Aflatoxin as a Global Food Safety Problem: Health Effects, Market Impacts, Interventions

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Aflatoxin as a Global Food Safety Problem: Health Effects, Market Impacts, Interventions Felicia Wu, PhD John A. Hannah Distinguished Professor Department of Food Science and Human Nutrition Department of Agricultural, Food & Resource Economics Michigan State University MSU Center for Research on Ingredient Safety (CRIS) Annual Meeting 5 October 2016 1

Outline Aflatoxin: background Regulations on aflatoxin in food Economic impacts of aflatoxin regulations Social network models of world food trade Health impacts Aflatoxin-related liver cancer worldwide Do aflatoxin regulations really protect health? Interventions that control aflatoxin & adverse effects Liver cancer in China: success story 2

Aflatoxin: Background Produced by fungi Aspergillus flavus, A. parasiticus in warm climates Maize, peanuts, tree nuts, cottonseed, spices Africa, south & southeast Asia, southern USA Group 1 human liver carcinogen Synergistic with hepatitis B (HBV): ~30-fold greater liver cancer risk ~400 million people worldwide have chronic HBV; 4.5 billion chronically exposed to aflatoxin Other effects: immune dysfunction, child stunting, acute liver failure 3

To protect populations from aflatoxin, >100 nations have regulatory standards in food Nation Allowable aflatoxin in food ( g/kg) Canada 15 China 20 European Union (EU) 4 Ghana No regulation Guatemala 20 India 30 Kenya 20 United Arab Emirates No regulation USA 20 4

3 questions relevant to these regulations FOOD TRADE. What are the impacts of these aflatoxin standards on global food trade? Which nations are most at risk? HEALTH. Do these aflatoxin standards actually protect human health (and to what extent)? Which nations are most at risk? INTERVENTIONS. How does global health improve when we introduce aflatoxin control methods & dietary diversity? 5

Strict aflatoxin standards can have severe economic impacts $670 million annual loss to African food exporters from attempting to meet EU aflatoxin standard (Otsuki et al. 2001) A World Bank study has calculated that the EU regulation on aflatoxins costs Africa $670 million each year in exports of cereals, dried fruit and nuts. And what does it achieve? It may possibly save the life of one citizen of the EU every two years. Surely a more reasonable balance can be found. Kofi Annan, former UN Secretary General Vardon et al. (2003): nearly $1 billion annual loss in US from 3 mycotoxins Milder estimate: $450 million annual loss to ALL food exporters ($40 million loss to African exporters) if ALL nations adopted EU standard - Wu F (2004). Mycotoxin Risk Assessment for the Purpose of Setting International Regulatory Standards. ES&T 38:4049-55. 6

Conversely: who experiences health benefits of stricter aflatoxin standards? JECFA (FAO/WHO) 1998: health effects of tightening global aflatoxin standard from 20 to 10 g/kg Where 25% population has HBV, tighter standard reduces liver cancer by 300 cases per year per billion persons Where 1% population has HBV, tighter standard reduces liver cancer by 2 cases per year per billion persons Undetectable by epidemiological methods Where are the populations with hepatitis B? High HBV populations: China (major food exporter), Africa Low HBV populations: most of industrial world (food importers!) 7

Countervailing risks Health policy dilemma: Regions that can t afford to set strict aflatoxin standards get more contaminated food, & often have more HBV Regions that import this higher-quality food (EU, Japan, Canada, Taiwan) experience insignificant health benefit Is this in fact true? We developed global network models of maize & pistachio trade to find out 8

Impact of aflatoxin regulations on world food trade: Insights from network models Network model = Collection of nodes, joined in pairs by edges Friendships, co-authors, roads, trade Why network models are useful Do trade clusters emerge? If drought or crop disease hits one nation, which other nations are affected? How do food safety regulations affect global trade patterns? 9

Collected global maize & pistachio trade data Maize: 2000-2009 Pistachios: 1996-2010 Developed global network models for trade for each year Determined impact of aflatoxin regulations on trade patterns How we developed global trade networks for maize & pistachios Data sources: United Nations Commodities Trade Database (UN Comtrade) Iranian Pistachio Association Trade Database USDA Foreign Agricultural Service Global Agricultural Trade System (GATS) Food and Agriculture Organization (FAO) mycotoxin regulation reports: 1995, 2003 European Union (EU) Rapid Alert System for Food & Feed (RASFF) Network model software: Pajek TM 10

Top exporters of maize worldwide: Three trading clusters emerge Wu F, Guclu H (2013). Global maize trade and food security: Implications from a social network model. Risk Analysis 33:2168-78.

Vulnerabilities revealed in global maize trade US at center of star-shaped cluster Nations with high maize consumption that import exclusively from US are vulnerable to US supply changes Drought, plant disease may reduce supply US maize ethanol production: in 2007, riots in 22 nations Conversely, who is less vulnerable? Nations that are well-connected Nations near center of maize trade network 12

Aflatoxin standards vary widely across nations: Effects on food trade? 13

Nations trade maize with nations that have similar aflatoxin standards Wu F, Guclu H (2012). PLOS ONE 7(9):e45141 14

Top maize-trading pairs have near-identical AF standards Top pairs & their total aflatoxin (AF) standards in µg/kg maize Rank Total amount (MT) Exporter AF standard Importer AF standard 1 USA 20 Japan 20 159,377,000 2 USA 20 Mexico 20 69,764,700 3 USA 20 Taiwan 15 44,212,000 4 USA 20 Korea 20 41,657,300 5 China 20 Korea 20 36,446,400 6 USA 20 Egypt 20 35,540,100 7 USA 20 Canada 15 25,933,000 8 USA 20 Colombia 20 21,726,900 9 Canada 15 USA 20 21,161,900 10 France 4 Spain 4 18,682,400 11 France 4 Netherlands 4 14,901,600 12 Brazil 30 Iran 30 12,588,000 13 Mexico 20 USA 20 10,947,000 14 Argentina 20 Chile 5 10,625,700 15 USA 20 Algeria 20 10,457,700 16 USA 20 Dominican Rep. 20 10,325,300 17 Argentina 20 Spain 4 10,311,600 18 China 20 Malaysia 35 10,119,800 19 France 4 UK 4 9,899,890 20 Argentina 20 Egypt 20 9,734,360 15

Do nations aflatoxin regulations affect global pistachio trade? Global pistachio market dominated by Iran and US Iran (50%) US (25%) Pistachios commonly contaminated with aflatoxin Pistachios contribute 7-45% of aflatoxin in human diets Aflatoxin levels in Iranian pistachios: avg 54 ng/g (JECFA 2007) Aflatoxin levels in US pistachios < 15 ng/g Which nations differentially import from Iran vs. US? Do aflatoxin regulations play a role?

Tons Number of RASFF Rejections EU used to import Iranian pistachios; now imports US pistachios Exports to EU, and Rejections by EU 90000 600 80000 500 70000 60000 400 50000 300 40000 30000 200 20000 USA Rejections 10000 100 Iran Rejections Iran-EU Exports 0 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 Year 0 US-EU Exports

In 1996, Iran was major pistachio exporter to EU & worldwide USA IRAN Iran total: >120k tons US total: 22k tons Iran-EU: 85k tons US-EU: 4k tons Iran: No reg. for pistachios US: 15 ng/g

Next year, high aflatoxin levels (up to 400 ng/g) drove Iranian exports to EU down dramatically USA IRAN Iran total: 55k tons US total: 26k tons Iran-EU: 17k tons US-EU: 8700 tons

In 2003, US started exporting large amounts of pistachios to EU; Iran shifted markets USA IRAN Iran total: 154k tons US total: 35k tons Iran-EU: 33k tons US-EU: 23k tons Iran Reg: 15 ng/g EU: 4 ng/g

Recently, US became main pistachio exporter to EU USA IRAN Iran total: 116k tons US total: 129k tons Iran-EU: 19k tons US-EU: 63k tons

US vs. Iran Pistachio Export Share: Clear evidence of market segregation

Iran vs. Greece Export Share Grape Control Crop: No evidence of market segregation Bui-Klimke TR, Guclu H, Kensler TW, Yuan J-M, Wu F (2014). Aflatoxin Regulations and Global Pistachio Trade: Insights from a Social Network Analysis. PLOS ONE 9(3):e92149

Conclusions from network models of world food trade When nation sets food safety standard, ripple effects all over world (disturbing one part of web) Aflatoxin regulations associated with global food trade patterns Nations trade more food with other nations that have identical or similar AF standards Nations with more relaxed standards import food with higher AF contamination These patterns exist irrespective of other political factors Who is vulnerable? Low-income nations depending on food trade (exports or imports) with relaxed or nonexistent AF standards Nations that import staple food only from one other nation 24

Meanwhile, what are the health impacts of aflatoxin exposure worldwide today? Focus on liver cancer Dose-response assessment Exposure assessment Slope of curve = cancer potency Aflatoxin HCC: 0.01 cases / 100,000 / yr / ng/kg bw/day Aflatoxin+HBV HCC: 0.30 cases / 100,000 / yr / ng/kg bw/day (JECFA 1998) Find, for each nation: Daily consumption of maize / nuts Aflatoxin levels in maize / nuts HBV prevalence Population size Captured 5.96 billion people 25

Risk characterization: Simplified model Global population cancer risk = Σ (all nations) ([Population HBV+ /100,000 * Potency HBV+ * Average aflatoxin intake] + [Population HBV- /100,000 * Potency HBV- * Average aflatoxin intake]) Potency HBV+ = 0.30 cases per 100,000/yr per ng/kg bw/day Potency HBV- = 0.01 cases per 100,000/yr per ng/kg bw/day Data Sources: HBV prevalence: WHO, multiple peer-reviewed papers Aflatoxin exposure & food consumption: FAOSTAT, multiple peerreviewed papers 26

Results: 25,200-155,000 global aflatoxininduced liver cancer cases/yr ~5-28% of all liver cancer cases Liu Y, Wu F. (2010). Global Burden of Aflatoxin-Induced Hepatocellular Carcinoma: A Risk Assessment. Environmental Health Perspectives 118:818-824. Is this bad? 27

Whether nations aflatoxin standards are adequate depends on what is acceptable risk. Don t increase cancer risk by >1/100,000 cases in population Almost no nations have adequately protective aflatoxin standards Exceptions: European nations Scandinavian nations could have AF standard as high as 82 ppb and still meet this low risk level! Ironically, EU has strictest AF standards in world Don t increase cancer risk by >1/10,000 cases in population Almost all nations have adequately protective aflatoxin standards Exceptions: Kenya (20 ppb) & Peru (15 ppb) Both nations have high maize consumption and high HBV Cannot afford to have much aflatoxin in their maize Wu F, Stacy SL, Kensler TW. (2013). Global risk assessment of aflatoxins in maize and peanuts: Are regulatory standards adequately protective? Tox Sci 135:251-9. 28

Interventions to reduce aflatoxin risk Preharvest Good agricultural practices Genetically enhancing plants resistance Biocontrol Postharvest Improved sorting, drying, food storage Dietary Improved dietary variety Dietary enterosorbents Dietary chemoprevention Curcumin Compounds in cruciferous & Allium vegetables Green tea polyphenols Hepatitis B vaccine

Geographic Pathology Liver Cancer Mortality by Township: < 1 per 10 5 /yr Jiangsu Province > 50 per 10 5 /yr Qidong 1.2 million residents Shanghai

Why was liver cancer so high, and what happened in Qidong since 1980? 1920-1980: Maoist agrarian socialism in China Each county must be self-sufficient No imports/exports allowed between counties Qidong: soil unsuitable for planting rice Consumed 82-124 kg maize/yr infected with Aspergillus flavus HIGH AFLATOXIN EXPOSURE: some years, 99% maize > 20 µg/kg AF Not allowed to purchase rice 1980: China relaxes agrarian socialism 1987: >97% Qidongese consume some rice 1998: <9% Qidongese ate any maize 2012: hardly any maize consumed 31

Since 1980, aflatoxin biomarkers decreased dramatically in Qidong 500 500 95 %ile 75 Aflatoxin (pg/mg of albumin) 50 20 10 5 2 1 0.5 Observ ations <0.5 pg/mg 50 25 n=0 n= 0 n= 2 n= 8 n= 24 n= 77 n= 93 95 50 20 10 5 2 1 0.5 0.2 75 0.2 0.05 50 0.05 Guangxi 1982 N= 77 HeZuo 1989 N= 75 Daxin 1995 Daxin 1999 HeZuo 2003 HeZuo 2009 Daxin 2012 N= 100 N= 100 N= 100 N= 100 N= 100

Reduced aflatoxin exposures, not HBV status, are associated with declining liver cancer mortality in Qidong (Chen et al. CaPR 2013).

What relatively aflatoxin-free crops could become dietary staples in Africa? Instead of only focusing on how to reduce aflatoxin in maize & nuts, consider increasing dietary variety or switching staple crops altogether Africa s indigenous crops Sorghum Millet Cowpea Pigeonpea Fonio (West Africa) Teff (northeastern Africa) Rice (some varieties native to Africa) These come with potential problems, but rarely Aspergillus Wu F, Mitchell NJ, Male D, Kensler TW (2014). Reduced foodborne toxin exposure is a secondary benefit of dietary diversity. Toxicological Sciences 141:329-34. 34

Conclusions >100 nations have aflatoxin standards to protect human health But regulations may not have the direct protective effects intended (indirect effects are important, though) And they may affect other countries economies and health Aflatoxin-related liver cancer highest in sub-saharan Africa, Southeast Asia, & China Recent agricultural policy changes improved liver health in China by indirectly lowering aflatoxin exposure While many interventions exist, long-term solutions should include switching to staple crops that are less infected with Aspergilli In China, switch was made in <7 years, but other parts of world not same Meanwhile, we must continue foci of reducing aflatoxin in maize & nuts