A Systematic Meta-Analysis of Aflatoxin B1 Presence in Red Pepper

Abstract

Aflatoxins are one of the pollutants that can be isolated from the dried food products, especially spices. Since red pepper is one of the most consumed spices all over the world, this research aimed to estimate the prevalence and concen-tration of aflatoxin B1 (AFB1) in different red pepper spices with the help of a systematic review and meta-analysis. Therefore, the articles published between January 2000 and December 6, 2020, were systematically collected from four well-known databases. In this context, 10 articles containing 455 samples in total among 981 articles were included in the meta-analysis according to the determined inclusion and exclusion criteria. According to the analysis results, the AFB1 prevalence of all studies was determined as 50.8%. The lowest and highest AFB1 concentrations were observed in seasoning paprika Korea (0.14 mg/kg) and Turkey (31.13 mg/kg), respectively. The result of this meta-analysis can be used in the evaluation and organization of solution actions to be devel-oped to reduce AFB1 exposure and prevent financial losses through the con-sumption of red pepper spice products.

Keywords

• AFB1
• Contamination
• Food safety
• Aflatoxin
• Red pepper
• Meta-analysis

Kırmızı Biberde Aflatoksin B1 Varlığının Sistematik Derlemesi ve Meta-Analizi

Öz

Aflatoksinler, kuru gıda ürünlerinden, özellikle baharatlardan izole edilebilen kirleticilerden biridir. Kırmızı biber tüm dünyada en çok tüketilen baharatlardan biri olduğu için bu araştırma, sistematik bir derleme ve meta-analiz yardımıyla farklı kırmızı biber baharatlarında aflatoksin B1 (AFB1) prevalansını ve konsantrasyonunu tahmin etmeyi amaçlamıştır. Bu nedenle Ocak 2000 ile 6 Aralık 2020 arasında yayınlanan makaleler, iyi bilinen dört veri tabanından sistematik olarak toplanmıştır. Bu kapsamda 981 makale arasından toplam 455 örnek içeren 10 makale belirlenen dahil etme ve hariç tutma kriterlerine göre meta-analize dahil edilmiştir. Analiz sonuçlarına göre tüm çalışmaların AFB1 prevalansı %50.8 olarak belirlenmiştir. En düşük ve en yüksek AFB1 konsantrasyonları sırasıyla Kore (0.14 mg/kg) ve Türkiye'de (31.13 mg/kg) kırmızı biberlerinde olarak gözlemlenmiştir. Bu meta-analiz sonuçlarının, kırmızı biber baharat ürünlerinin tüketimi yoluyla AFB1 maruziyetini azaltmak ve mali kayıpları önlemek için geliştirilecek çözüm eylemlerinin değerlendirilmesinde ve organizasyonunda kullanılabileceği düşünülmektedir.

Anahtar Kelimeler

• AFB1
• Kontaminasyon
• Gıda güvenliği
• Aflatoksin
• Kırmızı biber
• Meta-analiz

Kaynakça

1. Acaroz, U. (2019). Determination of the total aflatoxin level in red pepper marketed in Afyonkarahisar, Turkey. Fresenius Environmental Bulletin, 28(4A), 3276–3280.
2. Acu, M., & Ozdestan Ocak, Ö. (2019). The methods of analysis used in the determination of aflatoxin levels in foods (In Turkish). Sinop University Journal of Natural Sciences, 4(2), 168–181. DOI: https://doi.org/10.33484/sinopfbd.537820
3. Aksoy, A., Atmaca, E., Yazici, F., Güvenc, D., Gül, O., & Dervisoglu, M. (2016). Comparative analysis of aflatoxin M1 in marketed butter by ELISA and HPLC. Journal of the Faculty of Veterinary Medicine, Kafkas University, 22(4), 619–621. DOI: https://doi.org/10.9775/kvfd.2016.15115
4. Al Ayoubi, M., Solfrizzo, M., Gambacorta, L., Watson, I., & El Darra, N. (2020). Risk of exposure to aflatoxin b1, ochratoxin a, and fumonisin b1 from spices used routinely in Lebanese cooking. Food and Chemical Toxicology, 147, 111895. DOI: https://doi.org/10.1016/j.fct.2020.111895
5. Ardic, M., Karakaya, Y., Atasever, M., & Durmaz, H. (2008). Determination of aflatoxin b1 levels in deep-red ground pepper (isot) using immunoaffinity column combined with ELISA. Food and Chemical Toxicology, 46(5), 1596–1599. DOI: https://doi.org/10.1016/j.fct.2007.12.025
6. Atasoy, A. F., Hayoğlu, İ. A., Korkmaz, A., Kara, E., & Yildirim, A. (2017). A research on the determination of aflatoxin content of traditional home-made isot (In Turkish). Harran Journal of Agricultural and Food Science, 21(1), 35–40.
7. Barani, A., Nasiri, Z., & Jarrah, N. (2016). Natural occurrence of aflatoxins in commercial pepper in Iran. Food and Agricultural Immunology, 27(4), 570–576. DOI: https://doi.org/10.1080/09540105.2016.1148124
8. Beyene, A. M., Du, X., Schrunk, D., Ensley, S., & Rumbeiha, W. K. (2019). High-performance liquid chromatography and enzyme-linked immunosorbent assay techniques for detection and quantification of aflatoxin b1 in feed samples: a comparative study. BMC Research Notes, 12(1). DOI: https://doi.org/10.1186/s13104-019-4538-z

9. Cavus, S., Tornuk, F., Sarioglu, K., & Yetim, H. (2018). Determination of mold contamination and aflatoxin levels of the meat products/ingredients collected from Turkey market. Journal of Food Safety, 38(5), e12494. DOI: https://doi.org/10.1111/jfs.12494
10. Cho, S. H., Lee, C. H., Jang, M. R., Son, Y. W., Lee, S. M., Choi, I. S., Kim, S. H., & Kim, D. B. (2008). Aflatoxin contamination in spices and processed spice products commercialized in Korea. Food Chemistry, 107(3), 1283–1288. DOI: https://doi.org/10.1016/j.foodchem.2007.08.049
11. Colak, H., Bingöl, E. B. & Nazli, B. (2006). Determination of aflatoxin contamination in red-scaled, red and black pepper by ELISA and HPLC. Journal of Food and Drug Analysis, 14(3), 292–296. DOI: https://doi.org/10.38212/2224-6614.2476
12. Cuce, M. (2020). Incidence of aflatoxins, ochratoxin A, zearalenone, and deoxynivalenol in food commodities from Turkey. Journal of Food Safety, 40(6), 1-13. DOI: https://doi.org/10.1111/jfs.12849
13. FAO. (2000). Guidance for industry: action levels for poisonous or deleterious substances in human food and animal feed. Retrieved from: https://www.fda.gov/regulatory-information/search-fda-guidance-documents/guidance-industry-action-levels-poisonous-or-deleterious-substances-human-food-and-animal-feed#afla (Accessed 15.01.2021)
14. FAO. (2003). Mycotoxin Regulations for Food and Feeding stuffs for Countries Surveyed. Retrieved from: http://www.fao.org/3/a-y5499e.pdf (Accessed 15.01.2021)
15. Fofana-Diomande, A., Kouakou, K. J.-M., Aboua, K. N., Traore, K. S., & Dembele, A. (2019). Study of the contamination of some spices from Côte d’ivoire by mycotoxins (AFB1 and OTA). Journal of Chemical, Biological and Physical Sciences, 9(3), 389–399. DOI: https://doi.org/10.24214/jcbps.B.9.3.38999
16. Gunaydin, Ş., & Karaca, H. (2015). Use of natural extracts in control of mold contamination and mycotoxin production (In Turkish). Academic Food Journal, 13(2), 173–182.
17. Hashem, M., & Alamri, S. (2010). Contamination of common spices in Saudi Arabia markets with potential mycotoxin-producing fungi. Saudi Journal of Biological Sciences, 17(2), 167–175. DOI: https://doi.org/10.1016/j.sjbs.2010.02.01
18. Kathuria, S., Mathur, P., Gitau, C. M. W., Khanna, A., Manghnani, R., Rizwan, N., & Duch, E. (2020). Strengthening cross-border value chains opportunities for India and Bangladesh. Retrieved from: http://documents1.worldbank.org/curated/en/234891583753576911/pdf/Strengthening-Cross-Border-Value-Chains-Opportunities-for-India-and-Bangladesh.pdf (Accessed 15.01.2021)
19. Khazaeli, P., Mehrabani, M., Heidari, M. R., Asadikaram, G., & Lari Najafi, M. (2017). Prevalence of aflatoxin contamination in herbs and spices in different regions of Iran. Iranian Journal of Public Health, 46(11), 1540–1545.
20. Kim, S. J., Cheon, S. H., Kim, S. H., & Seo, H. Y. (2020). Determination of aflatoxins in red pepper and kimchi by ultra-high-performance liquid chromatography with fluorescence detection. Analytical Letters, 53(7), 1087–1096. DOI: https://doi.org/10.1080/00032719.2019.1696354
21. Kilic, F., & Tabanligil Calam, T. (2020). Determination of drying and rehydration kinetics of red capia pepper (Capsicum Annuum l.), energy analysis of drying process. Dokuz Eylul University Faculty of Engineering Journal of Science and Engineering, 22(65), 343–352. DOI: https://doi.org/10.21205/deufmd.2020226503
22. Kilic, S., Cam, I. B., Tongur, T., & Kilic, M. (2018). Health risk assessment of exposure to heavy metals and aflatoxins via dietary intake of dried red pepper from marketplaces in Antalya, Southern Turkey. Journal of Food Science, 83(10), 2675–2681. DOI: https://doi.org/10.1111/1750-3841.14322
23. Kilichan, R., & Calhan, H. (2015). Spices the Magic of Cuisines: Determination of spice consumption habits in Kayseri Province (In Turkish). Journal of Tourism and Gastronomy Studies, 3(2), 40–47.
24. Kos, J., Hajnal, E. J., Jajić, I., Krstović, S., Mastilović, J., Šarić, B., & Jovanov, P. (2016). Comparison of ELISA, HPLC-FLD and HPLC-MS/MS methods for determination of aflatoxin M1 in natural contaminated milk samples. Acta Chimica Slovenica, 63(4), 747–756. DOI: https://doi.org/10.17344/acsi.2016.2451
25. Koutsias, I., Kollia, E., Makri, K., Markaki, P., & Proestos, C. (2020). Occurrence and risk assessment of aflatoxin b1 in spices marketed in Greece. Analytical Letters. DOI: https://doi.org/10.1080/00032719.2020.1832509
26. Lakkireddy, K., Kondapalli, K., & Sambasiva Rao, K. R. S. (2014). Aflatoxins in food and feed: the science of safe food. Journal of Food Science and Technology, 3(2), 6–11.
27. Marshall, H., Meneely, J. P., Quinn, B., Zhao, Y., Bourke, P., Gilmore, B. F., Zhang, G., & Elliott, C. T. (2020). Novel decontamination approaches and their potential application for post-harvest aflatoxin control. Trends in Food Science and Technology, 106, 489–496. DOI: https://doi.org/10.1016/j.tifs.2020.11.001
28. Matthews, M., & Jack, M. (2011). Spices and herbs for home and market. Retrieved from: http://www.fao.org/3/i2476e/i2476e00.pdf (Accessed 15.01.2021)
29. Ostry, V., Malir, F., Toman, J., & Grosse, Y. (2017). Mycotoxins as human carcinogens-the IARC monographs classification. Mycotoxin Research, 33(1), 65–73. DOI: https://doi.org/10.1007/s12550-016-0265-7
30. Ozturk Yilmaz, S. (2017). The contamination rate of aflatoxins in ground red peppers, dried figs, walnuts without shell and seedless black raisins commercialized in Sakarya City Center, Turkey. Italian Journal of Food Science, 29(4), 591–598.
31. Pirestani, A., Tabatabaei, S. N., Fazeli, M. H., Antikchi, M., & Baabaei, M. (2011). Comparison of HPLC and Elisa for determination of aflatoxin concentration in the milk and feeds of dairy cattle. Journal of Research in Agricultural Science, 7(1), 71–78.
32. Prime Ministry General Directorate of Legislation Development and Publication. (2011, December 29). Turkish Food Codex Contaminants Regulation (In Turkish). Official Newspaper No:28157. Retrieved from: https://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-8.htm (Accessed 15.01.2021)
33. Reinholds, I., Pugajeva, I., Bavrins, K., Kuckovska, G., & Bartkevics, V. (2017). Mycotoxins, pesticides and toxic metals in commercial spices and herbs. Food Additives and Contaminants: Part B Surveillance, 10(1), 5–14. DOI: https://doi.org/10.1080/19393210.2016.1210244
34. Santos, L., Marín, S., Mateo, E. M., Gil-Serna, J., Valle-Algarra, F. M., Patiño, B., & Ramos, A. J. (2011). Mycobiota and co-occurrence of mycotoxins in capsicum powder. International Journal of Food Microbiology, 151(3), 270–276. DOI: https://doi.org/10.1016/j.ijfoodmicro.2011.09.011
35. Sugita-Konishi, Y., Sato, T., Saito, S., Nakajima, M., Tabata, S., Tanaka, T., Norizuki, H., Itoh, Y., Kai, S., Sugiyama, K., Kamata, Y., Yoshiike, N., & Kumagai, S. (2010). Exposure to aflatoxins in Japan: risk assessment for aflatoxin B1. Food Additives and Contaminants, 27(3), 365–372. DOI: https://doi.org/10.1080/19440040903317497
36. Tosun, H., & Arslan, R. (2013). Determination of aflatoxin B1 levels in organic spices and herbs. The Scientific World Journal, 2013, 1–4. DOI: https://doi.org/10.1155/2013/874093
37. Udomkun, P., Wiredu, A. N., Nagle, M., Müller, J., Vanlauwe, B., & Bandyopadhyay, R. (2017). Innovative technologies to manage aflatoxins in foods and feeds and the profitability of application – A review. Food Control, 76(2017), 127–138. DOI: https://doi.org/10.1016/j.foodcont.2017.01.008
38. Wacoo, A. P., Wendiro, D., Vuzi, P. C., & Hawumba, J. F. (2014). Methods for detection of aflatoxins in agricultural food crops. Journal of Applied Chemistry, 12(1), 1-15. DOI: https://doi.org/10.1155/2014/706291
39. Waśkiewicz, A., Beszterda, M., Bocianowski, J., & Goliński, P. (2013). natural occurrence of fumonisins and ochratoxin a in some herbs and spices commercialized in Poland analyzed by UPLC-MS/MS method. Food Microbiology, 36(2), 426–431. DOI: https://doi.org/10.1016/j.fm.2013.07.006
40. Yogendrarajah, P., Jacxsens, L., De Saeger, S., & De Meulenaer, B. (2014). Co-occurrence of multiple mycotoxins in dry chili (Capsicum Annum L.) samples from the markets of Sri Lanka and Belgium. Food Control, 46, 26–34. DOI: https://doi.org/10.1016/j.foodcont.2014.04.043