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

1Food 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.

2Unsafe 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.

3Food safety is being challenged nowadays by the global dimensions of food supply chains. 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. 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. 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.

4What food safety–related public health risks are commonly found in the food market?

5We 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.

6All 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.

7We 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.

8((((("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]))

9Search 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. 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.

10In order to minimize bias, we the reviewers independently extracted data from papers included in the review using JBI mixed methods data extraction form. 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.

11The 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.

12The 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. 1).

13In 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. 2).

14All 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).

15The 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 1).

16Table 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.

17Figure 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.

18In 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 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.

19Fifteen (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 4).

20In 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 5).

21In 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 6).

22Mislabeling 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 7).

23In 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 8).

24Six (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 9).

25This 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 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. 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. Moreover, hence the regulatory services are weak in developing countries, most food sellers may not comply with food hygiene and safety requirements or standards. In developing countries, the legislation enforcement is still weak about administrating the concentration of harmful contaminants in the food. In addition, there is inadequate information and technology to detect fake and fraud products.

26This 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. 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. Moreover, fraud of foods such as adulteration, mislabeling, and selling of spoiled or expired foods are also causing microbial contamination. Microbial contamination of foods causes millions of diseases and thousands of deaths. 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. 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. The standard culture–based technique, which is a predominant detection method in developing countries, is not effective for Campylobacter species.

27Contamination 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. The phases of food processing, packaging, transportation, and storage are significant contributors to food contamination. 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. Chemical contamination of foods is responsible millions of cases of poisoning with thousands of hospitalizations and deaths each year.

28Nine 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. 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. 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. Chemicals which are being used as adulterants have a wide range of serious effects on the health of consumers including cancer.

29In this systematic review of literature, 11 of the full-text articles reported that misuse of food additives in the food market endangers public health. 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. Substances generally recognized as safe (GRAS) can be used as food additives; 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.

30Mislabeling 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. 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. 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.

31In 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. 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. 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. 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.

32This 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. Growth of microorganisms in expired foods is very common. Most of these microorganisms are pathogenic and some microorganisms produce toxic substances as they develop.

33We 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.

34This 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.

35The full text articles included in this review are attached as a supplementary file (see supplementary file).