Contamination of honey products by Clostridium botulinum spores and fungi along with their effects on human health

Document Type : Reviewers

Authors

1 Department of Cardiology, School of Medicine, Shahid Madani Hospital, Lorestan University of Medical Sciences, Khorramabad, Iran

2 Catholic University of Cuenca, Azogues campus, Ecuador, University of Palermo, Buenos Aires, Argentina & National University of Education, Azogues, Ecuador; CES University, Colombia

3 Department of Nursing, Altoosi University College, Najaf, Iraq

4 Refrigeration & Air-conditioning Technical Engineering Department, College of Technical Engineering, The Islamic University, Najaf, Iraq

5 Experiential Learning Center Lead, Department of Nursing, University of Calgary in Qatar, Doha, Qatar

6 Department of Biomedical Engineering, Al-Mustaqbal University College, Babylon, Iraq

7 Department of Chemistry, College of Science, University of Babylon, Babylon, Iraq

8 Department of Food Hygiene and Safety, School of Public Health, Shahid Sadoughi University of Medical Sciences, Yazd, Iran

9 Department of Food Hygiene and Quality Control, Faculty of Veterinary, Shahrekord University, Shahrekord, Iran

10 Department of Environmental Health, Food Safety Division, Faculty of Public Health, Tehran University of Medical Sciences, Tehran, Iran

10.22124/cjes.2022.6095

Abstract

Bee products, such as honey, are widely consumed as food and medicine. Because of its sticky nature, honey does absorb bacterial spores from dust or bee activity, and their contamination may carry serious health hazards. Databases searched to obtain articles included “Google Scholar”, “SID”, “Scopus”, “PubMed”, “Science Direct”, and “ISI”. Keywords used in this study included Clostridium botulinum, Honey, bees, fungi in their titles. This study focused on published articles from 2016 to 2022. Result showed that this product may contain a great variety of bacteria and particularly, fungi that eventually entered the food chain at an early stage (e.g., via pollen). The ranges of samples with C. botulinum, yeast and mould infections were 0.5% - 68%, 15.78% - 100% and 17.22 - 100%, respectively. Overall, the amount of honey contaminated with Cl. botulinum spores, yeast, and molds in some of the samples that were evaluated was nil, however certain samples from the Lithuanian Kazakh, Turkey, and Brazil regions exhibited varying levels of contamination.

Keywords

References

Abbasi, N, Khalighi, Z, Eftekhari, Z & Bahmani, M 2020, Extraction and phytoanalysis of chemical compounds of Eucalyptus globulus leaf native to Dehloran, Ilam Province, Iran by HS-SPME and GC-MS. Advances in Animal and Veterinary Sciences, 8: 647-652.
Aureli, P, Franciosa, G & Fenicia, L 2002, Infant botulism and honey in Europe: a commentary. The Pediatric Infectious Disease Journal, 21: 866-868.
Bahmani, M, Jalilian, A, Salimikia, I, Shahsavari, S & Abbasi, N 2020, Phytochemical screening of two Ilam native plants Ziziphus nummularia (Burm. f.) Wight & Arn. and Ziziphus spinachristi (Mill.) Georgi using HS-SPME and GC-MS spectroscopy. Plant Science Today, 6: 275-80.
Bayrakal, GM, Ekici, G, Akkaya, H, et al. 2020, Detection and molecular examination of pathogens in honey and bees in the northern Marmara Region, Turkey. Kafkas Universitesi Veteriner Fakultesi Dergisi, 26: 313-319, DOI: 10.9775/kvfd.2019.22845.
Brčina, T, Seferović, S, Husejnagić, D, et al. 2021, Health safety and sensory properties of honey from two different areas in Tuzla Canton. International Journal for Research in Applied Sciences and Biotechnology, 8: 20-24.
Cenet, M, Bozdogan, A, Sezer, G, Acar, L, Ulukanli, Z 2017, Antimicrobial activities, pollen diversity and physicochemical properties of natural honey from Southeastern Anatolia of Turkey. Advancements in Life Sciences 4: 47-54,
Doudach, L, Al-mijalli, SH, Abdallah, EM, Mrabti, HN, Chibani, F, et al. 2022, Antibacterial Evaluation of The Roots of Moroccan Aristolochia longa Against Referenced Gram-positive and Gram-negative Bacteria. Advancements in Life Sciences 9: 116-121.
Ebrahimi, Y, Hasanvand, A, Safarabadi, AM, Sepahvand, H, Moghadasi, M & Abbaszadeh, S 2019, A review of the most important herbal drugs effective in chest pain due to cardiac disease. Anaesthesia, Pain & Intensive Care, 3 (23): 1.
Ebrahimi, Y, Hasanvand, A, Valibeik, A, Ebrahimi, F & Abbaszadeh S 2019, Natural antioxidants and medicinal plants effective on hyperlipidemia. Research Journal of Pharmacy and Technology, 31: 1457-1462.
Fernández, LA, Ghilardi, C, Hoffmann, B, Busso, C, et al. 2017, Microbiological quality of honey from the Pampas Region (Argentina) throughout the extraction process. Revista Argentina de Microbiología, 49: 55-61.
Finola, MS, Lasagno, MC & Marioli, JM, 2007, Microbiological and chemical characterization of honeys from central Argentina. Food Chemistry, 100: 1649-1653.
Galhardo, D, Garcia, RC, Schneider, CR, et al. 2020, Microbiological quality of honey samples from Western Paraná, Southern Brazil. Journal of Apicultural Science, 64: 209-218.
Grabowski, N, Klein, G, 2017, Microbiology and foodborne pathogens in honey. Critical Reviews in Food Science and Nutrition, 57: 1852-1862.
Grenda, T, Grabczak, M, Sieradzki, Z, et al. 2018, Clostridium botulinum spores in Polish honey samples. Journal of Veterinary Science, 19: 635-642.
Hajimohammadi, B, Dehghani, A, Javadzadeh, M, et al. 2017, Clostridium botulinum spores and fungal contamination in honeys of Iran. Tolooebehdasht, 15: 1-9.
Hasanvand, A, Ebrahimi, Y, Mohamadi, A, Nazari A 2019, Zingiber officinale Roscoe reduces chest pain on patients undergoing coronary angioplasty: A clinical trial. Journal of Herbmed Pharmacology, 8: 47-50. DOI: 10.15171/jhp.2019.08.
Heidari, S, Fotouhi Ghazvini, R, Zavareh, M & Kafi, M 2018, Physiological responses and phytoremediation ability of Eastern Coneflower (Echinacea purpurea) for crude oil contaminated soil. Caspian Journal of Environmental Sciences, 16: 149-164, DOI: 10.22124/cjes.2018.2957
Hocine, L, Tefiel, B, Moustapha, A, et al. 2018, Microbiological and physicochemical quality of honeys from South and South-West of Niger. Journal of Food and Nutrition Research, 6: 406-413.
Janbakhsh, S, Hosseini Shekarabi, S & Shamsaie Mergan, M 2018, Nutritional value and heavy metal content of fishmeal from the Southwest Caspian Sea. Caspian Journal of Environmental Sciences, 16: 307-317, DOI: 10.22124/cjes.2018.3200
Kazeminia, M, Mahmoudi, R, Aali, E & Ghajarbygi, P 2021, Evaluation of authenticity in honey samples from Qazvin, Iran. Journal of Chemical Health Risks, 11: 1.
Kiš, M, Furmeg, S, Jaki Tkalec, V, et al. 2018, Characterisation of Croatian honey by physicochemical and microbiological parameters with mold identification. Journal of Food Safety, 38(5):12492.
Koike, H, Kanda, M, Hayashi, H, et al. 2020, Development of an alternative approach for detecting botulinum neurotoxin type A in honey: Analysis of non-toxic peptides with a reference labelled protein via liquid chromatography-tandem mass spectrometry. Food Additives & Contaminants: Part A, 37: 1359-1373.
Landeka, V, Cvrtila, Ž, Kozačinski, L, et al. 2022, Microbiological and physicochemical quality of honey in Bosnia and Herzegovina. Veterinarska stanica, 53(5).
Maikanov, B, Mustafina, R, Auteleyeva, L, et al. 2019, Clostridium botulinum and Clostridium perfringens occurrence in Kazakh honey samples. Toxins, 11:472.
Manouchehri, A, Ghareghani, S, Shamaei, S, Nilechi. M, Bossaghzadeh, F 2021, A review on Aluminum phosphide (Rice Tablets) Poisoning; From Exposure to the Applicable and New Strategies of Clinical Management. Advancements in Life Sciences 8: 326-332.
Manouchehri, A, Pirhadi, M, shokri, S, et al. 2021, The possible effects of heavy metals in honey as toxic and carcinogenic substances on human health: a systematic review. Uludağ Arıcılık Dergisi, 2: 237-246.
Matović, K, Ćirić, J, Kaljević, V, et al. 2018, Physicochemical parameters and microbiological status of honey produced in an urban environment in Serbia. Environmental Science and Pollution Research, 25:14148-57.
Matović, K, Mišić, D, Karabasil, N, et al. 2019, Clostridium botulinum spores in European honey bees from Serbia. Journal of Apicultural Research, 58: 420-426.
Naila, A, WN, J, Abdul Hannan, N, et al. 2022, Microbiological and physiochemical quality of honey imported into the Maldives. ACS Food Science & Technology. 2: 836-843.
Namini, NZ, Mousavi, M, Mahmoudi, R, et al. 2018, Hygienic quality of the honey samples produced in the Iran in comparison with international standards. International Food Research Journal, 25(3).
Nardoni, S, D'Ascenzi, C, Rocchigiani, G, et al. 2016, Occurrence of moulds from bee pollen in Central Italy-A preliminary study. Annals of Agricultural and Environmental Medicine, 23(1).
Nevas, M, Lindström, M, Hautamäki, K, et al. 2005, Prevalence and diversity of Clostridium botulinum types A, B, E and F in honey produced in the Nordic countries. International Journal of Food Microbiology, 105: 145-150.
Nevas, M, Lindström, M, Hörman, A, et al. 2006, Contamination routes of Clostridium botulinum in the honey production environment. Environmental Microbiology, 8: 1085-1094.
Pasias, I. N, Kiriakou, I. K, Kaitatzis, A, et al. 2018, Effect of late harvest and floral origin on honey antibacterial properties and quality parameters. Food Chemistry, 242: 513-518.
Pinheiro, C, Abrantes, MR, Silva, ROS, et al. 2018, Microbiological quality of honey from stingless bee, jandaíra (Melipona subnitida), from the semiarid region of Brazil. Ciência Rural, 48.
Pirhadi M, Shariatifar N, Bahmani M & Manouchehri, A 2021, Heavy metals in wheat grain and its impact on human health: A mini-review. Journal of Chemical Health Risks. 2021 Apr 6.
Ragimov, AO, Mazirov, MA, Zinchenko, SI & Shitikova, AV 2021 Features of environmentally-friendly product obtaining from sugar and fodder beets in conditions of zinc contamination of sod-podzolic sandy loam soils. Caspian Journal of Environmental Sciences, 19: 939-945, DOI: 10.22124/cjes.2021.5270
Rall, V, Bombo, A, Lopes, T, Carvalho, L, et al. 2003, Honey consumption in the state of São Paulo: A risk to human health? Anaerobe, 9: 299-303.
Solati, K, Karimi, M, Rafieian-Kopaei, M, Abbasi, N, Abbaszadeh, S & Bahmani, M, 2021, Phytotherapy for wound healing: The most important herbal plants in wound healing based on iranian ethnobotanical documents. Mini Reviews in Medicinal Chemistry, 21: 500-519.
Soltanbeigi, A, Dastyar, N, Khajoei Nejad, F & Shokri, S 2022, Medicinal herbs affecting cancers in Iran and the world. Plant Biotechnology Persa, 4: 1-3.
Tosi, EA, Ré, E, Lucero, H & Bulacio, L 2004, Effect of honey high-temperature short-time heating on parameters related to quality, crystallisation phenomena and fungal inhibition. LWT-Food Science and Technology, 37: 669-678.
Vahdani, P, Abbasi, F, Mojarad, MR, et al. 2009, A six month-old girl with botulism due to honey ingestion. Indian Journal of Pathology Microbiology, 52: 592.
Vosloo, MN, Opperman, CJ, Geyer, HD, et al. 2021, First confirmed case of infant botulism in Africa, caused by a dual-toxin-producing Clostridium botulinum strain. International Journal of Infectious Diseases,103: 164-166.
Wojtacka, J, Wysok, B, Kabašinskienė, A, et al. 2017, Prevalence of Clostridium botulinum type A, B, E and F isolated from directly sold honey in Lithuania. Journal of Agricultural Science and Technology, 19: 335-343.
Wojtacka, J, Wysok, B, Lipiński, et al. 2016, Clostridium botulinum spores found in honey from small apiaries in Poland. Journal of Apicultural Science, 60: 89.
Zarei, L, Pourjabali, M, Naghdi, N, Naji-Haddadi, S, Bahmani, E 2017, A systematic review of the most important medicinal plants native to Iran effective on testicular morphology and hormonal testicular function. Journal of Pharmaceutical Sciences and Research, 9: 562.
Caspian Journal of Environmental Sciences
Volume 20, Issue 5
Special Issue: Economical Aspects of Environmental Studies
December 2022
Pages 1143-1148

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