some substances, such as preservatives, nutritional additives, color additives, and flavor enhancers, are intentionally added to food products. But adding an approved ingredient in inordinate amounts by accident--such as adding too much nitrite to cured meat--can result in a toxic product (Bryan et al., 1997). Thus, Tybor (1990) recommends that nitrite be stored in a locked cabinet and weighed and bagged separately before being added to any product. Nutritional safety issues can also arise when product labels' nutrition information is incorrect. Thus, it can be dangerous to public health when too little or too much of a specified nutrient is added. For example, malnutrition can occur if infant formula does not deliver the expected nutrient content during its shelf life. Due to the risk involved, infant formula quality control procedures and labeling requirements are addressed outside of GMPs in 21 CFR 106 and 107, respectively. There are also many examples of nutritional food safety issues arising when too much of a nutrient gets added to a product unintentionally. For example, some vitamins that are added to fortified foods (such as Vitamin A) are known to be toxic at high doses. And iron, a necessary dietary component, can cause severe illness and death if too much is ingested. Controlling chemicals by keeping an inventory of additives minimizes the occurrence of this type of contamination (Folks, 2001).

Natural toxins . Food can be contaminated with naturally occurring chemicals that cause disease. Toxins such as mycotoxins (discussed further below) and marine toxins are naturally produced under certain conditions. Given that these toxins generally occur in raw materials, especially crops and seafood, manufacturers should require suppliers to certify hat the products they purchase are free from natural toxins.

Cross-contamination with allergens on production lines . A product can become cross- contaminated with allergens on the production line. To minimize the risk of cross-contamination, equipment must be cleaned and sanitized to remove all traces of allergens when the next run includes product that should not contain allergens (Minnesota Department of Agriculture, 2003). Wash-down techniques may need adjustment to ensure that they remove allergens as well as pathogens (Higgins, 2000). Rinsing with water only or only cleaning at the end of the day is not adequate (FDA/CFSAN, 2001a). Some equipment may need to be disassembled to be cleaned. The cleaning process should be verified by visual inspection. Enzyme-linked immunosorbent assay (ELISA) tests can also help verify cleaning procedures (Deibel et al., 1997; Morris, 2002). Manufacturers may choose to physically separate lines for allergen- and nonallergen-containing products (Morris, 2002). This may be too costly for most plants; scheduling longer production runs to minimize changeovers, with allergen-containing product runs scheduled at the end of the day, may be a more suitable alternative (Deibel et al., 1997; FDA/CFSAN, 2001b; Floyd, 2000; Gregerson, 2003; Minnesota Department of Agriculture, 2003; Morris, 2002). Crossover points on production lines, including conveyor belts that transport products, should be enclosed to prevent cross-contamination. Physical detachments and lockouts can be used for equipment common to allergen- and nonallergen-containing foods (Deibel et al., 1997). Maintenance tools should be color-coded to prevent cross-contamination (FDA/CFSAN, 2001b; Morris, 2002). Allergenic materials should be stored separately from nonallergenic materials, with dedicated utensils and containers. Putting all of the ingredients for a specific batch on a pallet before taking them to the processing area, or "staging," will also minimize the risk of cross-contamination. Line clearance, such as removing all the ingredients from the production area and checking for cleanliness, can also help prevent cross-contamination (Floyd, 2000). Product can also be tested for the presence of allergens, although this does not appear to be a common industry practice (FDA/CFSAN, 2001a). Finally, allergens should be evaluated as part of a hazard analysis, and a HACCP plan or similar approach can be taken to identify process areas that are at high risk for contamination with allergens (Morris, 2002).

Raw material contamination with allergens . When controlling a production process for allergens, manufacturers must maintain a close working relationship with suppliers of raw materials. The ingredient specification should provide assurance that the product is allergen free (Deibel et al., 1997; FDA/CFSAN, 2001c). Manufacturers should also obtain full ingredient lists from their suppliers (Deibel et al., 1997; Gregerson, 2003). Reconditioned ingredients and oils should not be purchased (Minnesota Department of Agriculture, 2003). The manufacturer should also audit suppliers each year to determine other products that are run on the same production line, whether any allergenic processing aids or rework have been used in the product, and whether any contamination from other common equipment could have occurred (Gregerson, 2003). A training program may be necessary to educate suppliers about allergen control, especially if suppliers have not implemented an allergen control plan (Deibel et al., 1997, Minnesota Department of Agriculture, 2003).

Contamination with allergens by utilization of rework . Proper use of rework is essential to prevent contamination of product with allergens. A documented rework plan should be available. Rework areas, equipment, and containers must be clearly identified and documented, as well as the rework itself (Deibel et al., 1997; Gregerson, 2003). This can be done through the use of color tags, plastic liners, or bar coding.

Not declaring an allergen on labeling . Unavoidable product contamination with allergens may occur if it is impossible to verify that all residue has been removed from a line or if other controls cannot be put in place (Floyd, 2000). A good manufacturing practice includes reviewing the labeling to ensure that the allergen is declared. However, a study of inspections conducted by FDA/ CFSAN (2001a) indicated that many firms do not have label review policies. Further, a large percentage of these manufacturers had undeclared allergens in their products. Controls to prevent this problem can include removing old label and packaging inventories from plants, verifying labels by scanning bar codes, and conducting label audits (FDA/CFSAN, 2001b; FDA/CFSAN, 2001c; Minnesota Department of Agriculture, 2003).

Older equipment . Effective cleaning is paramount to controlling allergen contamination. Older equipment, however, may not be designed to verify cleaning with a visual inspection (Deibel et al., 1997). As noted in the section on microbiological issues and controls, all parts of the equipment should be readily accessible and visible for cleaning and sanitation to be effective. Further, equipment surfaces should not harbor allergens. Gregerson (2003) reports one such case in which cross-contamination with allergens occurred due to the surface nicks on the processing table. Thus, sanitary equipment design is necessary to ensure proper removal of allergens from equipment.

Infestation of mycotoxins due to drought . Toxigenic fungi, or mycotoxins, are found primarily in foods of plant origin, although they can also pass through the food chain in milk and meat. Drought can encourage the growth of mycotoxins in certain crops. For example, drought stress can cause aflatoxin, a type of mycotoxin, to grow in corn and treenuts (Moss, 2002). Drought can be minimized through adequate irrigation schedules (Park et al., 1999). Thermal and chemical treatments are also available for use on crop that is already affected by mycotoxins (Park et al., 1999). Thermal inactivation, however, is not effective on certain types of mycotoxins, such as aflatoxin. Chemical treatments, such as ammoniation and activated carbons and clays, are other possible controls (Boutrif, 1999; Horne et al., 1989; Park et al., 1999; Suttajit, 1989).

Infestation of mycotoxins due to damage . Insect damage is associated with high levels of mycotoxin infection, as is mechanical damage from harvesters (Boutrif, 1999; Moss, 2002; Park et al., 1999). Diseases, such as ear rot in corn, also cause damage that leaves the crop susceptible to mycotoxin infestation (Moss, 2002). Delayed harvesting can also make crops more susceptible to disease due to higher moisture levels (Park et al., 1999). Damage to the product, whether through insect feeding or mechanical harvesters, provides a potential entry point for the mold that produces the mycotoxin. Controls available include pest management to prevent insect damage, breeding cultivars that are resistant to pest damage, timely harvesting, hand picking or electronic sorting to remove damaged crops, and thermal or chemical treatment as noted above (Boutrif, 1999; Moss, 2002; Park et al., 1999; Suttajit, 1989). Possible biological control of insects and diseases in the field is also being investigated (Moss, 2002).

Infestation of mycotoxins due to moisture/heat during storage . Post-harvest storage that protects the product from heat and moisture is essential to prevent mycotoxin infestation (Boutrif, 1999). Grains should be dried as soon as feasible, and storage under modified atmospheric conditions is desirable (GASCA/CTA, 1997). Products should be dried rapidly to less than 10 percent moisture (Park et al., 1999). Products can also be sampled for mycotoxins during storage (Boutrif, 1999). Methods include visual inspection with black light, ELISA tests, and complex laboratory analysis using high-pressure liquid chromatography (Horne et al., 1989). While prevention with proper storage conditions is the best way to control mycotoxin infestation, thermal and chemical inactivation, as described earlier, can control any mycotoxins that do form under storage.

Patulin production in apples . Patulin is a mycotoxin that is produced by a number of molds associated with fruit spoilage (Bisessur et al., 2001). Control methods often used in the production of apple juice include using tree-picked apples, culling apples, washing apples, charcoal treatment, chemical preservation using sulfur dioxide, gamma radiation, fermentation, trimming of fungus-infected apples, and clarification methods (Bisessur et al., 2001; Jackson, et al., 2003).

Figure 2-2: Chemical Safety Problems, Related CFR Section or Guidance, Industries Affected, and Sample Preventive Controls Suggested

2.3 Physical Safety

Materials that do not belong in food, like glass or metal, cause physical safety hazards. A physical safety hazard is any extraneous object or foreign matter in food that can cause injury or illness in the person consuming the product (Folks, 2001). Rocks, metal, wood, and other objects are sometimes found in raw ingredients. Further, contamination can occur during transport, processing, and distribution of foods due to equipment failure, accidents, or negligence (Institute of Medicine/National Research Council, 1998). Separation equipment should be used to separate the foreign bodies from the product. Detection methods include metal detectors, x-ray machines, and optical systems (Wallin and Haycock, 1998).

Foreign matter in raw materials . Sources of foreign matter in raw materials can include nails from pallets and boxes, ingested metal from animals, harvesting machinery parts, elements from the field, veterinary instruments, caps, lids, closures, and more (Wallin and Haycock, 1998). Mechanical harvesters will often collect more than the product. Processors can include separation equipment, such as destoners, air cleaners, magnets, screens, sieves, traps, scalpers, and washers as part of their production lines. For example, grain processors use four screens to remove foreign materials (Stier, 2001). Foreign matter in raw materials can be controlled with raw material inspections and vendor certifications or guarantees from suppliers. X-ray technology is also available to examine incoming material (Folks, 2001).

Poorly maintained equipment and lines . Pieces of equipment can break off and enter food products during processing if equipment is poorly maintained. Routine or preventive maintenance and other periodic checks of equipment can minimize the risk from this safety issue. Risk is further minimized with the use of metal detectors and x-ray machinery. Proper calibration of equipment and minimizing contact between pieces of machinery is also helpful (Folks, 2001; Stier, 2001).

Lighting fixture/other glass breakage . Glass can be controlled by having a glass breakage policy, such as throwing away all food and containers within 10 feet of the incident (Stier, 2001). Light fixtures can be protected so that if they break, the glass does not spill out (Folks, 2001). Other controls include examining of empty glass containers visually or cleaning a container with water or compressed air and inverting the container to remove any shards. Capping equipment should be properly calibrated and lines should be monitored for evidence of glass breakage. X-ray technology can also be helpful in identifying glass pieces in food (Olson, 2002).

Human factors . Production line workers can be a major source of contamination. For example, jewelry can fall off or break, fingernails can break, and pens can fall into food. Jewelry removal is required under GMPs. If pens are metallic, a metal detector can detect them. Production workers' fingernails should be cut short and gloves should be worn under certain processing conditions.

Introduction of foreign matter during storage . Pests can enter products during storage, leaving remnants behind. Effective pest control is the solution. It can include preventive measures such as filling in all non-functional openings in a building; fully sealing doors, windows, and vents; protecting intake points with filters or grills; and protecting drains and other facility intakes and exits. Professional extermination is needed once pests have established. UV light traps can also be used, although they need to be designed to prevent further contamination from the tray that collects the insect remains (Wallin and Haycock, 1998).

Figure 2-3. Physical Safety Problems, Related CFR Section or Guidance, Industries Affected, and Sample Preventive Controls Suggested

2.4 Other Considerations

There is a wide range of issues related to the safety and wholesomeness of food in addition to GMPs. These should be considered in addition to the problems identified at the food processing level when evaluating the effectiveness of food GMPs. They include the following and are discussed in more detail below:

• New trends contributing to foodborne illness,
• Most common causes of foodborne illness,
• High-risk foods, and
• Role of market incentives

New trends contributing to foodborne illness . A number of recent trends contribute to the incidence of foodborne illness. For example, in recent years, there has been an increase in consumer purchases of ready-to-eat (RTE) foods, made popular by the busy lifestyles of people today. Many cases of foodborne illness are caused by RTE foods that were cross contaminated with pathogenic bacteria. Since RTE foods are generally not cooked prior to consumption, the likelihood of foodborne illness is high when these products are contaminated.

Another alerting trend is the increase in new and drug-resistant infectious foodborne agents since the GMPs were last revised. Listeria monocytogenes and Cryptosporidium are examples of newly recognized agents that has been of great concern in the last few years. Some pathogens have also shown antimicrobial resistance, such as Campylobacter jejuni and Salmonella typhimurium DT104. There is also evidence of well-known viruses, such as hepatitis A and Salmonella entertidis , appearing in new foods like produce (Institute of Medicine/National Research Council, 1998). The evolution of these new agents and new vehicles transmitting known pathogens makes prevention of food contamination a moving target for those in charge of ensuring food safety.

The aging population in the United States is another trend of concern: this group is at higher risk for developing illness from contaminated food. As the baby boomer generation enters their retirement years, one can expect this trend to become even more pronounced. These and other changes over time significantly increase the risk of contracting foodborne illness, necessitating a new look at food GMPs in light of these factors.

Most common causes of foodborne illness . Pathogenic bacteria are the most commonly reported agents of foodborne illness, closely followed by viruses (CDC, 2004). Further, most reported cases of foodborne illness are attributable to poor handling at the home or at retail food establishments rather than failures at the food processing level (CDC, 2000). It is not possible to determine (with certainty) the cause of foodborne illness in roughly 50 percent of all foodborne illness cases. Moreover, many foodborne illness cases go unreported.

High-risk foods . The level of risk to public health varies by type of food. Some food products, such as refrigerated RTE foods, have a higher risk of being contaminated by pathogenic bacteria (e.g., Listeria monocytogenes ) than others, such as frozen RTE products (NFPA, undated). Further, FDA/CFSAN (2001a) has also shown in their Listeria monocytogenes risk assessment that the level of risk varies for different types of RTE foods. Therefore, from a risk perspective, indiscriminate application and/or recommendation of controls and policies may unduly burden manufacturers as well as the FDA and in some cases lead to inadvertent outcomes. For example, under the current zero-tolerance policy of the Food Safety and Inspection Service (FSIS) for Listeria monocytogenes , when a plant's testing program detects Listeria monocytogenes on plant equipment, the plant is required to recall all product produced on that line during the period of contamination. FSIS may also obtain test data if a plant has a suspected problem with Listeria monocytogenes. While there is a consensus in the industry that aggressive environmental monitoring is essential to controlling Listeria monocytogenes, Tompkin (2002) argues that the zero-tolerance policy discourages, rather than encourages, the RTE food industry from confirming the presence of Listeria monocytogenes in their environmental sampling programs. Many companies may conduct less (rather than more) aggressive environmental monitoring and product testing to avoid regulatory conflict.

Role of market incentives . FSIS is required to inspect meat and poultry slaughtering and processing plants carcass by carcass. As a result of the continuous inspection requirements, FSIS's inspection budget is four times that of FDA (Institute of Medicine/National Research Council, 1998). The lack of inspection resources may contribute to less enforcement of food safety statutes under FDA's jurisdiction. Given the lack of resources, it is important to evaluate the role of other, non-regulatory incentives that encourage food safety. For example, food safety problems can be a major liability for manufacturers of brand name products. If food is said to be unsafe, these manufacturers can face a huge public relations crisis that will negatively affect their bottom line (Ballenger and Ollinger, 2003). Consumers may also shun an entire category of food (Institute of Medicine/National Research Council, 1998). Most producers of branded products, therefore, invest more to ensure the safety of the food they produce. Grocery stores and wholesalers also require strict food safety controls from their suppliers to protect their reputations. For example, USDA's Economic Research Service (ERS) researchers recently surveyed 1,000 slaughtering plants and found that contractual agreements covering food safety standards result in higher levels of food safety with regards to equipment, testing, dehiding, sanitation, and operating procedures (Ballenger and Ollinger, 2003). A similar study for FDA-regulated products may yield comparable results.

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FDA/CFSAN. 2001a. Draft Assessment of the Relative Risk to Public Health from Foodborne Listeria monocytogenes Among Selected Categories of Ready-to-Eat Foods . January.

FDA/CFSAN. 2001b. Seafood HACCP Alliance HACCP Training Curriculum Manual: Hazards -- Biological, Chemical, and Physical (Chapter 2) . November.

FDA/CFSAN. 2001c. Analysis and Evaluation of Preventive Control Measures for the Control and Reduction/Elimination of Microbial Hazards on Fresh and Fresh-cut Produce . September 30.

FDA/CFSAN. 1999a. Potential for Infiltration, Survival, and Growth of Human Pathogens within Fruits and Vegetables . November.

FDA/CFSAN. 1999b. Preliminary Studies on the Potential for Infiltration, Growth, and Survival of Salmonella enterica Hartford and Escherichia coli O157:H7 Within Oranges . November.

FDA/CFSAN. 1999c. Report of 1997 Inspections of Fresh, Unpasteurized Apple Cider Manufacturers . January.

Floyd, Bruce M. 2000. Battling Allergen Contamination. Food Product Design. December.

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Jackson, Lauren S.,, Tina Beacham-Bowden, Susanne E. Keller, Chaitali Adhikari, Kirk T. Taylor, Stewart J. Chirtel, and Robert I. Merker. 2003. Apple Quality, Storage, and Washing Treatments Affect Patulin Levels in Apple Cider. Journal of Food Protection . Vol. 66, No. 4.

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ORIGINAL RESEARCH article

Foodborne disease hazards and burden in ethiopia: a systematic literature review, 1990–2019.

• 1 Animal and Human Health Programme, International Livestock Research Institute, Addis Ababa, Ethiopia
• 2 Animal and Human Health Programme, International Livestock Research Institute, Nairobi, Kenya
• 3 Department of Medical Biochemistry and Microbiology, Uppsala University, Uppsala, Sweden
• 4 Department of Clinical Sciences, Swedish University of Agricultural Sciences, Uppsala, Sweden
• 5 College of Veterinary Medicine and Agriculture, Addis Ababa University, Bishoftu, Ethiopia
• 6 Veterinary Public Health Institute, University of Bern, Bern, Switzerland
• 7 School of Environment and Natural Resources, Ohio State University, Columbus, OH, United States
• 8 Department of Environmental and Occupational Health, and Safety, University of Gondar, Gondar, Ethiopia
• 9 Animal and Human Health Programme, International Livestock Research Institute, Dakar, Senegal
• 10 Animal and Human Health Programme, International Livestock Research Institute, Ouagadougou, Burkina Faso
• 11 Natural Resources Institute, University of Greenwich, Chatham, United Kingdom

Background: Foodborne disease (FBD) affects millions of people each year, posing a health burden similar to malaria, tuberculosis or HIV. A recent World Bank study estimated the productivity losses alone attributed to unsafe food within Africa at $20 billion in 2016, and the cost of treating these illnesses at an additional $3.5 billion. Ethiopia faces multiple food safety challenges due to lack of infrastructure and basic pre-requisites for food safety such as clean water and environment, washing facilities, compounded by limited implementation of food safety regulations, and a lack of incentives for producers to improve food safety. A consolidation of our understanding and evidence of the source, nature and scale of FBD in Ethiopia is needed to inform policy and future research. We performed a Systematic Literature Review (SLR) of publications on FBD occurrence in Ethiopia including hazard presence and impact.

Method: The SLR followed Cochrane and PRISMA guidelines. We searched PubMed and CAB-Direct for relevant publications between 1990 and 2019 (inclusive). Observational studies and reviews were included. Two reviewers screened titles and abstracts, and retained publications were reviewed in full for quality and data extraction.

Result: In total 128 articles met the inclusion criteria. Most articles focused on the identification of biological hazards in food. High levels of microbial contamination in different food value chains were often found in the small, ad hoc , observational studies that dominated the literature. Raw milk (22/128, 17.0%) and raw beef (21/128, 16.4%) were the most studied food products. Foodborne (FB) parasites were often found at higher rates in food than bacterial and viral pathogens, possibly due to differences in ease of identification. High levels of bacterial contamination on the hands of food handlers were widely reported. There were no reports on the incidence of human FBDs or resulting health and economic impacts.

Conclusion: Our findings reflect existing concerns around food safety in Ethiopia. A lack of substantial, coordinated studies with robust methodologies means fundamental gaps remain in our knowledge of FBD in Ethiopia, particularly regarding FBD burden and impact. Greater investment in food safety is needed, with enhanced and coordinated research and interventions.

1. Introduction

Foodborne diseases (FBDs) are illnesses caused by contaminated, or naturally harmful, food. A foodborne (FB) hazard is anything present in food that can harm consumers' health. They are usually categorized as: biological hazards, which are pathogenic organisms and the toxins they produce; chemical hazards, which may be artificial or natural; and physical hazards, such as foreign objects in food ( Grace et al., 2018 ). The most comprehensive estimates of the health burden of FBDs in African countries are those provided by the World Health Organization (WHO) Foodborne Disease Epidemiology Reference Group (FERG) ( Havelaar et al., 2015 ), which estimated that FBD burden is comparable to that of malaria, HIV/AIDS or tuberculosis. Nearly all of this burden (98%) is borne by low-income countries and most of it (97%) is due to biological hazards ( Havelaar et al., 2015 ), with diarrheal disease agents being the most important contributor to overall FBD burden in African region E (which includes Ethiopia), followed by helminths and invasive bacteria ( Havelaar et al., 2015 ).

Accurate information on the health and burden associated with FBDs is critical for countries to guide food safety risk management strategies and to justify allocation of resources. The lack of reliable data from surveillance systems for FBD in low and middle income countries limits the ability to conduct risk-based food safety management. FBD burden is thought to be high in Ethiopia ( Pieracci et al., 2016 ; Keba et al., 2020 ; Belina et al., 2021 ; Mekonnen et al., 2021 ). Salmonella, Listeria monocytogenes, Escherichia coli (E. coli), Campylobacter spp. and Shigella are among the most common FB pathogens reported from Ethiopia and food-producing animals are the major reservoirs ( Belina et al., 2021 ). Reports of food poisoning outbreaks in Ethiopia are often linked to consumption of raw meat and milk ( Kassahun and Wongiel, 2019 ), However, cases of FB illnesses are underreported and are rarely investigated in detail ( Ayana et al., 2015 ).

Given the lack of knowledge around this vital topic, this Systematic Literature Review (SLR) was conducted to investigate the existing literature and collate the evidence on FB hazards in Ethiopia. The SLR did not look at specific pre-specified hazards or specific foods, but instead explored available literature on any FB hazards and any foods. This SLR is one early output of a portfolio of research projects 1 looking to improve understanding and control of FBD in Ethiopia. This review was used to inform these projects which then went on to examine FBD using various approaches, including modeling, molecular and field-based approaches.

2.1. Research question

This SLR aimed to inform the design of further studies by addressing the following research questions:

• What biological and chemical hazards have been identified in foods in Ethiopia?

• What is the prevalence (i.e., percent of contaminated products) and concentration of these hazards in foods in Ethiopia?

• What is the incidence of FBD and what is the associated health burden in Ethiopia?

2.2. Search strategy

We conducted an SLR following the methods suggested by the Cochrane Collaboration and the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement ( Moher et al., 2009 ). A comprehensive search on PubMed and CAB Direct was performed for articles published in English from the 1st of January of 1990 to the 30th of September 2019, inclusive. The search was done on 30th of September 2019. The search syntax with different search terms and Boolean Operators including the following search terms:

i. foodborne OR “food borne” OR food-borne OR “food safety” OR “food related” OR “food associated” OR “food derived” OR “food * illness” OR “food * disease * ” OR “food * intoxica * ” OR “food pathogen” OR “food * poison * ” OR “food * microb * ” OR “food * vir * ” OR “food parasit * ” OR “food * toxin.”

ii. AND Ethiop * .

The syntax was left broad and generic to capture all the literature covering the various aspects of interest (e.g., prevalence, impact, risk factors, and control). Inclusion and exclusion criteria are shown in Table 1 .

Table 1 . Inclusion and exclusion criteria (inclusion also require Ethiopia focus and published on or after 1st January 1990 but not after 30th September 2019).

2.3. Article selection process and quality assessment

Lists with the identified titles and abstracts were downloaded to an excel file and checked for duplicates using Mendeley ( https://www.mendeley.com/download-reference-manager/windows ). After the removal of duplicates, titles and abstracts were reviewed independently by two reviewers against the inclusion and exclusion criteria. All titles considered relevant by both reviewers were included; articles considered relevant by just one reviewer were reviewed by a third reviewer who made a final decision on article inclusion.

Full articles for the included titles were obtained, when available. The full articles were then subjected to a two-step review process; Articles were reviewed against (1) inclusion/exclusion criteria (as above) and (2) quality criteria. The quality criteria considered the paper's merit on five aspects: (1) selection of subjects, (2) study methods, (3) data analysis, (4) reporting of methods and results, and (5) reliability of results ( Table 2 ). Quality of the papers was rated as “Good” (scoring positively to all five quality criteria), “Moderate” (scoring positively in three or four of the quality criteria) or “Poor” (scoring positively in two or less of the quality criteria). However, an overall reviewer's overall impression could over-ride this rating. Poor-quality articles were excluded from data synthesis.

Table 2 . Quality criteria used for the quality review.

2.4. Data extraction and analysis

An excel template was designed to allow standardized data extraction by different reviewers ( Supplementary material ). Ten percent ( n = 13) of the full articles were systematically selected by dividing the total number of included articles by 13 so each 10 th article in the list was selected. Then theses were reviewed in parallel by two reviewers and outputs were compared to ensure the review process was standardized and comparable across reviewers. After standardization, the remaining articles were reviewed by a single reviewer. Given the large diversity of foods, organisms, and studies, it was not possible to conduct any meaningful meta-analysis.

3.1. Literature search

The database searches returned 760 and 244 records from PubMed and Cab Direct, respectively. Out of 519 unique articles, 307 were excluded at title and abstract review, and 3 were not available as full manuscripts ( Figure 1 ). From the remaining 209 full articles, 53 were excluded based on the inclusion/exclusion criteria and 28 based on the quality criteria. These were excluded due to poor scientific quality, mostly from biased selection of subjects, inappropriate data analysis and incomplete and/or inaccurate results.

Figure 1 . Flow chart of the process followed during the literature search for data extraction. The PRISMA flow diagram for the systematic review detailing the database searches, the number of abstracts screened, and the full texts retrieved.

Data was ultimately extracted from 128 selected articles.

3.2. Profile of the reviewed publications

Articles reported studies conducted in Oromia (42/128, 32.8%), Amhara (30/128, 23.4%), Addis Ababa (29/128, 22.6%), and Southern Nation Nationalities People (SNNP; 21/128, 16.4%) region. Few studies had been done in the other regions of the country. These were generally conducted in major cities and were not representative of all regional states ( Figure 2 ).

Figure 2 . Spatial distribution of regions and towns where the studies were conducted. Concentration of included studies over regions in Ethiopia with dark blue color indicating the highest number of articles and light blue representing fewer number of articles. The green circle dots indicating the towns where the studies were conducted.

Most articles were conducted in the capital city, Addis Ababa ( n = 29), followed by Debre Zeit ( n = 14), Awassa ( n = 9), Jimma ( n = 9), Go n dar ( n = 9), Bahir Dar ( n = 7), Haromaya ( n = 6), and Arba Minch ( n = 5) the location of well-established universities.

The number of articles relevant to the topic identified in our review increased over time ( Figure 3 ).

Figure 3 . Number of retained publications on FBD in Ethiopia between 1990 and 2019. The solid line shows actual number of articles published in a particular year.

Majority of the articles included in the review (119/128, 93%) focused on biological hazards and six articles looked at presence of chemical hazards in food. Among the 119 articles focused on biological hazards, 82/119 (68.9%) investigated presence of pathogens in food, 48/119 (40.3%) presence in human samples (stool and hand swab samples) and 19/119 (15.9%) in food environments (i.e., beef slaughterhouses, butcheries, and milk shops). While half of the articles studied one food item and one hazard, other half covered various hazards and/or various matrices. None of the selected studies covered incidence of FBD or FBD burden.

The majority ( n = 119, 92.9%) of the 128 papers examined the presence of bacteria ( n = 87, 73.11%), parasites ( n = 23, 19.33%), parasites and bacteria ( n = 7, 5.88%), fungal toxins ( n = 3, 2.52%), and viruses ( n = 1, 0.84%) using a cross-sectional design. Nearly half of the articles (47.3%) incorporated risk factor analysis. The majority of these publications ( n = 32, 55.7%) concentrated on evaluating risks from food handlers, feverish patients in healthcare facilities, and randomly selected school students or community members. Of the 128 retained articles, 72 (56.25%) were mainly focused on detecting pathogens in animal source foods. Bacterial contamination was reported in food products in beef, dairy, and poultry value chains while parasites were reported from apparently healthy food handlers, from stool samples of patients of health care facilities and to some extent (4/10,40%) in vegetable value chain.

Figure 4 below, describes number of articles reporting a particular bacteria species. 2

Figure 4 . Number of articles reporting a particular bacterial pathogen. Numbers are derived from every article investigating on the pathogens. That is an article may report more than one bacteria species.

In terms of parasitic hazards, Entamoeba, Giardia and Ascaris were the most commonly studied hazards ( Figure 5 ).

Figure 5 . Number of articles reporting a particular parasite. Numbers are derived from every article investigating on parasites. That is an article may report more than one parasite.

Study designs were often duplicated, to identify similar pathogens in similar populations. For example, most of the articles investigating pathogens on food handlers were conducted in student cafeterias of public universities. However, this may be more down to convenience, rather than intended inter-study comparability or the widespread use of established, optimized methods. The parasites investigated in these articles were similar, focusing on widely known FB parasites (e.g., Ascaris lumbricoides, Giardia lamblia, Entamoeba histolytica, Taenia spp. etc.).

3.3. Prevalence of foodborne hazards in the food value chains

Of the 82 articles that investigated hazards in food, the majority (64/82, 78%) focused on beef, dairy, vegetable poultry, and eggs value chains. Other value chains, such as camel, pork, fish, mutton, goat meat, fruits, crops, and street-vended locally made food (Sambusa, Bombolino, donat, and all doughnut variants) were the focus of 18 (22%) articles, the results of which are not reported on this paper ( Ashenafi, 1995 ; Muleta and Ashenafi, 2001 ; Molla et al., 2005 ; Abdel Gadir Atif et al., 2006 ; Hiko et al., 2008 ; Kibret and Tadesse, 2013 ; Dulo et al., 2015 ; Garedew et al., 2015b ; Eromo et al., 2016 ; Taye et al., 2016 ; Messele et al., 2017 ; Wendwesen et al., 2017 ; Tegegne et al., 2019 ) ( Supplementary material ). This section presents the literature findings per value chain or host, and per pathogen investigated. Pathogens are listed from the more frequently studied to the least, for each value chain or host.

3.3.1. Beef value chain

Close to one third of the articles investigated bacterial pathogens in the beef value chain (37/128, 28.9%).

3.3.1.1. Salmonella spp.

Eighteen articles (48.6%) reported information on Salmonella spp. Salmonella spp. contamination estimates ranged from 1 to 13% in raw beef samples collected from slaughterhouses in different parts of the country ( Molla et al., 2003 ; Alemu and Zewde, 2012 ; Hiko et al., 2016 , 2018 ; Edget et al., 2017 ; Wabeto et al., 2017 ; Ketema et al., 2018 ; Takele et al., 2018 ; Bersisa et al., 2019 ), and between 1 and 35% in raw meat samples from butcheries and retail shops ( Garedew et al., 2015b ; Hiko et al., 2016 , 2018 ; Edget et al., 2017 ). One study found 70% of fresh meat samples collected in butcher shops contaminated with Salmonella spp. ( Azage and Kibret, 2017 ). Four articles investigated foodborne pathogens in “ kitfo ,” a traditional Ethiopian raw (or lightly cooked) minced meat dish. About 9.8–12, 8, and 30% of “ kitfo ” samples in supermarkets, restaurants, and street vendors, respectively, were found to carry Salmonella spp. ( Muleta and Ashenafi, 2001 ; Molla et al., 2003 ; Ejo et al., 2016 ; Dagnachew, 2017 ). One article investigated Salmonella spp. in processed meat (mortadella) and found 0.8% positive samples ( Hiko et al., 2015 ).

3.3.1.2. Escherichia coli

Eleven articles (29.7%) reported contamination of beef with E. coli . About 5.5%−35.5% of raw beef samples from slaughterhouses,13.8% from restaurants, and 6%−29.4% from supermarkets were found contaminated with E. coli ( Hiko et al., 2015 ; Edget et al., 2017 ; Messele et al., 2017 ; Bedasa et al., 2018 ; Bersisa et al., 2019 ). Kumar et al. (2014) , reported that 62.5% of raw beef samples from butcher shops were positive for E. coli . Articles showed E. coli O157:H7 detection ranged from 0.8 to 9% in raw beef samples from slaughterhouses ( Hiko et al., 2016 ; Abdissa et al., 2017 ; Atnafie et al., 2017 ; Edget et al., 2017 ; Haile et al., 2017 ; Bedasa et al., 2018 ). The rate of contamination was higher in raw beef samples from butchers (2%−18%) ( Kumar et al., 2014 ; Hiko et al., 2016 ; Atnafie et al., 2017 ; Beyi et al., 2017 ). Escherichia coli O157:H7 was detected in raw beef and minced meat samples in (0%−3.1%) from retailer shops, restaurants, and supermarkets ( Beyi et al., 2017 ; Edget et al., 2017 ; Bedasa et al., 2018 ).

3.3.1.3. Mycobacterium bovis

Five articles (13.5%) looked at Mycobacterium bovis; postmortem inspection studies conducted in abattoirs reported 0.8%−10% of carcasses showing mycobacterial lesions. The sensitivity and specificity of the routine postmortem examination method was also reported to be lower compared to detailed inspection and culturing. Specifically, 0.7–7.5 and 2.7–19.4% of carcass negative in routine postmortem examination were found to be positive in detailed examination and by culture, respectively ( Asseged et al., 2004 ; Teklu et al., 2004 ; Demelash et al., 2009 ; Biffa et al., 2010 ; Aylate et al., 2013 ).

3.3.1.4. Listeria monocytogenes

In four (10.8%) articles investigating L. monocytogenes , 1.6%–−2.6% of raw and minced meat samples at retailer shops in Addis Ababa were found to be positive ( Molla et al., 2005 ; Gebretsadik et al., 2011 ; Derra et al., 2013 ; Garedew et al., 2015b ). 6.7%−12% of raw meat and minced meat samples from restaurants in Gondar showed contamination with L. monocytogenes ( Garedew et al., 2015b ).

3.3.1.5. Staphylococcus spp .

According to findings in three (8.1%) articles, up to 11.6% of samples from slaughterhouses and 19.7% from butchers were contaminated with Staphylococcus aureus ( Beyene et al., 2017 ; Adugna et al., 2018 ; Bersisa et al., 2019 ). Authors indicated continuous contamination throughout transportation from slaughterhouses to butcher shops ( Tolosa et al., 2016 ; Beyene et al., 2017 ). Beyene et al. (2017) reported 10.6% carcass swabs from slaughterhouse were positive for coagulase-negative Staphylococci in beef.

3.3.1.6. Shigella spp.

Three articles (8.1%) investigated Shigella spp. in beef. None of the beef samples (“kitfo” and raw meat) collected from restaurants and slaughterhouses were positive for Shigella spp. ( Muleta and Ashenafi, 2001 ; Bersisa et al., 2019 ). However, 11% of raw beef samples from butchers were found to be contaminated with this pathogen ( Garedew et al., 2016 ).

3.3.2. Dairy value chain

Bacterial pathogens in dairy value chains were reported in 23.4% (30/128) of the articles reported.

3.3.2.1. Staphylococcus spp.

Different Staphylococcus spp. were reported in 15 articles (50%). Staphylococcus aureus was common in milk at the farm (14.3%−73.2%) and up to 80% of milk samples at collection centers carried this pathogen ( Almaw et al., 2008 ; Lakew et al., 2009 ; Daka et al., 2012 ; Haftu et al., 2012 ; Makita et al., 2012 ; Tigabu et al., 2015 ; Abebe et al., 2016 ; Tolosa et al., 2016 ; Ayele et al., 2017 ; Beyene et al., 2017 ). Coagulase-negative Staphylococcus was found in 5%−15% of milk samples collected from farms ( Almaw et al., 2008 ; Lakew et al., 2009 ; Beyene et al., 2017 ). Baby bottle (made of cow milk, powder, and cereal blend) samples collected from outpatient infants visiting public clinics in Addis Ababa were contaminated with S. aureus (64.2%−68.3%) ( Erku and Ashenafi, 1998 ).

3.3.2.2. Listeria spp.

Six (20%) articles looked at the presence of Listeria spp. in the dairy value chain. Listeria monocytogenes was detected in 4%−13% of raw milk samples collected from retailers ( Gebretsadik et al., 2011 ; Garedew et al., 2015b ). While pasteurization should kill this bacterium, an article reported that 20% of pasteurized milk samples from retailers carried this pathogen, likely derived from cross-contamination during processing ( Seyoum et al., 2015 ). However, another article reported that none of the pasteurized milk samples at restaurants carry L. monocytogenes ( Garedew et al., 2015b ). Contamination rate of L. monocytogenes in locally produced cottage cheese was low (0%−1%) ( Molla et al., 2005 ; Gebretsadik et al., 2011 ; Garedew et al., 2015b ). On the contrary, 27% of cheese and 5% of yogurt from supermarkets were positive for L. monocytogenes ( Seyoum et al., 2015 ). Also, two articles reported that 15%−20% of ice cream samples from retailers were contaminated with L. monocytogenes ( Molla et al., 2005 ; Garedew et al., 2015b ).

3.3.2.3. Bacillus cereus

According to five (16.7%) articles, 0.6 to 0.8% of milk samples collected from producers were positive for B. cereus ( Almaw et al., 2008 ; Getahun et al., 2008 ). Up to 63% of milk samples from markets were contaminated with B. cereus ( Ashenafi, 1990 ; Abraha et al., 2017 ). Erku and Ashenafi (1998) also identified contamination of baby bottle contents with B. cereus , including 38.3% of cow's milk samples, 42.8% in cereal blend and none in powder milk.

3.3.2.4. Salmonella spp.

Five studies (16.7%) investigated Salmonella spp. in the dairy value chain. Three percent to 20% of milk samples collected at dairy farms carried Salmonella spp. ( Addis et al., 2011 ; Tadesse and Dabassa, 2012 ). While Salmonella spp. was absent in dairy products (cottage cheese and cream) or pasteurized milk, 6% of raw milk samples from retailers were found to be contaminated ( Ejo et al., 2016 ). Erku and Ashenafi (1998) also identified Salmonella contamination of baby bottle contents (3.3% of cow's milk and 7.1% of cereal blends), but not in powder milk.

3.3.2.5. Mycobacterium bovis

Mycobacterium species were the focus in four (13.3%) articles. One article reported that 13% of farms with tuberculosis reactors had milk contaminated with M. bovis ( Fetene et al., 2011 ). Between 3%−14% of tuberculosis infected animals were reported to shed M. bovis in their milk ( Ameni and Erkihun, 2007 ; Elias et al., 2008 ).

3.3.2.6. Escherichia coli

Articles on E. coli were seen in four (13.3%) recently published articles on the dairy value chain (since 2017). Articles on milk found E. coli contamination increasing from 7% on farm to above 60% at retailer milk shops selling raw milk. This increase was attributable to post-farm contamination and lack of cold chain ( Disassa et al., 2017 ; Bedasa et al., 2018 ; Haftay et al., 2018 ; Messele et al., 2019 ). An article reported that none of the pasteurized milk samples collected at cafeterias, restaurants, and supermarkets were contaminated with E. coli while milk derived products, like cheese (40%) and yogurt (25.7%), contained E. coli ( Bedasa et al., 2018 ). Two articles detected E. coli O157:H7 in pasteurized milk (5.7%) sampled from cafeterias, restaurants, open markets, and supermarket but E. coli O157:H7 was not detected in yogurt and cheese samples ( Disassa et al., 2017 ; Bedasa et al., 2018 ).

3.3.3. Poultry and egg value chains

Ten (7.81%) of the included articles reported pathogens in poultry value chain. An article on chicken meat detected E. coli in 37% of samples from slaughterhouses ( Messele et al., 2017 ). Off the 452 chicken meat samples from retailer shops, 11.5% were contaminated with Non-typhoidal Salmonella spp. ( Molla et al., 2003 ). Listeria monocytonenes was detected in 1.9% of raw chicken meat samples collected from retailers ( Molla et al., 2005 ). Salmonella spp. was isolated in 2.6%−18% of egg content and egg sandwich samples collected from either retailers, producers and restaurants ( Muleta and Ashenafi, 2001 ; Bayu et al., 2013 ; Ejo et al., 2016 ; Kemal et al., 2016 ; Taddese et al., 2019 ). Listeria monocytogenes was detected in 4.3% of eggs sampled at retailer ( Gebretsadik et al., 2011 ).

3.3.4. Vegetable value chain

Ten (7.81%) of the included articles investigated hazards in vegetable value chain. High parasite contamination rates were reported for a range of raw vegetables. Presence of at least one type of parasite ( A. lumbricoides, E. histolytica/dispar, G. lamblia ) in samples of raw vegetables (including green paper, carrot, tomato, cabbage, lettuce) was reported in 49%−71% samples ( Bekele et al., 2017 ; Alemu A. S. et al., 2019 ; Bekele and Shumbej, 2019 ). Two articles looked at bacterial hazards in vegetables and reported Salmonella spp. in 0 to 10% of samples and Shigella spp. in 10%−20% of samples ( Guchi and Ashenafi, 2011 ; Eromo et al., 2016 ). Contaminated irrigation water attributed to open air defecation was stated as a possible source of vegetable contamination at the farm ( Alemu G. et al., 2019 ).

3.3.5. Prevalence of hazards in the environment

The selected articles included studies looking at food safety hazards in the environment of beef slaughterhouses (six articles), butcheries (three articles) and milk shops (two articles). However, these studies had small samples sizes (2–30 samples per study).

In slaughterhouses , Salmonella spp. was detected in workers hand swab (2%−50%), surfaces (50%), environmental pooled samples (6.7%), aprons (7.1%), knives (7.7%), room floor (23.5%), refrigerator (10%), beef transport truck (36.4%) and tap water (8.3%) used for washing ( Sibhat et al., 2011 ; Edget et al., 2017 ; Hiko et al., 2018 ). Escherichia coli was present on 50, 23, and 50% of samples from equipment, environment pooled samples and workers hand swab, respectively ( Edget et al., 2017 ; Bersisa et al., 2019 ). Escherichia coli O157:H7 was identified on knife swabs (13.3%) and in environmental pooled samples (6.6%) at slaughterhouses ( Atnafie et al., 2017 ; Edget et al., 2017 ). Staphylococcus spp. ( S. aureus, Staphylococcus intermedius , and Staphylococcus hyicus ) were detected in swab samples from knives (16.7%−33.3%) and hanging materials (33.3%−50%) ( Beyene et al., 2017 ).

About 0%−6.6% cutting board swabs samples from butchers were positive for E. coli O157:H7 ( Atnafie et al., 2017 ; Beyi et al., 2017 ). Bersisa et al. (2019) reported 11.1% cutting board swab and 5.5% of knives swab in butchery shops positive for Salmonella species. In One article E. coli was found in 25% and 19.4% of cutting board and knives swab. This study also reported presence of other bacteria ( Klebsiella, Proteus , and Shigella species) in butchery shops ( Bersisa et al., 2019 ).

Articles found S. aureus contamination rate ranging between 12 and 25% in samples from milk buckets. Same rate was reported in milk tank samples ( Ayele et al., 2017 ; Beyene et al., 2017 ).

3.4. Prevalence in clinically healthy food operators

Articles investigated (26/128, 20%) carriage of bacteria and parasites by food handlers, including workers in universities cafeteria (9/26, 34%), workers at dairy farms, abattoirs, and butchery (9/26, 34%), and workers in other food establishments (hotels, restaurants, bars, and cafeterias; 6/26, 23%). Nineteen (73%) and 12 (46%) of the 26 articles, respectively identified bacteria (mainly Salmonella spp., Shigella spp. and S. aureus ) and parasites from stool samples collected from apparently health food handlers. Table 3 presents the range of contamination with different foodborne pathogens reported in the selected articles.

Table 3 . Pathogens detected from stool samples of food handlers working in food establishments.

One article reported 6% of stool samples from abattoir staff carrying non-typhoidal Salmonella spp. ( Molla et al., 2003 ).

Four articles reported isolation of different bacteria species on worker's hand swab samples. Results showed these swab samples were frequently positive for Salmonella spp., having been found in 24% of samples from butchers' shops operators and 30%−50% of samples of slaughterhouse personnel ( Garedew et al., 2015a ; Edget et al., 2017 ; Hiko et al., 2018 ). Shigella spp. was present in 13% of hand swab samples from butcher shops. Staphylococcus aureus was reported in 25%−32% of dairy farm milkers, and coagulase-negative Staphylococcus in 12%−16% of dairy and beef farm workers' hands. Escherichia coli was found in 50% of hand swabs taken from slaughterhouse workers ( Garedew et al., 2016 ; Ayele et al., 2017 ; Beyene et al., 2017 ; Edget et al., 2017 ).

Swabs from fingernails examined for the presence of bacteria and internal parasites were often positive for coagulase-negative Staphylococcus (12%) and S. aureus (5%) ( Mengist et al., 2018a ).

3.5. Prevalence in non-food operators

Parasites were the most common foodborne hazard investigated in stool samples from children at school, patients visiting health centers and household members of community, including A. lumbricoides (4.2%−28%), G. lamblia (0.8%−10%), Entamoeba (6.7%−7.8%), Trichuris trichuria (0.4%−5.6%), hookworm (0.6%−1.3%) and other parasites ( Desalegn et al., 2014 ; Alelign et al., 2015 ; Jejaw et al., 2015 ; Gebresilasie et al., 2018 ; Gizaw et al., 2018 ; Mekonnen and Ekubagewargies, 2019 ).

In stool samples from adult patients (mostly with enteric signs), Salmonella spp. (non-typhoidal Salmonella 7.18%−39.7%, typhoidal Salmonella 0.8%−39.7%, and unspecified Salmonella species 10.7%), Shigella (1.13%−13.86%), Campylobacter spp. ( Campylobacter jejuni 7.3%−11.89%, C. coli 0.6%−3.5%), and internal parasites ( Entamoeba, Giardia and Cryptosporidium in 24.6%−35.6% of the patients) were identified ( Kassu et al., 2007 ; Ewnetu and Mihret, 2010 ; Tafa et al., 2014 ; Eguale et al., 2015 , 2018 ; Lamboro et al., 2016 ; Berhe et al., 2018 ; Deksissa and Gebremedhin, 2019 ). Acute gastroenteritis patients were positive for norovirus (25.3%) and less commonly for sapovirus (4.2%) ( Sisay et al., 2016 ).

Among prison inmates in north Ethiopia, intestinal parasites were detected in 40% of sample population and the dominant parasite was E. histolytica/dispar (n = 60, 22.2%) followed by G. lamblia , 39 (14.4%) ( Mardu et al., 2019 ). In Gondar, 37.0% of apparently healthy street dwellers carried A. lumbricoides ( Moges et al., 2006 ).

An article exploring the risk of congenital transmission of Toxoplasma gondii showed that 85% of pregnant women monitored in a hospital in Ethiopia had seroconverted by the third trimester of pregnancy ( Gelaye et al., 2015 ). In another article, 31.3% of pregnant women attending antenatal care at Gondar were infected with one or more intestinal parasites. The most common single and mixed parasites observed were E. histolytica (38.1%) and A. lumbricoides (24.6%) ( Kumera et al., 2018 ). Entamoeba histolytica, G. lamblia, Taenia species, A. lumbricoides , and Cryptosporidium parvum were mainly identified in one article which determine the presence of intestinal parasites and associated risk factors among HIV/AIDS patients ( Gedle et al., 2017 ).

4. Discussion

The literature on FBDs hazards in Ethiopia is patchy, mostly consisting of small ad hoc local investigations, with no single comprehensive overview of the topic. This is not a unique feature of Ethiopia and has been reported across Africa ( Alonso et al., 2016 ). The majority of the studies were performed in Oromia, Amhara, Addis Ababa and Southern Nation Nationalities People (SNNP) region which may reflect local outbreaks occurring more frequently in this area due to presence of many food establishments and consumers (Addis Ababa and surrounding Oromia region). It may also reflect a biased picture, with studies performed where relevant research groups happen to be based. The Ethiopian FBD literature has focused on measuring food contamination with key biological hazards, especially bacteria, which are suggested to account for much of the FBD burden ( Havelaar et al., 2015 ).

The identified articles focusing on the prevalence of FB hazards in humans mostly focused on parasitic infection in children (sampled from schools, health centers and community households), adult patients with enteric signs, and susceptible populations (pregnant women and HIV/AIDS patients). A few studies looked at, and reported findings from, presence of Salmonella spp. (typhoidal and non-typhoidal), Campylobacter spp. and Shigella spp. in blood and stool samples.

Some of the most important bacteria in terms of public health (e.g., non-typhoidal Salmonella, L. monocytogenes , and Campylobacter spp.), compared to Salmonella, Staphylococcus and Shigella , have received, to date, little attention in the country. Assessments of the amount of these bacterial pathogens present in food and food environments are very rare. Few of the included articles which reported pathogens in environment do not take representative samples which compromises the quality of work. However, such quantitative assessments are needed to estimate consumer-pathogen exposure and health and economic risk from FBD ( Zaneti et al., 2021 ). The outputs of such assessments are a critical part of food safety management systems and are important for countries to prioritize food safety areas of interventions.

Hazards that are harder to study such as chemicals, viruses, and certain bacteria like Campylobacter spp., were investigated less frequently. This is a well-known challenge in low- and middle-income countries, where resources and facilities for diagnostics are often limited. In our review, we observed an increase overtime in the number of articles on FBD. This could be suggestive of an increased interest in the topic over the past few years, which could have been matched with increased funding for research in this area. It could also be a result of the quality of articles having improved overtime, meaning that an increasing proportion of identified papers would have passed the review's quality assessment which is evidenced by increased number of included (five-fold) than excluded articles from 2015 to 2019. Both options are encouraging and suggest that more attention is being given to food safety and FBD among the national scientific and the international donor communities.

Foodborne pathogens, such as intestinal parasites, E. coli including O157:H7, Salmonella species and S. aureus , were commonly isolated on different foods and at different levels in various value chains. This is not surprising as the level of hygiene and the application of good practices of food quality management are highly variable across the country, but in general are limited, especially in rural areas. Even simple equipment, refrigeration, and key infrastructure, such as a reliable power and clean water supply are not available in informal food supply chains, where most people get their food ( FAO, 2007 ; Glatzel, 2017 ) Even in the more up-market outlets, including supermarkets and restaurants, food safety is a challenge, given both the limited infrastructure and the relative lack of quality suppliers and quality management.

Beef and milk are widely consumed in Ethiopia and were often the target of the included articles. Although consumption of raw beef is a common practice in Ethiopia, hygiene standards in abattoirs are poor, with high levels of E. coli and Salmonella spp. For most pathogens, contamination rates are lower for samples of product collected in slaughterhouses compared to subsequent steps in the supply chain. In the case of meat, the butcher appears to be a node in the chain where levels of contamination tend to increase. Unhygienic practices, both at the slaughterhouses and retail shops, which underpin the public health risk associated with meat-borne pathogens, have been reported in Ethiopia ( Gutema et al., 2021 ).

A variety of articles assessed hygiene and bacterial contamination of milk, typically finding high microbial contamination. Lack of cold chain and the presence of technical limitations by dairy operators were frequently reported as reasons for poor microbial quality of milk ( Disassa et al., 2017 ; Bedasa et al., 2018 ; Haftay et al., 2018 ; Messele et al., 2019 ). Escherichia coli, S. aureus , and Bacillus spp. were the most prevalent bacteria identified in the milk value chain. A recent article showed that the proportion of contamination was significantly lower in milk collected from dairy farms when compared to milk from vendors ( Berhe et al., 2020 ). Generally, presence of E. coli, E. coli 0157:H7, Bacillus spp, and Listeria spp was more likely in raw milk samples collected from retailers than those from producers, indicating that milk microbial quality may derived from contamination at various points of the value chain post-harvest, and that storage conditions are facilitating bacterial growth. The literature also showed contamination by foodborne pathogens of various milk derived products; it is worth noting that, in Ethiopia, these products are typically consumed without any further processing at home, meaning that no steps that could reduce the pathogen load are taken before consumption ( Beyene et al., 2017 ; Amenu et al., 2019 ; Mebrate et al., 2020 ; Deneke et al., 2022 ). The presence of hazards in pasteurized milk reported in some of the studies is concerning. Pasteurization is a heat-treatment process used to decrease the bacterial load of milk. Presence of bacteria in pasteurized milk is indicative of failures in the pasteurization process, cross- or re-contamination post-pasteurization or inadequate storage after pasteurization ( Garedew et al., 2012 ; Tekilegiorgis, 2018 ).

The importance of beef and milk processing points and practices to food safety, are highlighted in articles from beef and dairy value chains. Foodborne pathogens originating from fecal contamination during slaughter, such as Salmonella spp. and E. coli , can potentially contaminate the carcass and spread to the cut or raw meat intended for further processing, causing a major public health threat ( Soepranianondo et al., 2019 ). This is supported by several of the included articles which show presence of different bacterial species in samples collected from different environmental surfaces at beef slaughterhouses ( Hiko et al., 2015 ; Edget et al., 2017 ; Messele et al., 2017 ; Bedasa et al., 2018 ). However, extrapolation of these findings to the entire country could not be reliable due to the small sample sizes and geographical coverage in the majority of the articles reviewed.

Further evidence of sources of contamination along the food value chains is presented by the microbial investigations of apparently healthy food handlers. These records confirm the potential role of food handlers in the spread of FBD ( Dagnew et al., 2012 ). Food handlers with poor health and hygiene may be infected with a wide range of foodborne pathogens and have already been demonstrated to play a role in transmitting disease to the public ( Khurana et al., 2007 ). This is an important area in food safety research, and our results show that it deserves greater attention in the country.

There were no published assessments of FBD burden and incidence in humans. The SLR only included published literature but did not consider hospital records that are unpublished (gray literature), therefore, the study cannot assess the true burden of FBD. However, it is true that in Ethiopia, many foods are consumed raw (beef, milk) ( Dagne et al., 2022 ; Deneke et al., 2022 ), therefore the risk of FBD is higher if the prevalence of pathogens in the product is high. Disease burden and cost estimates are critical for risk-based decision-making. Estimating the incidence of illness caused by FBD is a gap to be addressed in the future.

It is important for policy makers to know the burden of a disease in order to allocate appropriate resources for its control. However, FBD burden is harder to measure than food contamination, either requiring an effective FBDs surveillance system, which does not exist in many low- and middle-income countries, or well-designed, large epidemiological studies. These studies require complex analysis to overcome issues of under-reporting and imperfect diagnosis.

We acknowledge that the search being done only in two databases and required articles to be available electronically some articles may not have been detected. Therefore, information from gray literatures is not included. However, all quality research articles are expected to have been captured and inclusion of electronically available articles as a limitation to this review. Only 10% ( n = 13) of the 128 articles were reviewed in pairs. This may also be one limitation of this review. In addition, publications since 2019 recent years are not considered due to time constraints and because the review was performed at the time to inform overarching research projects that started around 2019. Lastly, we cannot exclude the possibility that the results from our review are affected by publication bias, but we have no ability to estimate the magnitude of that potential bias.

5. Conclusion

In conclusion, little has been done to assess FBD burden in Ethiopia. The scientific literature reveals high levels of contamination, with both bacterial and parasitic pathogens, and shows fundamental gaps in food safety for many food value chains. Pathogens that are hard to assess are largely over-looked. In both beef and dairy value chains bacterial contamination was observed with increasing prevalence from farm/slaughterhouse to point of sale. Given the findings, the following recommendations are made to improve food safety in Ethiopia:

1. More systematic and ongoing evaluation of contamination should be implemented to provide a comprehensive overview of the topic including in Benishangul-gumuz, Afar, and Somali regions.

2. Chemicals, viruses and some of the most important bacteria which are of public health concern should be investigated more.

3. Future research on FBD should thoroughly investigate risk factors.

4. The potential role of food handlers and food environment should be investigated in detail by considering representative samples.

5. In addition to assessing presence or absence of hazards, quantitative assessments of the amount of hazards present in food and food environments is required.

6. Due attention should be given to vegetables, fruits, crops, fish, sheep, goats, and camel value chains.

7. Incidence of human FBDs or resulting health and economic impacts should also be center of attention.

Data availability statement

The original contributions presented in the study are included in the article/ Supplementary material , further inquiries can be directed to the corresponding author.

Author contributions

Conceived and designed the study protocol: DG, SA, FMu, KR, JL, KA, and MD. Carried out the screening and data extraction from records: DG, SA, FMu, KR, JL, LG, KA, FMa, PU, TG, and GI. Drafted the manuscript: LG, SA, and TK-J. All authors read, reviewed, and approved the final manuscript.

This publication is based on research funded by the Bill & Melinda Gates Foundation and the UK Government Foreign, Commonwealth & Development Office (FCDO)—UK Aid from the United Kingdom government (INV-008430-OPP1195588 and OPP1156625). The findings and conclusions are those of the authors and do not necessarily reflect positions or policies of the Bill & Melinda Gates Foundation or the UK government. The work also received financial support from the CGIAR Research Program on Agriculture for Nutrition and Health. The funder played no role in the design or conclusion of the study.

Acknowledgments

This activity is part of the Urban food markets in Africa: incentivizing food safety using a pull-push approach and the MoreMilk: making the most of milk investments, which are supported by the Bill & Melinda Gates Foundation, the Foreign, Commonwealth and Development Office (FCDO) of the UK Government, with co-funding from the One Health Research, Education and Outreach Center in Africa (OHRECA) funded by German Federal Ministry of Economic Cooperation and Development (BMZ) and the CGIAR Research Program on Agriculture for Nutrition and Health (A4NH) led by the International Food Policy Research Institute. We also acknowledge the CGIAR Fund Donors ( https://www.cgiar.org/funders ).

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Supplementary material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fsufs.2023.1058977/full#supplementary-material

• Urban food markets in Africa: Incentivizing food safety using a pull-push approach (“pull-push” project), led by the International Livestock Research Institute.

• The assessment and management of risk from non-typhoidal Salmonella, diarrheagenic Escherichia coli and Campylobacter in raw beef and dairy in Ethiopia (TARTARE), led by Ohio State University.

• Foodborne disease epidemiology, surveillance and control in African LMIC (FOCAL), led by Technical University of Denmark.

• Ensuring the safety and quality of milk and dairy products across the dairy value chain in Ethiopia (ENSURE), led by Addis Ababa University.

2. ^ Salmonella spp.—many studies did not provide the speciation of Salmonella , and it is possible some of these studies may or may not include Non-Typhoidal Salmonella ., N.B. Salmonella spp. does not include Non-Typhoidal Salmonella , and Escherichia coli does not include E. coli O157:H7. N.B. articles may include more than one bacteria and parasite.

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Keywords: food borne diseases, value chains, hazards, burden, Ethiopia

Citation: Gazu L, Alonso S, Mutua F, Roesel K, Lindahl JF, Amenu K, Maximiano Sousa F, Ulrich P, Guadu T, Dione M, Ilboudo G, Knight-Jones T and Grace D (2023) Foodborne disease hazards and burden in Ethiopia: A systematic literature review, 1990–2019. Front. Sustain. Food Syst. 7:1058977. doi: 10.3389/fsufs.2023.1058977

Received: 30 September 2022; Accepted: 25 January 2023; Published: 15 February 2023.

Reviewed by:

Copyright © 2023 Gazu, Alonso, Mutua, Roesel, Lindahl, Amenu, Maximiano Sousa, Ulrich, Guadu, Dione, Ilboudo, Knight-Jones and Grace. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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A review of environmental impacts of wheat production in different agrotechnical systems.

1. Introduction

2. evaluation of environmental impacts in the life cycle assessment, 3. impact categories of wheat grain production, 4. irrigated and non-irrigated production systems, 5. conventional versus organic farming systems, 6. the impact of fertilizers on the environment, 7. conventional and conservation tillage methods, 8. crop rotation effect, 9. consequences for social and political systems of wheat production, 10. conclusions, author contributions, data availability statement, conflicts of interest.

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Kheiralipour, K.; Brandão, M.; Holka, M.; Choryński, A. A Review of Environmental Impacts of Wheat Production in Different Agrotechnical Systems. Resources 2024 , 13 , 93. https://doi.org/10.3390/resources13070093

Kheiralipour K, Brandão M, Holka M, Choryński A. A Review of Environmental Impacts of Wheat Production in Different Agrotechnical Systems. Resources . 2024; 13(7):93. https://doi.org/10.3390/resources13070093

Kheiralipour, Kamran, Miguel Brandão, Malgorzata Holka, and Adam Choryński. 2024. "A Review of Environmental Impacts of Wheat Production in Different Agrotechnical Systems" Resources 13, no. 7: 93. https://doi.org/10.3390/resources13070093

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