Aflatoxin contamination of dried red chilies: Contrasts between the United States and Nigeria, two markets differing in regulation enforcement

Highlights

• Chilies are a source of exposure to the human carcinogen Aflatoxin B₁ (AFB₁).

• Over 60% of chilies purchased in US and Nigerian markets contained AFB₁.

• Two percent of US and 7% of Nigerian chilies were unfit for human consumption.

• Chilies from Nigeria contained more fungi and AFB₁ than US chilies.

• Post-harvest processing influences potential for AFB₁ formation.

Abstract

Dried red chilies are among the world’s most consumed spices. From farm to fork, chilies go through cropping, harvest, drying, processing and storage. Chilies are susceptible to infection by aflatoxin producing fungi and subsequent contamination by aflatoxins at every stage. Aflatoxins are highly regulated, hepatotoxic carcinogens produced by fungi in Aspergillus section Flavi. The current study examined prevalence of aflatoxin B₁ (AFB₁) in chilies from markets across the United States (US) and Nigeria, and determined predisposition of chilies to aflatoxins post-harvest. Aflatoxin B₁ was detected in 64% chilies from US markets (n = 169), and 93% of Nigerian chilies (n = 55) with a commercial lateral flow assay (Limit of Detection = 2 μg/kg). Two percent of US samples exceeded the aflatoxin regulatory limit of 20 μg/kg, while the highest concentration detected was 94.9 μg/kg. Aspergillus spp. could be recovered only from 40% of samples from the US, and aflatoxin levels did not correlate with quantities of Aspergillus section Flavi (Colony Forming Units g⁻¹), suggesting fungi associated with chilies in US markets were killed during processing. Both average AFB₁ concentrations and fungal quantities were significantly higher (p < 0.01) in Nigerian chilies. The most contaminated sample contained 156 μg/kg AFB₁. Aflatoxin concentrations in Nigerian chilies increased as an exponential function of the quantities of Aspergillus section Flavi (r² = 0.76). Results indicate that high rates of chili consumption may be associated with unacceptable aflatoxin exposure.

Introduction

Dried red chili (Capsicum spp.), a member of the nightshade family of Solanacea, is used to enhance flavor, taste and aroma of foods. Chilies are native to the new world where they were domesticated about 6000 years ago (Perry et al., 2007). The economically notable species of Capsicum are C. annuum, C. baccatum, C. chinense, C. frutescens, and C. pubescens (Perry et al., 2007). Dried red chili is consumed across the globe in whole, crushed and ground forms. It stands second among spices in global consumption after black pepper (Piper nigrum) (Yogendrarajah, Jacxsens, De Saeger, & De Meulenaer, 2014). Over 80% of red chili is produced in tropical or sub-tropical regions (FAOSTAT, 2017). During the past decade, India, China and Thailand produced almost half of the world’s dried chilies (FAOSTAT, 2017).

Fungal infection and subsequent mycotoxin contamination of chilies are affected by environmental conditions, with high temperatures and humidity favoring infection (El Mahgubi et al., 2013, Iamanaka et al., 2007, Iqbal et al., 2010). Red chilies available in commercial markets are frequently contaminated with unacceptable concentrations of aflatoxins (Bircan, 2005, Paterson, 2007, Reddy et al., 2001). This can be attributed to pre and/or post-harvest colonization of chilies by aflatoxin producing Aspergillus species. Inadequate conditions during drying, followed by poorly sheltered transport and storage can exacerbate contamination levels (Duman, 2010, Jalili and Jinap, 2012).

Aflatoxins in food and feed are of global concern because aflatoxins are highly toxic fungal metabolites that cause human cancer, immune suppression, and stunting (Khlangwiset et al., 2011, Liu and Wu, 2010, Mehl et al., 2012, Schatzmayr and Streit, 2013, Williams et al., 2004, van Egmond and Jonker, 2004). Several Aspergilli belonging to section Flavi cause aflatoxin contamination of a wide range of crops including maize, groundnuts, tree nuts, cottonseed and spices (Doster and Michailides, 1994, Jaime-Garcia and Cotty, 2003, Probst et al., 2014, Tansakul et al., 2013). Aflatoxin B₁ is the only mycotoxin classified as group 1 human carcinogen by the International Agency for Research on Cancer (International Agency for Research on Cancer, 2002). Aflatoxins are stringently regulated in the developed world, resulting in huge economic losses. Aflatoxin contamination of food and feed can result in annual losses of more than $500 million in the US alone (Robens and Cardwell, 2003, Vardon et al., 2003). In developing countries, aflatoxin is both an economic threat and a health concern. Many developing countries do not enforce aflatoxin regulations in crops, resulting in exposure of humans to chronic and acute health risks (Shephard, 2003, Williams et al., 2004). Food and feed contaminated with aflatoxin concentrations above legislated limits can face border rejections, and loss of both markets, and product value. The European Union (EU) regulates AFB₁ at 5 μg/kg and total aflatoxins at 10 μg/kg in spices (European Spice Association, 2004). Chili shipments to the EU from several nations are rejected every year due to aflatoxin contamination (RASFF, 2015).

Most dry chilies in retail markets across the US are imported (FAOSTAT, 2017). Over 100,000 tonnes of dried red chili are imported annually into the US. Aflatoxins are regulated at 20 μg/kg in the US in foods for human consumption. This regulation can have a severe impact on the value of crops intended for US markets. Nigeria accounts for about 50% of chili production on the continent of Africa (FAOSTAT, 2017, Mohammed et al., 2015). Chilies are an integral part of Nigerian cuisine. Although, Nigeria regulates AFB₁ at 20 μg/kg (FAO, 2004), these regulations are less effectively enforced, leading to chronic exposure (Omojokun, 2013, Williams et al., 2004). The current study sought to: (i) contrast prevalence of aflatoxin contamination in dried red chili from markets in US with those from markets in Nigeria, (ii) determine the relationship between quantities of Aspergillus section Flavi and aflatoxin concentrations, and (iii) test potential for post-harvest contamination of market-purchased chilies.