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MILK Symposium review: Foodborne diseases from milk and milk products in developing countries—Review of causes and health and economic implications*

  • D. Grace
    Affiliations
    Animal and Human Health Program, International Livestock Research Institute, Nairobi, Kenya 00100

    Natural Resources Institute, University of Greenwich, Central Avenue, Chatham Maritime, Kent, ME4 4TB United Kingdom
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  • F. Wu
    Affiliations
    Department of Food Science and Human Nutrition, Department of Agricultural, Food, and Resource Economics, Michigan State University, East Lansing 48824
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  • A.H. Havelaar
    Correspondence
    Corresponding author
    Affiliations
    Animal Sciences Department, Emerging Pathogens Institute, Institute for Sustainable Food Systems, University of Florida, Gainesville 32605
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  • Author Footnotes
    * Presented as part of the MILK Symposium: Improving Milk Production, Quality, and Safety in Developing Countries at the ADSA Annual Meeting, Cincinnati, Ohio, June 2019.

      ABSTRACT

      Dairy production is rapidly increasing in developing countries and making significant contributions to health, nutrition, environments, and livelihoods, with the potential for still greater contributions. However, dairy products can also contribute to human disease in many ways, with dairyborne disease likely being the most important. Health risks may be from biological, chemical, physical, or allergenic hazards present in milk and other dairy products. Lacking rigorous evidence on the full burden of foodborne and dairyborne disease in developing countries, we compiled information from different sources to improve our estimates. The most credible evidence on dairyborne disease comes from the World Health Organization initiative on the Global Burden of Foodborne Disease. This suggests that dairy products may has been responsible for 20 disability-adjusted life years per 100,000 people in 2010. This corresponds to around 4% of the global foodborne disease burden and 12% of the animal source food disease burden. Most of this burden falls on low- and middle-income countries (LMIC). However, the estimate is conservative. Weaker evidence from historical burden in high-income countries, outbreak reports from LMIC and high-income countries, and quantitative microbial risk assessment suggest that the real burden may be higher. The economic burden in terms of lost human capital is at least US$4 billion/yr in LMIC. Among the most important hazards are Mycobacterium bovis, Campylobacter spp., and non-typhoidal Salmonella enterica. The known burden of chemical hazards is lower but also more uncertain. Important chemical hazards are mycotoxins, dioxins, and heavy metals. Some interventions have been shown to have unintended and unwanted consequences, so formative research and rigorous evaluation should accompany interventions. For example, there are many documented cases in which women's control over livestock is diminished with increasing commercialization. Dairy co-operatives have had mixed success, often incurring governance and institutional challenges. More recently, there has been interest in working with the informal sector. New technologies offer new opportunities for sustainable dairy development.

      Key words

      INTRODUCTION

      Dairy production is rapidly increasing in developing countries, making significant contributions to health, nutrition, environment, and livelihoods, and it has the potential to make still greater contributions. At the same time, there are negative effects associated with dairy production, processing, and consumption. This paper focuses on one of the most important negative effects: human diseases that can be transmitted through milk and dairy product consumption. We focus on bovines which produce 96% of the world's milk (
      • FAO (Food and Agriculture Organization of the United Nations)
      Gateway to dairy products.
      ). In this review, we describe the main health, nutrition, and other benefits of milk to place the health risks in a broader perspective. Next, we set out some important concepts that are needed to understand the health implications of dairyborne disease, including differentiating safety and quality, hazard and risk, and dairyborne diseases and diseases associated with dairy. Until the last century, milk was an important source of foodborne pathogens, which pasteurization and other hygienic technologies and practices helped to overcome. We describe evidence streams that can contribute to understanding milkborne disease, concluding that milkborne disease is likely to be an important public health issue in developing countries, but evidence on the burden is incomplete.
      One of the most comprehensive and credible studies on foodborne contaminants is the Global Burden of Food-Borne Disease Initiative, under the aegis of the World Health Organization (WHO); we summarize its findings relevant to milkborne disease. The next section focuses on aflatoxin, a fungal toxin, of which a metabolite frequently appears in dairy products worldwide. We then review the scant literature on the economic implications of milkborne disease. The final section summarizes some of the approaches and options for reducing the burden of milkborne disease.

      HEALTH, NUTRITION, AND LIVELIHOOD BENEFITS OF DAIRY PRODUCTION

      Milk and dairy products are a source of essential nutrients, especially for children and pregnant woman. Milk contains protein and calcium and is a good source of vitamin B12, thiamine, and riboflavin. Along with other animal-source foods, milk consumption has been found to improve anthropometric indices and cognitive function in children and to reduce nutritional deficiencies (
      • Dror D.K.
      • Allen L.H.
      The importance of milk and other animal-source foods for children in low-income countries.
      ;
      • Grace D.
      • Dominguez-Salas P.
      • Alonso S.
      • Lannerstad M.
      • Muunda E.
      • Ngwili N.
      • Omar A.
      • Khan M.
      • Otobo E.
      The influence of livestock-derived foods on the nutrition of mothers and infants during the first 1,000 days of a child's life. Research Report 44.
      ).
      Diets of young children in developing countries are often restricted to cereals and legumes; however, the inclusion of animal-source foods is necessary to optimize children's nutritional needs. There is convincing evidence that dairy protein improves linear growth even in well-nourished children; evidence is strongest for school-age children (
      • Grenov B.
      • Michaelsen K.F.
      Growth components of cow's milk: Emphasis on effects in undernourished children.
      ). A review on the importance of milk and dairy in children's diets concluded that its consumption is associated with improved bone development (
      • Dror D.K.
      • Allen L.H.
      The importance of milk and other animal-source foods for children in low-income countries.
      ) in both wealthier and poorer populations.
      Milk is widely consumed in low- and middle-income countries (LMIC), although this is strongly influenced by culture and geography. It is especially important in South Asia and North Africa as well as the East African highlands (
      • Headey D.D.
      • Hirvonen K.
      • Hoddinott J.F.
      Animal sourced foods and child stunting. Discussion Paper 1695.
      ). Production of dairy may be easier to intensify and scale up than production of meat, and predictive models show how dairy products are among the leaders in the livestock revolution (Figure 1).
      Figure thumbnail gr1
      Figure 1Global production of some livestock-derived foods (1961–2050). Data from
      • Alexandratos N.
      • Bruinsma J.
      World food and agriculture to 2030/50: The 2012 revision (03 No. 12). ESA Working Paper.
      .
      Dairy production as well as consumption contributes to livelihoods. In many LMIC, dairy value chains are a primary source of income for rural populations. Money earned from producing, processing, and selling milk can be used to improve quality of life. In many cultures, milk is one of the few resources that is under the control of women, both as food for the family and a source of earnings from processing and sale. For example, a food safety project assessed gender roles in 20 animal-source food value chains (
      • Grace D.
      • Roesel K.
      • Kang'ethe E.
      • Bassirou B.
      • Theis S.
      Gender roles and food safety in 20 informal livestock and fish value chains. IFPRI Discussion Paper 1489.
      ). Overall, women were more involved in dairy and fish and less involved in meat and game value chains. In West Africa, men fed cattle and milked cows, but in Kenya this was women's responsibility. In all studies women were responsible for processing (e.g., fermentation). In 3 of the studies where traditional dairying predominated, women were in charge of marketing. In urban Cote d'Ivoire, where dairying was novel, men had taken over marketing. Entrepreneurship can also empower women, and several studies have shown positive links between women's empowerment and children's health. This fact is of great importance in the link between dairy production, consumption, and nutrition because women are generally in charge of household nutrition, are the main custodians of food cultures, and have been shown to prioritize food expenditures more than men do (
      • Grace D.
      • Roesel K.
      • Kang'ethe E.
      • Bassirou B.
      • Theis S.
      Gender roles and food safety in 20 informal livestock and fish value chains. IFPRI Discussion Paper 1489.
      ).
      Moreover, whereas poultry, pig, and fish production have large economies of scale, making it hard for smallholders to compete with industrial production, dairying is much more land and labor intensive, so it is more likely to remain a viable option for smaller farmers for longer, thus supporting livelihoods in LMIC. Dairy production can also be environmentally sustainable, especially when cattle diets rely on crop by-products and non-commodity feeds such as pastures and forages (
      • Britt J.H.
      • Cushman R.A.
      • Dechow C.D.
      • Dobson H.
      • Humblot P.
      • Hutjens M.F.
      • Jones G.A.
      • Ruegg P.S.
      • Sheldon I.M.
      • Stevenson J.S.
      Invited review: Learning from the future—A vision for dairy farms and cows in 2067.
      ). A comparative study found that dairy-based diets ranked more highly than vegan-, egg-, and omnivore-based diets in terms of feeding the greatest number of people while adhering to recommended agronomic practices for various classes of lands (
      • Peters C.J.
      • Picardy J.
      • Darrouzet-Nardi A.F.
      • Wilkins J.L.
      • Griffin T.S.
      • Fick G.W.
      Carrying capacity of U.S. agricultural land: Ten diet scenarios.
      ). Manure is also an important source of organic matter in soil.
      Despite these benefits of dairy production and consumption, several important risks are associated with milkborne contaminants. These are discussed in the next sections.

      HEALTH RISKS OF MILK

      This section summarizes concepts that are important for understanding milk and health risks but that are often confused: (1) the difference between safety and quality, (2) hazards associated with consumption of milk, and (3) the difference between hazard and risk.
      Food safety refers to the absence of substances, whether natural or artificial, that may make food injurious to the health of the consumer. Quality includes all other attributes that influence a product's value to the consumer. This includes negative attributes such as spoilage, adulteration, contamination with filth, discoloration, off-odors, and other nonhazardous substances as well as positive attributes such as the nutritional quality attributes (e.g., fat, protein), origin, color, flavor, texture, and processing method of the food. Adulteration always reduces the value of the product to the consumer (a measure of quality) and, depending on the type of adulteration, may introduce health hazards or reduce other aspects of quality, such as nutritional content (
      • Spink J.
      • Ortega D.
      • Chen C.
      • Wu F.
      Food fraud prevention shifts the food risk focus to vulnerability.
      ).
      In food safety terminology, a hazard is something that can harm human health. A wide range of hazards can be present in food.
      Milk is an excellent substrate for bacterial growth and microbial survival at permissive temperatures (
      • Hassan A.N.
      • Frank J.F.
      Microorganisms associated with milk.
      ). Harmful bacteria may originate from the animal, the environment, milking equipment, or the milk handlers or be introduced with an adulterant such as contaminated water. Chemical contaminants may enter the milk through the feed or veterinary treatments of the animal or through later accidental or deliberate contamination.
      Several chronic diseases have also been associated with milk consumption (especially at high levels), linking dairy consumption to cancer, cardiovascular disease, and obesity, which may be linked to milk fat or specific dairy proteins. Other studies show the opposite or no relation between dairy consumption and these diseases (
      • Larsson S.C.
      • Crippa A.
      • Orsini N.
      • Wolk A.
      • Michaelsson K.
      Milk consumption and mortality from all causes, cardiovascular disease, and cancer: A systematic review and meta-analysis.
      ;
      • Mozaffarian D.
      Dairy foods, obesity, and metabolic health: The role of the food matrix compared with single nutrients.
      ).
      A health problem unambiguously linked to milk consumption is lactose intolerance. (Food intolerances are nonimmunological adverse reactions to food as the result of pharmacological effects, non-celiac gluten sensitivity, or enzyme or transport defects.) Lactose is a sugar that is naturally present in milk that all infants can digest because they produce lactase. However, lactase production does not persist in many people. Undigested lactose is fermented by bacteria in the colon, resulting in mild to moderate gastrointestinal symptoms such as diarrhea and pain. About 70% of the world's population is lactose intolerant (
      • Heine R.G.
      • AlRefaee F.
      • Bachina P.
      • De Leon J.C.
      • Geng L.
      • Gong S.
      • Madrazo J.A.
      • Ngamphaiboon J.
      • Ong C.
      • Rogacion J.M.
      Lactose intolerance and gastrointestinal cow's milk allergy in infants and children—Common misconceptions revisited.
      ). The public health burden from deficiencies attributable to lactose intolerance has not been established, but the condition is mild and can be managed.
      However, dairy production can affect health through other pathways (
      • McDaniel C.J.
      • Cardwell D.M.
      • Moeller Jr., R.B.
      • Gray G.C.
      Humans and cattle: A review of bovine zoonoses.
      ). Cattle can be reservoirs for zoonotic diseases, which can be transmitted by direct contact or by environments contaminated with animal manure. For example, brucellosis is often acquired by handling aborted material (although it is also transmitted by milk), and campylobacteriosis may result from environment contamination in rural areas or contamination of the milk by bovine feces. Antimicrobial residues are chemical hazards commonly found in food, but their main health effects are through fostering pathogens resistant to antimicrobial treatment, not through direct consumption of milk. Cattle may also cause acute injuries or be associated with chronic trauma (e.g., arthritis associated with repetitive joint stress from working in dairies).
      Hazards, as discussed above, are important because they have the potential to cause sickness and, in some cases, even death. However, the mere presence of a hazard in milk does not mean that it is necessarily going to harm a person's health; “the dose makes the poison” (
      • Grandjean P.
      Paracelsus revisited: The dose concept in a complex world.
      ). To understand the implication of hazards for human health, we need to assess risk. In food safety, risk is a combination of the severity of harm to human health and the probability of its occurrence. This has several important implications. First, just because a hazard is found in milk does not necessarily mean it will cause illness or death; this implies that regulation and control should be based on risks and not hazards. Second, substances may be harmless or even beneficial in small amounts but cause problems if they are consumed in large amounts. Third, for many chemical substances there may be a threshold below which a hazard is unlikely or unable to cause harm.

      MILKBORNE DISEASE IN LMIC

      Dairy products were an important cause of disease in the 19th century in now-developed countries. Milk became safer as the result of widespread pasteurization and improvements in hygiene and disease eradication schemes (especially addressing tuberculosis, brucellosis, typhoid, paratyphoid, and food poisoning) in combination with testing, regulation, and advances in hygiene. In developed countries, almost all milk is now pasteurized and standards for dairy products are effectively maintained. Consumption of unpasteurized milk continues to be associated with foodborne disease (FBD) outbreaks, even in developed nations where a small proportion of consumers choose to drink raw milk (
      • Costard S.
      • Espejo L.
      • Groenendaal H.
      • Zagmutt F.J.
      Outbreak-related disease burden associated with consumption of unpasteurized cow's milk and cheese, United States, 2009–2014.
      ). A small number of studies from LMIC have also implicated dairy as a cause of FBD. For example, in India dairy products have been implicated as important in several studies (
      • Abraham M.
      • Pai M.
      • Kang G.
      • Asokan G.V.
      • Magesh S.R.
      • Bhattacharji S.
      • Ramakrishna B.S.
      An outbreak of food poisoning in Tamil Nadu associated with Yersinia enterocolitica.
      ;
      • Sudershan R.V.
      • Naveen Kumar R.
      • Kashinath L.
      • Bhaskar V.
      • Polasa K.
      Foodborne infections and intoxications in Hyderabad India.
      ;
      • Khare S.
      • Tonk A.
      • Rawat I.
      Foodborne diseases outbreak in India: A review.
      ).
      Until recently, there was very little solid evidence of the health and economic burden of FBD, let alone milkborne disease, in LMIC. However, we can triangulate different approaches to better understand the health burden. In the rest of this section, we summarize the methods and findings of 6 important approaches, including (1) global burden of disease studies, especially the World Health Organization study on the burden of FBD; (2) official records on FBD outbreaks; (3) historical evidence from high-income countries (HIC); (4) studies on hazard presence and prevalence in milk; (5) assessments of the health risk posed by different hazards; and (6) studies on compliance with standards.

      Global Burden Studies: WHO Foodborne Disease Burden Epidemiology Reference Group and Institute of Health Metrics and Evaluation

      For many years, information on health effects of FBD was not available or was limited to selected HIC, such as the United States, Canada, and the Netherlands (
      • Scallan E.
      • Griffin P.M.
      • Angulo F.J.
      • Tauxe R.V.
      • Hoekstra R.M.
      Foodborne illness acquired in the United States—Unspecified agents.
      ;
      • Thomas M.K.
      • Murray R.
      • Flockhart L.
      • Pintar K.
      • Pollari F.
      • Fazil A.
      • Nesbitt A.
      • Marshall B.
      Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006.
      ;
      • Havelaar A.H.
      • Kirk M.D.
      • Torgerson P.R.
      • Gibb H.J.
      • Hald T.
      • Lake R.J.
      • Praet N.
      • Bellinger D.C.
      • de Silva N.R.
      • Gargouri N.
      • Speybroeck N.
      • Cawthorne A.
      • Mathers C.
      • Stein C.
      • Angulo F.J.
      • Devleesschauwer B.
      World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010.
      ). To address this gap, an initiative was launched by the WHO Foodborne Disease Burden Epidemiology Reference Group (FERG) in 2006. Based on almost a decade of work by various experts and expert panel groups, the results were published in December 2015. The FERG used systematic reviews and meta-analysis to estimate the global incidence of disease, deaths, and disease burden (disability-adjusted life years, DALY; see, e.g.,
      • Devleesschauwer B.
      • Havelaar A.H.
      • Maertens de Noordhout C.
      • Haagsma J.A.
      • Praet N.
      • Dorny P.
      • Duchateau L.
      • Torgerson P.R.
      • Van Oyen H.
      • Speybroeck N.
      DALY calculation in practice: A stepwise approach.
      ). They then used a structured elicitation of scientific judgment that consisted of expert panels combined with various mathematical models to estimate the proportion of FBD. They found that 31 FBD hazards (both biological and chemical hazards) globally accounted for around 600 million cases of FBD and 420,000 deaths, imposing a burden of around 33 million DALY each year (
      • Havelaar A.H.
      • Kirk M.D.
      • Torgerson P.R.
      • Gibb H.J.
      • Hald T.
      • Lake R.J.
      • Praet N.
      • Bellinger D.C.
      • de Silva N.R.
      • Gargouri N.
      • Speybroeck N.
      • Cawthorne A.
      • Mathers C.
      • Stein C.
      • Angulo F.J.
      • Devleesschauwer B.
      World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010.
      ). More recently, the FERG reported on the burden of disease due to 4 heavy metal chemical hazards; this was an additional 9 million DALY globally. The FERG estimates have been broken down by subregion based on the 6 WHO regions and further subdivided based on child and adult mortality. It was found that the largest share of FBD burden occurred in LMIC, where particularly children under 5 yr of age bear a large share of the burden (
      • Havelaar A.H.
      • Kirk M.D.
      • Torgerson P.R.
      • Gibb H.J.
      • Hald T.
      • Lake R.J.
      • Praet N.
      • Bellinger D.C.
      • de Silva N.R.
      • Gargouri N.
      • Speybroeck N.
      • Cawthorne A.
      • Mathers C.
      • Stein C.
      • Angulo F.J.
      • Devleesschauwer B.
      World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010.
      ).
      A follow-up study by the FERG attempted to assess the contribution of animal-source foods. The study involved 13 out of 31 hazards that were included in the global burden of FBD estimates and can be associated with animal-source foods. These hazards accounted for just over 40% of the total foodborne DALY. The proportion of FBD attributable to 8 different animal-source food groups was estimated by structured expert elicitation (
      • Hoffmann S.
      • Devleesschauwer B.
      • Aspinall W.
      • Cooke R.
      • Corrigan T.
      • Havelaar A.
      • Angulo F.
      • Gibb H.
      • Kirk M.
      • Lake R.
      • Speybroeck N.
      • Torgerson P.
      • Hald T.
      Attribution of global foodborne disease to specific foods: Findings from a World Health Organization structured expert elicitation.
      ). By combining these attribution estimates with the burden estimates, dairy was estimated to be responsible for 20 DALY per 100,000 people in 2010 (
      • Li M.
      • Havelaar A.H.
      • Hoffmann S.
      • Hald T.
      • Kirk M.D.
      • Torgerson P.R.
      • Devleesschauwer B.
      Global disease burden of pathogens in animal source foods, 2010.
      ). This corresponded to around 12% of the FBD burden associated with animal-source food and 4% of the overall FBD burden. The importance of dairy products and the pathogens causing the highest burden varied considerably by region, as shown in Figure 2. Globally, non-typhoidal Salmonella enterica, Campylobacter spp., and Mycobacterium bovis are the most important hazards in dairy products, whereas Brucella spp. are of particular concern in the Eastern Mediterranean region. Shiga toxin-producing Escherichia coli, Cryptosporidium spp., and Toxoplasma gondii caused a relatively low burden through dairy.
      Figure thumbnail gr2
      Figure 2Global burden of disease from dairy products by region and some important hazards. DALY = disability-adjusted life years; STEC = Shiga toxin-producing Escherichia coli. The x-axis codes refer to WHO regions: AFR = Africa; AMR = the Americas; EMR = Eastern Mediterranean; EUR = Europe; SEAR = South-East Asia; and WPR = Western Pacific. Regions are further subdivided on the basis of mortality: B = low child mortality and very low adult mortality; C = low child mortality and high adult mortality; D = high child and adult mortality; E = high child and very high adult mortality. For more details, see
      • Li M.
      • Havelaar A.H.
      • Hoffmann S.
      • Hald T.
      • Kirk M.D.
      • Torgerson P.R.
      • Devleesschauwer B.
      Global disease burden of pathogens in animal source foods, 2010.
      .
      The regional classification of the WHO does not completely correspond to World Bank income categories. For example, Cuba is an LMIC but along with Canada and the United States (both HIC) constitutes the region AMR A. However, the regions AMR A, EUR A, and WPR A comprise mainly HIC, and the other 11 regions comprise mainly LMIC. This allows us to make an approximate estimate of the health burden of milkborne disease in LMIC.
      The FERG estimates may underestimate the true burden of FBD, including diseases related to dairy. Only a limited number of pathogens for which cattle can be reservoirs and that can be transmitted by dairy products were assessed due to a lack of reliable data (see Table 1). Furthermore, dairy products can be a vehicle for non-zoonotic pathogens. For example, ice cream from unreliable sources is frequently contaminated with hepatitis A virus, and dairy products can be a vehicle for listeriosis. Although the FBD burden of these hazards has been quantified by FERG, it has not been attributed to dairy or other food products. Not all health outcomes from FBD could be included in the estimates, again because of a lack of data. For example, there is increasing evidence that asymptomatic infections with enteric pathogens, including those that can be transmitted by dairy, are associated with malnutrition, in particular stunting, which affects 155 million children globally (
      • Rogawski E.T.
      • Liu J.
      • Platts-Mills J.A.
      • Kabir F.
      • Lertsethtakarn P.
      • Siguas M.
      • et al.
      Use of quantitative molecular diagnostic methods to investigate the effect of enteropathogen infections on linear growth in children in low-resource settings: Longitudinal analysis of results from the MAL-ED cohort study.
      ). Also, FBD occurring in highly vulnerable populations, such as people with HIV or AIDS, were not included in the FERG estimates because they were already included in the burden of HIV infection. Nevertheless, these FBD would be prevented by improved food safety management.
      Table 1Comparing different burden of disease studies
      FERG = World Health Organization Foodborne Disease Burden Epidemiology Reference Group (Havelaar et al., 2015); CHERG = World Health Organization Childhood Epidemiology Reference Group (Lanata et al., 2013); WHO-GHE = WHO Global Health Estimates (World Health Organization, 2017); IHME-GBD = Institute of Health Metrics and Evaluation, Global Burden of Disease (Lozano et al., 2012; Vos et al, 2012). Only FERG estimated foodborne disease hazards.
      ItemFERGCHERGWHO-GHEIHME-GBD
      Year of publication2015201320172012
      Time period of data collection1990–20121990–20111990–20131980–2010
      Year represented in data2010201120102010
      Geographical range of estimates194 countries, grouped by 14 subregionsGlobal183 countries187 countries
      Age groups<5 yr, ≥5 yr<5 yr0–4, 5–14, 15–29, 30–49, 50–59, 60–69, ≥70 yr0–6 d, 7–27 d, 28–364 d, 1–4 yr, 5–9 yr, . . ., 75–79 yr, ≥80 yr
      Metrics
      YLD = years lived with disability; YLL = years of life lost; DALY = disability-adjusted life years.
      Incidence, deaths, YLD, YLL, DALYDeathsDeaths, YLD, YLL, DALYIncidence, deaths, YLD, YLL, DALY
      Campylobacter spp.XXX
      Shiga toxin-producing Escherichia coliX
      Non-typhoidal Salmonella entericaXXX
      Cryptosporidium spp.XXX
      Brucella spp.X
      Mycobacterium bovisX
      1 FERG = World Health Organization Foodborne Disease Burden Epidemiology Reference Group (
      • Havelaar A.H.
      • Kirk M.D.
      • Torgerson P.R.
      • Gibb H.J.
      • Hald T.
      • Lake R.J.
      • Praet N.
      • Bellinger D.C.
      • de Silva N.R.
      • Gargouri N.
      • Speybroeck N.
      • Cawthorne A.
      • Mathers C.
      • Stein C.
      • Angulo F.J.
      • Devleesschauwer B.
      World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010.
      ); CHERG = World Health Organization Childhood Epidemiology Reference Group (
      • Lanata C.F.
      • Fischer-Walker C.L.
      • Olascoaga A.C.
      • Torres C.X.
      • Aryee M.J.
      • Black R.E.
      Global causes of diarrheal disease mortality in children <5 years of age: A systematic review.
      ); WHO-GHE = WHO Global Health Estimates (
      • World Health Organization
      Health statistics and information systems: Global health estimates for 2000–2015.
      ); IHME-GBD = Institute of Health Metrics and Evaluation, Global Burden of Disease (
      • Lozano R.
      • Naghavi M.
      • Foreman K.
      • Lim S.
      • Shibuya K.
      • Aboyans V.
      • et al.
      Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: A systematic analysis for the Global Burden of Disease Study 2010.
      ;
      • Vos T.
      • Flaxman A.D.
      • Naghavi M.
      • Lozano R.
      • Michaud C.
      • Ezzati M.
      • et al.
      Years lived with disability (YLDs) for 1160 sequelae of 289 diseases and injuries 1990–2010: A systematic analysis for the Global Burden of Disease Study 2010.
      ). Only FERG estimated foodborne disease hazards.
      2 YLD = years lived with disability; YLL = years of life lost; DALY = disability-adjusted life years.
      Other sources of global disease burden estimates include the WHO Global Health Estimates, the WHO Childhood Epidemiology Reference Group, and the Institute of Health Metrics and Evaluation. A direct comparison of FERG results with those sources is difficult because of differences in methods and assumptions that may have an important effect on burden estimates, but the results are reasonably consistent. Table 2 shows estimates of the disease burden of milkborne hazards considered by different studies. Note that only the FERG study has estimated, for a limited number of hazards, how much of that burden is attributable to dairy products.
      Table 2Quantitative microbial risk assessments on dairy products in low- and middle-income countries
      LocationFoodHazard assessedRiskReference
      Debre Zeit, EthiopiaFermented milkStaphylococcal enterotoxin20 illnesses (90% CI: 14–27) per 1,000 people per year
      • Makita K.
      • Desissa F.
      • Teklu A.
      • Zewde G.
      • Grace D.
      Risk assessment of staphylococcal poisoning due to consumption of informally-marketed milk and home-made yoghurt in Debre Zeit, Ethiopia.
      Debre Zeit, EthiopiaRaw milkStaphylococcal enterotoxin316 illnesses (90% CI: 224–423) per 1,000 people per year
      • Makita K.
      • Desissa F.
      • Teklu A.
      • Zewde G.
      • Grace D.
      Risk assessment of staphylococcal poisoning due to consumption of informally-marketed milk and home-made yoghurt in Debre Zeit, Ethiopia.
      Tigray, EthiopiaRaw milkSalmonella spp.5.72% chance of illness per year for milk consumed on farm; 11.42% for milk collection
      • Weldeabezgi L.T.
      • Atsbha T.W.
      • Kassegn H.H.
      • Gebremichael T.F.
      • Berhe M.H.
      A quantitative risk assessment model for Staphylococcus aureus and Salmonella associated with consumption of informally marketed milk products in Tigray, Ethiopia.
      Tigray, EthiopiaBoiled milkSalmonella spp.1.8% chance of illness per year for milk consumed on farm; 4.02% for milk collection
      • Weldeabezgi L.T.
      • Atsbha T.W.
      • Kassegn H.H.
      • Gebremichael T.F.
      • Berhe M.H.
      A quantitative risk assessment model for Staphylococcus aureus and Salmonella associated with consumption of informally marketed milk products in Tigray, Ethiopia.
      Tigray, EthiopiaFermented milkStaphylococcal enterotoxin2.54% chance of illness per year
      • Weldeabezgi L.T.
      • Atsbha T.W.
      • Kassegn H.H.
      • Gebremichael T.F.
      • Berhe M.H.
      A quantitative risk assessment model for Staphylococcus aureus and Salmonella associated with consumption of informally marketed milk products in Tigray, Ethiopia.
      Tigray, EthiopiaRaw milkStaphylococcal enterotoxin24% chance of illness per year for milk consumed on farm; 48% for milk collection
      • Weldeabezgi L.T.
      • Atsbha T.W.
      • Kassegn H.H.
      • Gebremichael T.F.
      • Berhe M.H.
      A quantitative risk assessment model for Staphylococcus aureus and Salmonella associated with consumption of informally marketed milk products in Tigray, Ethiopia.
      Nairobi, KenyaFormal-sector milkAflatoxin M10.003 cases of cancer per 100,000 (95% CI: 0.000012–0.011) per year
      • Ahlberg S.
      • Grace D.
      • Kiarie G.
      • Kirino Y.
      • Lindahl J.
      A risk assessment of aflatoxin M1 exposure in low and mid-income dairy consumers in Kenya.
      Nairobi, KenyaInformal-sector milkAflatoxin M10.006 cases of cancer per 100,000 people (95% CI: 0.000019–0.018)
      • Ahlberg S.
      • Grace D.
      • Kiarie G.
      • Kirino Y.
      • Lindahl J.
      A risk assessment of aflatoxin M1 exposure in low and mid-income dairy consumers in Kenya.
      Rural KenyaMilkAflatoxin M10.003 cancer cases per year per 100,000 adult females (95% CI: 0.003–0.0039)
      • Sirma A.J.
      • Makita K.
      • Grace D.
      • Senerwa D.
      • Lindahl J.F.
      Aflatoxin exposure from milk in rural Kenya and the contribution to the risk of liver cancer.
      Rural KenyaMilkAflatoxin M10.0014 cancer cases per year per 100,000 adult men (95% CI: 0.0012–0.0015)
      • Sirma A.J.
      • Makita K.
      • Grace D.
      • Senerwa D.
      • Lindahl J.F.
      Aflatoxin exposure from milk in rural Kenya and the contribution to the risk of liver cancer.
      Dagoretti, KenyaInformal milkCryptosporidium oocysts1.02% of children ingesting oocysts per day (90% CI: 0.703–1.4157)
      • Grace D.
      • Monda J.
      • Karanja N.
      • Randolph T.F.
      • Kang'ethe E.K.
      Participatory probabilistic assessment of the risk to human health associated with cryptosporidiosis from urban dairying in Dagoretti, Nairobi, Kenya.
      Dagoretti, KenyaInformal milkCryptosporidium oocysts0.88% of adults ingesting oocysts per day (90% CI: 0.614–1.218)
      • Grace D.
      • Monda J.
      • Karanja N.
      • Randolph T.F.
      • Kang'ethe E.K.
      Participatory probabilistic assessment of the risk to human health associated with cryptosporidiosis from urban dairying in Dagoretti, Nairobi, Kenya.
      Urban East AfricaRaw milkShiga toxin2–3 infections per 10,000 servings (CI: 0–22)
      • Grace D.
      • Omore A.
      • Randolph T.
      • Kang'ethe E.
      • Nasinyama G.W.
      • Mohammed T.
      Assessment for Escherichia coli O157:H7 in marketed unpasteurized milk in selected East African countries.
      South AfricaRaw milkShiga toxin52 cases per 100,000 servings for children and 3.2 for adults
      • Ntuli V.
      • Njage P.M.K.
      • Bonilauri P.
      • Serraino A.
      • Buys E.M.
      Quantitative risk assessment of hemolytic uremic syndrome associated with consumption of bulk milk sold directly from producer to consumer in South Africa.
      South AfricaPasteurized milkShiga toxin47 cases per 100,000 servings for children and 2.9 for adults
      • Ntuli V.
      • Njage P.M.K.
      • Bonilauri P.
      • Serraino A.
      • Buys E.M.
      Quantitative risk assessment of hemolytic uremic syndrome associated with consumption of bulk milk sold directly from producer to consumer in South Africa.
      EgyptRaw marketed milkOrganochlorine pesticidesPotential elevated cancer risk especially among children consuming goat milk
      • Raslan A.A.
      • Elbadry S.
      • Darwish W.S.
      Estimation and human health risk assessment of organochlorine pesticides in raw milk marketed in Zagazig City, Egypt.

      Official Records on Outbreaks

      One must be cautious when extrapolating from outbreak data. Most cases of FBD do not occur as outbreaks but rather as sporadic cases. Moreover, in many countries there is no requirement to report FBD. Even if there is a requirement, the reporting system may not be adequate, resulting in massive underreporting. For example, in Gansu in China, there were an estimated 30 million cases of acute gastrointestinal disease, but only 400 cases were reported to the official system (
      • Sang X.L.
      • Liang X.C.
      • Chen Y.
      • Li J.D.
      • Li J.G.
      • Bai L.
      • Sun J.Y.
      Estimating the burden of acute gastrointestinal illness in the community in Gansu Province, northwest China, 2012–2013.
      ). Even when outbreaks are reported, the investigations may not be comprehensive. Nonetheless, data from outbreak investigations may be the most readily available and reliable source of information in some situations (
      • Pires S.M.
      • Vieira A.R.
      • Hald T.
      • Cole D.
      Source attribution of human salmonellosis: An overview of methods and estimates.
      ).
      In HIC, dairy is responsible for around 1 to 6% of reported outbreaks (
      • Claeys W.L.
      • Cardoen S.
      • Daube G.
      • De Block J.
      • Dewettinck K.
      • Dierick K.
      • De Zutter L.
      • Huyghebaert A.
      • Imberechts H.
      • Thiange P.
      • Vandenplas Y.
      • Herman L.
      Raw or heated cow milk consumption: Review of risks and benefits.
      ). However, these do not include dairy products incorporated into other foods (e.g., custards). When modeling is used to attribute the ingredients of complex foods, the burden of milkborne diseases is higher. Using data from outbreak-associated illnesses for 1998 to 2008,
      • Painter J.A.
      • Ayers T.
      • Woodruff R.
      • Blanton E.
      • Perez N.
      • Hoekstra R.M.
      • Griffin P.M.
      • Braden C.
      Recipes for foodborne outbreaks: A scheme for categorizing and grouping implicated foods.
      estimated annual US foodborne illnesses, hospitalizations, and deaths attributable to each of 17 food commodities. Dairy was responsible for 13.8% of all illnesses, 16.2% of hospitalizations, and 9.7% of deaths.
      • Pires S.M.
      • Vieira A.R.
      • Perez E.
      • Wong D.L.F.
      • Hald T.
      Attributing human foodborne illness to food sources and water in Latin America and the Caribbean using data from outbreak investigations.
      analyzed official records of FBD outbreaks in the Caribbean and Latin America from 1993 to 2010 using a similar method. Overall, animal-source food was responsible for 85% of the food-associated outbreaks and dairy was responsible for 20% of the total outbreaks.
      In HIC there is currently widespread pasteurization, animal disease control, hygienic milking, testing, and cold chains, which are lacking in many LMIC. This would imply that dairy is an important contributor to FBD LMIC. Interestingly, in the United States, drinking raw millk was associated with 840 times as many illnesses as drinking heat-treated milk (
      • Costard S.
      • Espejo L.
      • Groenendaal H.
      • Zagmutt F.J.
      Outbreak-related disease burden associated with consumption of unpasteurized cow's milk and cheese, United States, 2009–2014.
      ). On the other hand, milk consumption is absolutely and relatively higher in HIC, which might imply that milk would contribute less to FBD in LMIC. Latin America and the Caribbean are more representative of LMIC. Here, the contribution of dairy to FBD declined 14-fold over the 2 decades (1990s and 2000s;
      • Pires S.M.
      • Vieira A.R.
      • Perez E.
      • Wong D.L.F.
      • Hald T.
      Attributing human foodborne illness to food sources and water in Latin America and the Caribbean using data from outbreak investigations.
      ). This was associated with rapid growth and formalization of the dairy sector, which has not been seen in most LMIC, where smallholder and informal production continue to predominate.

      Historical Importance of Dairy Products in FBD

      Somewhat analogous to the situation in LMIC today, the 19th century saw many European and North American countries undergoing rapid urbanization, industrialization, and economic growth. This was associated with a decline in the wholesomeness of food as production shifted closer to cities, where conditions were often unhygienic and opportunities for food fraud increased (
      • Grace D.
      • Omore A.
      • Randolph T.
      • Kang'ethe E.
      • Nasinyama G.W.
      • Mohammed T.
      Assessment for Escherichia coli O157:H7 in marketed unpasteurized milk in selected East African countries.
      ). Milk was a major cause of FBD, especially for infants. In the 19th century, typhoid was the major cause of FBD, followed by streptococcal disease and diphtheria, which were mainly attributed to milk (
      • Currier R.W.
      • Widness J.A.
      A brief history of milk hygiene and its impact on infant mortality from 1875 to 1925 and implications for today: A review.
      ), whereas in the mid 20th century, brucellosis and tuberculosis were important. In 1938, milkborne outbreaks accounted for 25% of all disease outbreaks from contaminated food and water in the United States (
      • FDA (Food and Drug Administration)
      Grade “A” pasteurized milk ordinance. Revision 2011.
      ). Introduction of widespread pasteurization of milk has dramtically reduced this disease burden. The pre-pasteurization era in developed countries can be considered analogous to the current situation in many LMIC, and major health benefits can be expected from more broadly adopting pasteruization or other effective processing methods.

      Presence and Prevalence of Hazards in Milk

      The isolation of disease-causing bacteria in raw milk is another indicator of potential risk to human health. As mentioned, the presence of a hazard in food is often a poor guide to the risk to human health. Storage, processing, amount consumed, diet, co-infection, and host factors may contribute to the amplification, reduction, or elimination of risk associated with hazards present in milk. Information on the presence and prevalence of hazards in milk is also useful as benchmarks and in prioritization for subsequent risk assessment. Systematic data from developing countries are largely lacking, but many individual studies have been conducted, and these often find hazards in milk.
      Table 3 sets out hazards of concern, their potential health effects in LMIC, how they enter milk, and the limited evidence for their importance in LMIC (ordinal scale: major, moderate, minor, very low, possible). For milk contamination route, 4 pathways are considered: animal (direct passage from the blood into the milk), udder (udder infection), feces (contamination of milk with animal feces during milking or on-farm storage), and environment (e.g., air, dirty equipment, contaminated water, milker, milk handler). The authors used largely subjective criteria to assess health importance based on their personal experience of working in LMIC. The category “possible” indicates that the role of milk consumption in disease transmission is still ambiguous.
      Table 3Hazards found in milk and dairy products in low- and middle-income countries (LMIC)
      Table adapted and updated from Grace et al. (2007); references given in that paper are not repeated here.
      HazardPotential health importanceImportance in LMIC
      Campylobacter coli and jejuni
      Considered by the World Health Organization Foodborne Disease Burden Epidemiology Reference Group (FERG) in attributing foodborne disease to milk and other animal-source foods.
      MajorHigh prevalence reported in West Africa and Kenya
      Human pathogenic verocytotoxigenic Escherichia coli
      Considered by the World Health Organization Foodborne Disease Burden Epidemiology Reference Group (FERG) in attributing foodborne disease to milk and other animal-source foods.
      Only certain strains of E. coli that are transferred by cattle, which contain a combination of virulence factors and that are pathogenic to humans. Strains of the serotype O157:H7 are the most frequently reported, but strains of other serotypes can result in human cases as well (e.g., O26, O91, O103, O111, O121 and O145).
      MajorUp to 2% of dairy products in Kampala and Nairobi, 10% in Nigeria and Tanzania, and 21% in Libya are positive (
      • Garbaj A.M.
      • Awad E.M.
      • Azwai S.M.
      • Abolghait S.K.
      • Naas H.T.
      • Moawad A.A.
      • Gammoudi F.T.
      • Barbieri I.
      • Eldaghayes I.M.
      Enterohemorrhagic Escherichia coli O157 in milk and dairy products from Libya: Isolation and molecular identification by partial sequencing of 16S rDNA.
      )
      Listeria monocytogenesMajorReported in milk in dairy products in India and Africa
      Mycobacterium bovis
      Considered by the World Health Organization Foodborne Disease Burden Epidemiology Reference Group (FERG) in attributing foodborne disease to milk and other animal-source foods.
      MajorUp to 10% of cases of tuberculosis in some areas. In Tanzania, 10% of the extrapulmonary and 4% of pulmonary cases. FERG has used an estimate of 1%.
      Non-typhoidal Salmonella enterica
      Considered by the World Health Organization Foodborne Disease Burden Epidemiology Reference Group (FERG) in attributing foodborne disease to milk and other animal-source foods.
      MajorHigh; among the most common causes of bacteremia in under-fives and a common cause of meningitis and septicemia
      Staphylococcus aureusMajorMay be important; present in 6% of raw milk samples in Tanzania
      Brucella abortus
      Considered by the World Health Organization Foodborne Disease Burden Epidemiology Reference Group (FERG) in attributing foodborne disease to milk and other animal-source foods.
      ModerateHigh; 40% cows in Africa serologically positive. 35% of raw milk samples produced and sold in peri-urban Bamako in Mali contained antibodies from Brucella abortus.
      Brucella melitensisModerateTypically a disease of small ruminants; in some countries has also been found in cattle at high levels (
      • Kolo F.B.
      • Fasina F.O.
      • Ledwaba B.
      • Glover B.
      • Dogonyaro B.B.
      • van Heerden H.
      • Adesiyun A.A.
      • Katsande T.C.
      • Matle I.
      • Gelaw A.K.
      Isolation of Brucella melitensis from cattle in South Africa.
      )
      Cryptosporidium parvum
      Considered by the World Health Organization Foodborne Disease Burden Epidemiology Reference Group (FERG) in attributing foodborne disease to milk and other animal-source foods.
      ModerateRecent studies have shown a high prevalence in Kenya milk
      DioxinsModeratePeople eating a North American diet ingest 23% of dioxins through dairy products (
      • Grace D.
      • Dominguez-Salas P.
      • Alonso S.
      • Lannerstad M.
      • Muunda E.
      • Ngwili N.
      • Omar A.
      • Khan M.
      • Otobo E.
      The influence of livestock-derived foods on the nutrition of mothers and infants during the first 1,000 days of a child's life. Research Report 44.
      )
      Heavy metalsModerateIn developed countries, dairy products contribute to about 10% of dietary lead, less than 10% of dietary cadmium, and are major contributors of arsenic for children and minor for adults (
      • Grace D.
      • Lindahl J.
      • Kang'ethe E.
      • Harvey J.
      Detecting and preventing contamination of dairy cattle feed.
      )
      Hepatitis A and E virus
      Only genotype 4 of hepatitis E has been found in cattle; genotypes 3 and 4 are zoonotic, but the main host is pigs.
      ModerateHepatitis E is highly prevalent in milk in China (
      • Huang F.
      • Li Y.
      • Yu W.
      • Jing S.
      • Wang J.
      • Long F.
      • He Z.
      • Yang C.
      • Bi Y.
      • Cao W.
      • Liu C.
      • Hua X.
      • Pan Q.
      Excretion of infectious hepatitis E virus into milk in cows imposes high risks of zoonosis.
      ). Hepatitis A is associated with ice cream and milk, among other foods.
      Streptococcus spp.ModerateIn rare cases group A can be spread by milk and milk products; group B is a potential zoonosis; group C are zoonotic and the main origin is animals and dairy products
      Shigella spp.ModerateMilk and dairy have been associated with a few outbreaks, including in India
      Salmonella enterica serovar Typhi and serovar ParatyphiModerateIn HIC,
      HIC = high-income countries.
      dairy products are associated with 25% of typhoid outbreaks of known origin (
      • Glynn J.R.
      • Bradley D.J.
      The relationship between infecting dose and severity of disease in reported outbreaks of salmonella infections.
      ). Reports from LMIC of milk and dairy contamination.
      Vibrio choleraModerateIn Morocco, 7% of dairy products were contaminated; in India, 12% of milk sampled (
      • Sharma D.
      • Malik A.
      Incidence and prevalence of antimicrobial resistant Vibrio cholerae from dairy farms.
      )
      Bacillus cereus (enterotoxigenic)MinorHigh presence in dairy products in Abidjan, India, China, and Thailand (
      • Kumari S.
      • Sarkar P.K.
      Bacillus cereus hazard and control in industrial dairy processing environment.
      )
      Corynebacterium ulceransMinorVery low, reported mainly in HIC, which may be due to reporting bias
      Cronobacter sakazakiiMinorEmerging pathogen associated with rehydrated milk; it has been reported in Asia and Africa (
      • Parra-Flores J.
      • Cerda-Leal F.
      • Contreras A.
      • Valenzuela-Riffo N.
      • Rodríguez A.
      • Aguirre J.
      Cronobacter sakazakii and microbiological parameters in dairy formulas associated with a food alert in Chile.
      )
      PesticidesMinorPesticide residues are often detected in milk in LMIC, including residues from banned pesticides
      MycotoxinsMinorHigh prevalence in tropical feeds; has been detected in milk in East Africa; one study found positive association with stunting
      Rift Valley fever virusMinorDrinking raw milk has been identified as a risk factor, but most risk through slaughter
      Toxoplasma gondii
      Considered by the World Health Organization Foodborne Disease Burden Epidemiology Reference Group (FERG) in attributing foodborne disease to milk and other animal-source foods.
      MinorRaw goat milk has been identified as a source of infection in Ethiopia and Uganda
      Trueperella pyogenesMinorCommon in HIC but not well documented in LMIC. Zoonotic potential unclear.
      Yersinia enterocoliticaMinorIn Morocco, 7% of dairy products were contaminated
      Viruses of the tick-borne encephalitis complexMinorA problem in Europe and Asia. Raw goat milk responsible for several cases.
      Citropbacter freundiiVery lowHas been isolated from milk in Kampala (
      • Kateete D.P.
      • Kabugo U.
      • Baluku H.
      • Nyakarahuka L.
      • Kyobe S.
      • Okee M.
      • Najjuka C.F.
      • Joloba M.L.
      Prevalence and antimicrobial susceptibility patterns of bacteria from milkmen and cows with clinical mastitis in and around Kampala, Uganda.
      ), Cameroon (
      • Moh L.G.
      • Keilah L.P.
      • Etienne P.T.
      • Jules-Roger K.
      Seasonal microbial conditions of locally made yoghurt (shalom) marketed in some regions of Cameroon.
      ), and Ethiopia (
      • Worku T.
      • Negera E.
      • Nurfeta A.
      • Welearegay H.
      Microbiological quality and safety of raw milk collected from Borana pastoral community, Oromia regional state.
      ); considered emerging but few studies in LMIC
      Clostridium botulinumVery lowSpores often detected in feces of cattle and occasionally in milk and dairy products in HIC. Milkborne outbreaks reported in HIC, Kenya, Latin America (
      • Lindström M.
      • Myllykoski J.
      • Sivelä S.
      • Korkeala H.
      Clostridium botulinum in cattle and dairy products.
      ).
      Clostridium perfringensVery lowFew studies conducted in LMIC but reported in milk from Egypt
      Corynebacterium diptheriaeVery lowOften detected in milk but mainly a problem in India, Haiti, and parts of central Africa. Current role of dairy unknown, but historically milk an important vehicle
      HistamineVery lowMicroorganisms in cheese can produce histamine, which can have life-threatening symptoms. Aged cheese is second to fish as a source of disease (
      • Stratton J.E.
      • Hutkins R.W.
      • Taylor S.L.
      Biogenic amines in cheese and other fermented foods: A review.
      ). Importance in LMIC not known.
      Leptospira spp.Very lowCommon in cattle in HIC and LMIC; most infections are transmitted by cattle urine but can be present in milk (
      • Fratini F.
      • Turchi B.
      • Ferrone M.
      • Galiero A.
      • Nuvoloni R.
      • Torracca B.
      • Cerri D.
      Is Leptospira able to survive in raw milk? Study on the inactivation at different storage times and temperatures.
      ).
      Streptobacillus moniliformisVery lowReported in Kenya, Nigeria, and China (
      • Zhang W.W.
      • Hu Y.
      • He G.
      • Zhou Y.
      • Hong L.
      • Ding J.-G.
      Rat bite fever caused by Streptobacillus moniliformis infection in a Chinese patient.
      ). Milk-associated disease only reported from United States.
      Antibiotic residuesPossibleHigh; prevalence of 6% (Mali), 50% (Niger), 36% (Tanzania), 33% (Uganda), and 6–15% (Kenya)
      Coxiella burnetiPossibleUrban outbreaks are increasingly reported and may be associated with milk
      Mycobacterium paratuberculosisPossibleInfections common in cattle; implicated in the pathogenesis of Crohn's disease (
      • Bharathy S.
      • Gunaseelan L.
      • Porteen K.
      Exploring the potential hazard of Mycobacterium avium subspecies paratuberculosis as a cause for Crohn's disease.
      )
      1 Table adapted and updated from
      • Grace D.
      • Randolph T.
      • Omore A.
      • Schelling E.
      • Bonfoh B.
      Place of food safety in evolving pro-poor dairy policy in East and West Africa.
      ; references given in that paper are not repeated here.
      2 Considered by the World Health Organization Foodborne Disease Burden Epidemiology Reference Group (FERG) in attributing foodborne disease to milk and other animal-source foods.
      3 Only certain strains of E. coli that are transferred by cattle, which contain a combination of virulence factors and that are pathogenic to humans. Strains of the serotype O157:H7 are the most frequently reported, but strains of other serotypes can result in human cases as well (e.g., O26, O91, O103, O111, O121 and O145).
      4 Only genotype 4 of hepatitis E has been found in cattle; genotypes 3 and 4 are zoonotic, but the main host is pigs.
      5 HIC = high-income countries.

      Risk Assessments

      Quantitative risk assessment is a predictive or inductive method that assesses risk by combining exposure, dose-response, and severity of health effects. It has been adopted by the Codex Alimentarius Commission and underpins trade in foods and livestock. By taking the core concepts of risk analysis and combining them with proven development analytic methods such as participatory rural appraisal and gender analysis, an approach emerged that could be successfully applied to the food safety challenges in developing countries (
      • Grace D.
      • Randolph T.
      • Karanja N.
      • Kang'ethe E.
      Modular process risk models for better management of Cryptosporidium parvum—An emerging zoonotic pathogen.
      ). The approach was subsequently used in Tanzania, Uganda, Vietnam, and elsewhere, and its strengths and weaknesses as well as the recommendations generated were captured in peer-reviewed publications (
      • Häsler B.
      • Msalya G.
      • Garza M.
      • Fornace K.
      • Eltholth M.
      • Kurwijila L.
      • Rushton J.
      • Grace D.
      Integrated food safety and nutrition assessments in the dairy cattle value chain in Tanzania.
      ;
      • Nguyen-Viet H.
      • Dang-Xuan S.
      • Pham-Duc P.
      • Roesel K.
      • Huong N.M.
      • Luu-Quoc T.
      • Hung P.V.
      • Nga N.T.D.
      • Lapar L.
      • Unger F.
      • Häsler B.
      • Grace D.
      Rapid integrated assessment of food safety and nutrition related to pork consumption of regular consumers and mothers with young children in Vietnam.
      ;
      • Roesel K.
      • Ejobi F.
      • Dione M.
      • Pezo D.
      • Ouma E.
      • Kungu J.
      • Clausen P.-H.
      • Grace D.
      Knowledge, attitudes and practices of pork consumers in Uganda.
      ).
      This approach, involving rapid qualitative and quantitative studies on hazards and risk, has been applied to several dairyborne diseases; many of the studies were conducted by scientists at the International Livestock Research Institute in Kenya. Table 3 summarizes key findings.
      These risk assessments confirm that aflatoxins in milk have lesser known health effects than biological hazards. The risk assessments also suggest that processing milk (boiling, fermentation, or pasteurizing) reduces but does not eliminate risk. Some assessments find relatively high risks for single pathogens, implying that milkborne disease may be more common than the estimates from the FERG. However, bottom-up quantitative risk assessments tend to produce higher estimates of risk than top-down epidemiologic methods.

      Studies on Compliance

      Public food safety standards are enacted to protect consumers' health by ensuring safe food and to eliminate fraudulent practices. Food legislation has typically been designed to set a minimum standard (or agreed level) of safety and quality that society finds acceptable. Historically, many food standards were hazard-based, specifying that a hazard should be absent according to a specified testing method. More recently, standards often seek to incorporate a risk perspective but may also take a precautionary approach. Such standards have been developed mainly in HIC. In the absence of resources and data to define standards that are appropriate for the local context, LMIC often copy standards from HIC. Compliance with standards is only a proxy for food safety, as food may not comply and yet pose little risk and vice versa. In LMIC, it is very common for a substantial proportion of food and feed to fail to comply with standards adopted from HIC, which may cause considerable concern among governments and consumers. Table 4 summarizes some studies on dairy products in Kenya that are not atypical for other LMIC.
      Table 4Dairy products failing to comply with standards in Kenya
      Adapted from Harcourt-Brown et al. (2018).
      SiteSampleFailure to comply with standards
      AM = antimicrobial residues; TVC = total viable count; WHO/FAO = World Health Organization and Food and Agriculture Organization of the United Nations.
      Reference
      Lamu CountyMilk vendor (informal)25% unacceptable composition 18% were outside limit for AM residues 29% failed composition or AM residue
      • Ondieki G.K.
      • Ombui J.N.
      • Obonyo M.
      • Gura Z.
      • Githuku J.
      • Orinde A.B.
      • Gikunju J.K.
      Antimicrobial residues and compositional quality of informally marketed raw cow milk, Lamu West Sub-County, Kenya, 2015.
      NakuruPeri-urban milk43% were outside limit for sulphonimides
      • Orwa J.D.
      • Matofari J.W.
      • Muliro P.S.
      • Lamuka P.
      Assessment of sulphonamides and tetracyclines antibiotic residue contaminants in rural and peri urban dairy value chains in Kenya.
      Nanyukii and IsioloCamel milk75% were outside microbiological limits
      • Kaindi D.M.
      • Schelling E.
      • Wangoh J.
      • Imungi J.K.
      • Farah Z.
      • Meile L.J.
      Microbiological quality of raw camel milk across the Kenyan market chain.
      Not reportedCamel milk92% exceeded TVC 100% exceeded coliform
      • Matofari J.W.
      • Shalo P.L.
      • Younan M.
      • Nanua J.N.
      • Adongo A.
      • Misiko B.N.
      Analysis of microbial quality and safety of camel (Camelus dromedarius) milk chain and implications in Kenya.
      Kisumu and EldoretInformal and pasteurized43% of informal milk and 71% of formal milk did not meet total bacterial count standards
      • Alonso S.
      • Muunda E.
      • Ahlberg S.
      • Blackmore E.
      • Grace D.
      Beyond food safety: Socio-economic effects of training informal dairy vendors.
      NandiRaw and boiled vended60% of raw and boiled milk were outside coliform
      • Ogot H.
      • Ochuodho H.O.
      • Machoka R.
      Microbial Analysis of raw and boiled milk sold at Baraton Center in Nandi County, Kenya.
      NairobiRaw and pasteurized53% exceeded acidity standards 96% of raw and 21% of pasteurized exceeded TVC 78% of raw and 5% of pasteurized exceeded coliform
      • Wanjala G.
      Microbiological quality and safety of raw and pasteurized milk marketed in and around Nairobi region.
      KiambuShop milk64% of milk exceeded coliform 54% exceeded total plate count 27% exceeded adulteration (compositional) 0% exceeded AM residue 0% with hydrogen peroxide
      • Orregård M.
      Quality analysis of raw milk along the value chain of the informal milk market in Kiambu County, Kenya.
      NairobiInformal66% of samples above aflatoxin limits
      • Kuboka M.M.
      • Imungi J.K.
      • Njue L.
      • Mutua F.
      • Grace D.
      • Lindahl J.F.
      Occurrence of aflatoxin M1 in raw milk traded in peri-urban Nairobi, and the effect of boiling and fermentation.
      5 Urban centersFormal31% exceeded the WHO/FAO levels for aflatoxin
      • Kang'ethe E.K.
      • Lang'a K.
      Aflatoxin B1 and M1 contamination of animal feeds and milk from urban centers in Kenya.
      NairobiInformal55% were over EU maximum for aflatoxin
      • Kirino Y.
      • Makita K.
      • Grace D.
      • Lindahl J.
      Survey of informal milk retailers in Nairobi, Kenya and prevalence of aflatoxin M1 in marketed milk.
      Bomet CountyFormalNo aflatoxin in processed milk or UHT
      • Langat G.
      • Tetsuhiro M.
      • Gonoi T.
      • Matiru V.
      • Bii C.
      Aflatoxin M1 contamination of milk and its products in Bomet County, Kenya.
      1 Adapted from
      • Harcourt-Brown L.
      • Alonso S.
      • Lindahl J.
      • Varnell H.
      • Hoffmann V.
      • Grace D.
      Regulatory compliance in the Kenyan dairy sector: Awareness and compliance among farmers and vendors. Project Note.
      .
      2 AM = antimicrobial residues; TVC = total viable count; WHO/FAO = World Health Organization and Food and Agriculture Organization of the United Nations.
      It has been said that when 5% of milk fails to meet standards, there is a problem with milk, but when 90% fails, there may be a problem with standards. The high level of noncompliance, the many different regulations between and sometimes within countries, and the proliferation of regulations in advance of the ability to enforce them raise concerns, and there is an urgent need to develop approaches to develop standards for LMIC that are locally appropriate and focus on the most important health risks rather than hazards that are easily measured. There may also be severe tradeoffs between compliance with food safety regulations and other societal objectives such as food and nutrition security that raise difficult questions. For example, one study in Kenya found that if aflatoxin standards for maize and sorghum were strictly enforced, around 9,000,000 Kenyans would be deprived of the bulk of their diet and about 3,400,000 Kenyans would be deprived of milk (
      • Sirma A.J.
      • Lindahl J.F.
      • Makita K.
      • Senerwa D.
      • Mtimet N.
      • Kang'ethe E.K.
      • Grace D.
      The impacts of aflatoxin standards on health and nutrition in sub-Saharan Africa: The case of Kenya.
      ).

      Appropriate Dairy Safety Regulation: Aflatoxin M1 as an Example

      Discovered in 1960, aflatoxins—toxins produced by certain Aspergillus fungi primarily in maize and nuts—have long been known to cause liver cancer in humans and diverse other adverse effects in humans and animals, including acute toxicity, growth impairment, and immune system dysfunction (
      • Kensler T.W.
      • Roebuck B.D.
      • Wogan G.N.
      • Groopman J.D.
      Aflatoxin: A 50-year odyssey of mechanistic and translational toxicology.
      ;
      • Khlangwiset P.
      • Shephard G.S.
      • Wu F.
      Aflatoxins and growth impairment: A review.
      ;
      • Wu F.
      Global impacts of aflatoxin in maize: Trade and human health.
      ). Lactating animals that consume aflatoxin B1 (AFB1; the most prevalent and toxic of the aflatoxins in maize and nuts) in their feed secrete a metabolite of that toxin in their milk, referred as aflatoxin M1 (AFM1;
      • Kensler T.W.
      • Roebuck B.D.
      • Wogan G.N.
      • Groopman J.D.
      Aflatoxin: A 50-year odyssey of mechanistic and translational toxicology.
      ). Although the human health risks of AFM1 are far from well established, regulatory agencies have set standards for AFM1 in milk and dairy products simply based on taking the existing AFB1 or total aflatoxin standard (in a given nation) and dividing by a factor that roughly estimates how much AFM1 is produced in milk when parent aflatoxin is present in dairy animals' diets (
      • Wu F.
      • Saha Turna N.
      Aflatoxin M1 occurrence in dairy products worldwide: Summary of literature review and policy implications. Feed the Future Innovation Lab for Food Security Policy, Research Paper 153.
      ). Implicit in this calculation is that AFM1 is as toxic as AFB1, which no evidence has shown. Indeed, existing studies suggest that AFM1 toxicity and carcinogenicity are far less than that of AFB1 (
      • EFSA (European Food Safety Authority)
      Risk assessment of aflatoxins in food.
      ). Unfortunately, many policymakers worldwide have assumed that AFM1 is just as toxic as AFB1. Consequently, newspaper headlines have warned people to avoid drinking locally produced milk; this has set back early childhood milk-based nutrition interventions and paralyzed the dairy industry in Ethiopia, for example. Similar headlines have been published in other countries such as Kenya. As ever more nations suffer market losses due to AFM1 in dairy products exceeding regulated levels, especially the stringent EU limit of 0.05 µg/kg, there is a need to better characterize the true human health risk of this chemical in our daily diets in order to inform policy decision making and public health officials on the true nature of the risk.
      For the purposes of sensible policymaking on food safety that does not cause excessive economic loss (
      • Wu F.
      Mycotoxin risk assessment for the purpose of setting international regulatory standards.
      ), there is a critical need to compare both the toxicity of and the exposure to AFM1 with AFB1 to be able to judge relative risks. It is also important to understand whether AFM1, like AFB1, has a synergistic interaction with hepatitis B virus infection to increase liver cancer risk and to compare exposure patterns of these 2 chemicals. In multiple LMIC, high AFM1 contamination levels have been detected in milk (as reviewed in
      • Wu F.
      • Saha Turna N.
      Aflatoxin M1 occurrence in dairy products worldwide: Summary of literature review and policy implications. Feed the Future Innovation Lab for Food Security Policy, Research Paper 153.
      ). This is likely because maize grain and oil seed cakes are used in animal feed, and these can have extremely high aflatoxin levels (
      • Liu Y.
      • Wu F.
      Global burden of aflatoxin-induced hepatocellular carcinoma: A risk assessment.
      ;
      • Liverpool-Tasie L.S.
      • Turna N.S.
      • Ademola O.
      • Obadina A.
      • Wu F.
      The occurrence and co-occurrence of aflatoxin and fumonisin along the maize value chain in southwest Nigeria.
      ). For instance, studies in Ethiopia and Rwanda have identified oil seed cakes as the main source of AFB1 in feed (
      • Gizachew D.
      • Szonyi B.
      • Tegegne A.
      • Hanson J.
      • Grace D.
      Aflatoxin contamination of milk and dairy feeds in the Greater Addis Ababa milk shed, Ethiopia.
      ;
      • Nishimwe K.
      • Bowers E.
      • Ayabagabo J.D.
      • Habimana R.
      • Mutiga S.
      • Maier D.
      Assessment of aflatoxin and fumonisin contamination and associated risk factors in feed and feed ingredients in Rwanda.
      ). There is a need to continue to identify which feed components contribute most to AFB1 exposure of cattle and how to control this contamination.

      ECONOMIC BURDEN OF DAIRYBORNE DISEASE

      Foodborne diseases are associated with a wide range of economic costs. These can be divided into (1) the harm caused by the disease (e.g., lost productivity from illness), (2) the cost of response (e.g., treatment, food recalls), and (3) cost of prevention (e.g., food safety governance, risk-reducing practices). Alternatively, costs may be allocated to different actors (consumer, health care, agro-food industry, government;
      • McLinden T.
      • Sargeant J.M.
      • Thomas M.K.
      • Papadopoulos A.
      • Fazil A.
      Component costs of foodborne illness: A scoping review.
      ). Zoonotic diseases often exert additional burdens on the livestock sector, and it is important that estimates of costs cover multiple sectors. Costs associated with market access and trade are not further discussed in this paper.
      Valuation of health benefits is now an established tool for identifying the highest priorities for public health investments. Although valuation methods have recognized limitations, they can provide insights into the economic cost of illness and the potential value of reducing the burden of illness. It is important to understand the basis for such estimates, as they can be misinterpreted. For example, estimates of the economic burden of FBD in the United States vary from $14 billion to $77 billion due to differences in methodology and pathogen coverage (
      • Hoffmann S.
      • Anekwe T.D.
      Making Sense of Recent Cost-of- Foodborne-Illness Estimates. Economic Information Bulletin Number 118.
      ).
      Gross national income per capita can be used as a measure of lost productivity. Intuitively, for each year lost to illness, disability, or premature death, the economy loses the economic output associated with that year. Using this approach, a recent paper by the World Bank estimated the cost of FBD at US$95.2 billion for LMIC in 2016 (Figure 3;
      • Jaffee S.
      • Henson S.
      • Unnevehr L.
      • Grace D.
      • Cassou E.
      The safe food imperative: Accelerating progress in low- and middle-income countries. Agriculture and Food Series.
      ). Using the FERG estimates that 4% of the FBD burden in term of DALY is due to milk and combining it with the approach used in the aforementioned World Bank paper, this would imply that the economic cost is around US$4 billion, which likely is an underestimate.
      Figure thumbnail gr3
      Figure 3Economic cost per year of foodborne disease in low- and middle-income countries (
      • Jaffee S.
      • Henson S.
      • Unnevehr L.
      • Grace D.
      • Cassou E.
      The safe food imperative: Accelerating progress in low- and middle-income countries. Agriculture and Food Series.
      ). MENA = Middle East and North Africa.

      REDUCING THE HEALTH AND ECONOMIC BURDEN OF DAIRYBORNE DISEASE

      There have been many approaches to improving milk safety and quality in LMIC. Some of the most important, summarized in
      • Grace D.
      Food safety in developing countries: Research gaps and opportunities. White paper.
      , are as follows:
      • Training farmers in hygienic milk production
      • Organizing farmers into dairy co-operatives that can better control quality
      • Linking farmers to a variety of services through dairy hubs to improve milk production
      • Supporting the formal sector processing and retail
      • Training and legitimization of the informal sector
      • Improving consumer awareness on milk handling and safety
      • Technologies that improve health of cattle, such as mastitis detection and treatment
      • Technologies that help preserve milk, such as lactoperoxidase, heating, and chilling
      • Technologies that improve handling of milk, such as wide-necked milk cans
      • Technologies that improve access to information and services, such as obtaining information or making payments using mobile phones
      • Enforcing food safety legislation
      Milk safety can also be improved as a by-product of more general development interventions such as improving road, water, and electricity infrastructure and better primary and secondary education. In most countries these broad-based interventions have been associated with improvement in a wide range of health outcomes.
      Although many of the more specific approaches have had some success, major problems with milk safety persist in many countries (
      • Grace D.
      • Randolph T.
      • Omore A.
      • Schelling E.
      • Bonfoh B.
      Place of food safety in evolving pro-poor dairy policy in East and West Africa.
      ). One key aspect is that most milk is still obtained from informal markets. For example, in Tanzania more than 90% of marketed milk goes through the informal sector (
      • Kilelu C.
      • Klerkx L.
      • Omore A.
      • Baltenweck I.
      • Leeuwis C.
      • Githinji J.
      Value chain upgrading and the inclusion of smallholders in markets: Reflections on contributions of multi-stakeholder processes in dairy development in Tanzania.
      ), and in more urbanized Kenya 86% of milk is informal (
      • Kaitibie K.D.
      • Omore S.
      • Rich A.
      • Kristjanson D.P.
      Kenyan dairy policy change: Influence pathways and economic impacts.
      ). Even in India, the world's top milk producer and which has heavily invested in co-operatives, 83% of the milk is consumed in the unorganized sector (
      • DAHD (India Department of Animal Husbandry and Dairying)
      Cattle and dairy development.
      ). These markets are favored by consumers because, for example, milk is cheaper than that sold in the formal sector, there is more flexibility in the quantity sold, outlets are closer to the consumer's house and some hawkers even deliver to the doorstep, and consumers prefer the taste of unprocessed milk. The lower price of informal-sector milk is especially important to poor consumers. A recent study in Nairobi found that poor households spend 38% of their total food expenditure on livestock products and fish, and of that, 37% was spent on milk and dairy product. In this context, increasing the price of milk could have adverse effects on nutrition (
      • Cornelsen L.
      • Alarcon P.
      • Häsler B.
      • Amendah D.D.
      • Ferguson E.
      • Fèvre E.M.
      • Grace D.
      • Dominguez-Salas P.
      • Rushton J.
      Cross-sectional study of drivers of animal-source food consumption in low-income urban areas of Nairobi, Kenya.
      ).
      Working with the informal sector is likely to be necessary if widespread and rapid improvements in food safety and quality are desired. In Kenya in the early 2000s, a training and certification scheme was designed and launched to improve quality and safety in informal dairy markets by improving the practices of traders and at the same time supporting the livelihoods of dairy value chain actors. The scheme was taken up by a large proportion of eligible traders (with project support). They received capacity-building training in hygienic milk handling and business practices and at the end of training could apply for a certificate from the Kenya Dairy Board that entitled them to legally sell milk. Participant tests before and after training showed that trader knowledge and practices improved, and microbiological tests showed that there was a substantial and significant decrease in unsafe milk. A later economic evaluation found an important reduction in transaction costs attributable to less harassment by authorities, less confiscated equipment, and fewer bribes paid but also fewer losses of milk due to spoilage (
      • Kaitibie K.D.
      • Omore S.
      • Rich A.
      • Kristjanson D.P.
      Kenyan dairy policy change: Influence pathways and economic impacts.
      ).
      There is also much scope to improve milk safety in high-risk communities. Especially relevant are pastoralists who often have high dietary dependence on milk yet risky practices such as drinking raw milk. In these communities, women often play a key role and must be engaged (
      • FAO (Food and Agriculture Organization of the United Nations) and CARE
      Good practices for integrating gender equality and women's empowerment in climate-smart agriculture programmes.
      ).

      CONCLUSIONS

      This paper draws on the literature in order to assess the health and economic burden of milk and dairy products in LMIC and to identify the priority hazards. Much is unknown about the disease burden of milkborne disease. The best estimates come from the FERG study, which suggests that milk and dairy are responsible for 4% of the overall global FBD burden, corresponding to 20 DALY per 100,000 people in 2010. In Africa, the burden is considerably higher at 50 DALY per 100,000 people. This study covers a small number of known pathogens and is likely to underestimate burden. Historical studies and outbreak investigations suggest that between 14 and 25% of all cases of identified FBD are related to dairy. Depending on the hazard and method, quantitative microbial risk assessment gives even higher estimates, but these may be inflated. This high disease burden corresponds to a high economic burden. Taking a conservative estimate of 4% of the FBD, it would correspond to around US$4 billion/yr in poor countries and warrants greater investment in assessing, communicating, and managing dairyborne disease. There are many successful and promising approaches for reducing the burden of dairyborne disease, but caution should be used in their application to avoid unintended consequences such as disempowerment of women or reducing access to dairy. For example, there are many documented cases in which women's control over livestock is diminished with increasing commercialization (
      • Kristjanson P.
      • Waters-Bayer A.
      • Johnson N.
      • Tipilda A.
      • Njuki J.
      • Baltenweck I.
      • Grace D.
      • MacMillan S.
      Livestock and women's livelihoods: A review of the evidence. Discussion Paper 20.
      ).

      ACKNOWLEDGMENTS

      The authors have not stated any conflicts of interest. Travel to the meeting was funded by the American Dairy Science Association.

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