The Occurrence and Human Health Impacts of mycotoxins in Somalia

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Food Safety and Toxicology

The Occurrence and Human Health Impacts of mycotoxins in Somalia Ewa Wielogorska, Mark H Mooney, Mari Eskola, Chibundu N Ezekiel, Milena Stranska, Rudolf Krska, and Christopher T. Elliott J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.8b05141 • Publication Date (Web): 29 Jan 2019 Downloaded from http://pubs.acs.org on January 29, 2019

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Journal of Agricultural and Food Chemistry

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The Occurrence and Human Health Impacts of Mycotoxins in

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Somalia

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Ewa Wielogorskaa, b, Mark Mooneyb, Mari Eskolac, Chibundu N. Ezekield, Milena Stranskae,

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Rudolf Krskab, c, Chris Elliottb

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a School

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b

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Queen’s University Belfast, Northern Ireland, United Kingdom

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c

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Natural Resources and Life Sciences, Vienna (BOKU), Konrad Lorenz Str. 20, 3430 Tulln, Austria

of Pharmacy, Queen’s University Belfast, Northern Ireland, United Kingdom

Institute for Global Food Security, Advanced ASSET Centre, School of Biological Sciences,

Center for Analytical Chemistry, Department of Agrobiotechnology (IFA-Tulln), University of

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d

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e Department

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Czech Republic

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Corresponding author’s address: Institute for Global Food Security, Queen’s University Belfast,

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18-30 Malone Road, Belfast BT9 5BN, United Kingdom; e-mail: [email protected];

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phone number: +44(0)28 90974155.

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Mycotoxins are secondary metabolites produced by various moulds, which contaminate many

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staple foods and cause a broad range of detrimental health effects in animals and humans through

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chronic exposure or acute toxicity. As such, the worldwide contamination of food and feed with

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mycotoxins is a significant problem, especially in Sub-Saharan Africa. In this study, mycotoxin

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occurrence in staple foods consumed in Somalia was determined. A total of 140 (42 maize, 40

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sorghum and 58 wheat) samples were collected from a number of markets in Mogadishu, Somalia,

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and analyzed by a UPLC-MS/MS multi-mycotoxin method, encompassing 77 toxins. All of the

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maize samples tested contained eight or more mycotoxins, with AFB1 and FB1 reaching up to 908

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µg/kg and 17,322 µg/kg, respectively, - greatly exceeding the EU limits/guidance values. The

Department of Microbiology, Babcock University, Ilishan Remo, Ogun State, Nigeria. of Food Analysis and Nutrition, University of Chemistry and Technology, Prague,

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average probable daily intake for the sum of fumonisins (FB1+FB2) was 16.70 µg/kg bw/day,

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representing 835% of the recommended provisional maximum tolerable daily intake value of 2

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µg/kg bw/day. A risk characterization revealed the mean national margin of exposure of 0.62 for

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AFB1 with an associated risk of developing primary liver cancer estimated at 75

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cancers/year/100,000 population for white maize consumption alone. The results clearly indicate

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that aflatoxin and fumonisin exposure is a major public health concern with risk management

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actions requiring prioritization in Somalia.

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Keywords: food safety, exposure assessment, mycotoxins, risk characterization, Somalia

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1.Introduction

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Mycotoxins are chemically diverse secondary metabolites produced by filamentous fungi that

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contaminate food commodities in the field and/or during storage, transportation or food

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processing, impacting both human and animal health as well as the feed but also food industry and

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international trade 1. Although mycotoxin contamination of agricultural commodities is a global

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challenge and still occurs in the developed world, good agricultural practices, widely enforced

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legislation have greatly reduced mycotoxin exposure in these populations. However, the risk of

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mycotoxin contamination of food and feed in developing countries is increasing

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environmental, agronomic and socio-economic factors 3. In most developing countries, such as

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those within sub-Saharan Africa (SSA), increased climatic stress and pest activity combined with

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poor storage conditions, favor toxigenic fungal growth and so accumulation of mycotoxins in

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agricultural produce 2, 4.

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due to

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Maize and sorghum are two most important crops in the SSA region with about 300 million people

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depending on maize in Africa alone

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particularly aflatoxins (AFs) and fumonisins (FUMs) and deoxynivalenol (DON), have been

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widely described and their high occurrence in Africa reported 5-10. Consequently, the SSA region

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has suffered from many mycotoxin poisoning incidences, some resulting in fatalities associated

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with acute exposure to AFs and FUMs 7, 11. Apart from acute toxicosis, chronic exposure to AFs

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has been associated with carcinogenicity 12, particularly in conjunction with chronic hepatitis B

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virus (HBV) infection 13, 14. Aflatoxin B1 (AFB1) has been suspected of a causative role in 4.6 to

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28.2% of all global hepatocellular carcinoma (HCC) cases

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between AFB1 and HBV whereby toxin’s potency may increase up to 30 times in individuals with

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HBV 16, increasing liver cancer risk substantially 17. Also, FUMs are suspected of carcinogenicity

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12

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parts of Africa, Central America, and Asia 18. As such, an estimated 40% of the reduction in life

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expectancy in developing countries is related to the presence of mycotoxins in the foods consumed

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by these populations 19.

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What is more, substantial economic losses have been attributed to cereals’ contaminations with

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mycotoxins; around one-third of foodstuffs (1.3 billion metric tons per annum) produced for the

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world's population are lost from the field to consumer

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developing countries 5. In SSA estimated 40% of produce is lost, worth around $4 billion, and

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equivalent to the annual caloric requirement of at least 48 million people 22, with additional export

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losses due to EU regulation amounting to additional $670 million each year 23. Consequently, the

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need for regulations imposing limits on the concentration of mycotoxins in foods and feeds are

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generally recognized in many countries. Governmental and international institutions, including the

5, 6.

Susceptibility of cereals to mycotoxin contamination,

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as a strong synergy is observed

and have been associated with the elevated incidence of human oesophageal cancer in many

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which is especially severe in the

Journal of Agricultural and Food Chemistry

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World Health Organization (WHO), the European Commission (EC) and the US Food and Drug

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Administration (FDA), have thus set specific mycotoxin regulations and established maximum

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tolerated levels of mycotoxins in foodstuffs, dairy products and animal feedstuffs 24-27. Currently,

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over 100 countries, 15 being African, have regulations in setting maximum levels for main

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foodstuffs affected to safeguard consumers from the harmful effects of the most significant

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mycotoxins including AFs, FUMs, ochratoxin A (OTA), deoxynivalenol (DON), zearalenone

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(ZEA), trichothecenes and ergot alkaloids

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management systems in most countries of SSA are either non-existent or not effective enough to

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adequately protect both the public health and economic interests of developing economies 29.

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Somalia has a turbulent recent history with a civil war followed by violent domestic conflicts since

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the collapse of the central Government in 1991. Consequently, the problem of food safety has not

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been prioritized 30, due to food insecurity and famine resulting from natural disasters plaguing the

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region 31. As such, there is no regulations in place and very little information regarding mycotoxin

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occurrence in food and resulting exposure of the Somali population. The only available report on

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mycotoxin concentrations in maize focuses on AFB1, FB1 and DON only, assessed employing

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ELISA 32. Consequently, the goal of this article was to assess multi-mycotoxin occurrence in staple

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foods for the first time in this geographical region. Generated data was employed to assess the

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possible impact of exposure to aflatoxins and fumonisins and could be used to assess the impact

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of other mycotoxins on the health of Somali population. The conclusions of the performed study

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are hoped to encourage further research and bolster initiatives in the region aimed at providing

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safe food to the people of Somalia.

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Nevertheless, both food safety regulation and

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2. Materials and methods

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2.1. Samples

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A market survey three staple Somali foods i.e. maize, sorghum and wheat was performed utilizing

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a multi-analyte LC-MS/MS approach. Approximately 80 percent of domestic cereal output in

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Somalia comes from Bay, Bakool, Lower and Middle Shabelle regions 33 around the larger inter-

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riverine area between the Shabelle and Juba river valleys of southern Somalia (Figure 1,

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Supplementary Material). Maize, sorghum and wheat are harvested in the first monsoon season -

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Gu (long rains) - which lasts between April and June and the second rainy season - Deyr (short

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rains) - that lasts from October to November. A set of 140 samples which included 42 maize (21

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white and 21 yellow maize), 40 sorghum (20 white and 20 red sorghum) 58 wheat (25 locally

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grown and 33 imported) were collected from different local markets in Mogadishu, Somalia,

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between October 2014 and February 2015. Due to the fact that the aim of the study was to perform

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a market survey to reflect real exposure of the Somali consumers living in Mogadishu, samples of

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1 kg were bought from local retailers and shipped to the UK. All samples stored in a dark and dry

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place at 4 °C until their analysis.

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2.2. Sample analysis

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Sample extraction and analysis were performed using a previously validated multi-mycotoxin LC-

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MS/MS method

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employing QuEChERS approach and analysed on an Acquity UPLC I-Class system coupled to a

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Briefly, samples were homogenized to obtain a fine powder, extracted

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Xevo TQ-S triple quadrupole mass spectrometer (both from Waters, Milford, MA). The MS

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system was controlled by MassLynx™ software and data was processed using TargetLynx™

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software (Waters, Milford, MA). The method employed herein was initially, validated for

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distiller’s dried grain, maize and wheat and its performance additionally assessed in white and red

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sorghum for the purpose of the current study. Mycotoxins quantitation was achieved using

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extracted, matrix-matched calibration with blank maize, sorghum and wheat samples spiked before

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extraction, covering seven different calibration ranges depending on the requirements and/or

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sensitivity. Blank samples (