Prevalence of Listeria Monocytogenes in Food in Iran

Author
Department of Biology, School of Basic Science, Neyshabur Branch, Islamic Azad University, Neyshabur, Iran
Abstract
Introduction

Listeria monocytogenes has been described as an opportunistic pathogen that mainly affects children, pregnant women, the elderly, or immunocompromised patients. This disease is associated with serious public health and economic consequences. In recent years, due to the importance of this disease, there have been reports of the spread of this pathogen in various food products. Therefore, the aim of this study was to determine the prevalence of Listeria species in different foods in Iran. The prevalence of Listeria in Iran was compared with the rest of the world, and finally, the antibiotic resistance of Listeria monocytogenes isolated from food was discussed. The results showed that L. monocytogenes were most prevalent in chicken, raw meat, ready-to-eat, fish, dairy, and egg food groups, respectively. In addition, the prevalence of this bacterium, especially in ready-to-eat foods (which are consumed without further heat treatment) and undercooked products, can be a potential risk to public health. Therefore, contamination must be monitored and controlled at all levels of the food chain continuously and periodically.

Keywords

1. World Health Organization (WHO) (2007-2015) Estimates of the Global Burden of Food Borne Diseases; Foodborne Disease Burden Epidemiology Reference Group. http://apps.who.int/iris/bitstream/10665/199350/1/9789241565165_eng.pdf?ua=1. [Ref list]
2. Silk BJ, Mahon BE, Griffin PM, Gould LH, Tauxe RV, Crim SM, Jackson KA, Gerner-Smidt P, Herman KM, Henao OL. Vital signs: Listeria illnesses, deaths, and outbreaks—United States, 2009–2011. MMWR. Morb. Mortal. Wkly. Rep. 2013;7:62(22):448.
3. Shamloo E, Hosseini H, Moghadam ZA, Larsen MH, Haslberger A, Alebouyeh M. Importance of Listeria monocytogenes in food safety: a review of its prevalence, detection, and antibiotic resistance. Iran. J. Vet. Res. 2019;20(4):241.
4. Amagliani G, Brandi G, Omiccioli E, Casiere A, Bruce IJ, Magnani M. Direct detection of Listeria monocytogenes from milk by magnetic based DNA isolation and PCR. Food Microbiol. 2004 Oct 1;21(5):597-603.
5. Moshtaghi H, Mohamadpour AA. Incidence of Listeria spp. in raw milk in Shahrekord, Iran. Foodborne Pathog. Dis. 2007;4(1):107-10.
6. Gasanov U, Hughes D, Hansbro PM. Methods for the isolation and identification of Listeria spp. and Listeria monocytogenes: a review. FEMS Microbiol. Rev. 2005;29(5):851-75.
7. Mahdavi M, Jalali M, Safaei HG, Shamloo E. Microbial quality and prevalence of Salmonella and Listeria in eggs. Int. J. Environ. Health Eng. 2012;1(1):48.
8. Moosavy MH, Esmaeili S, Mostafavi E, Amiri FB. Isolation of Listeria monocytogenes from milks used for Iranian traditional cheese in Lighvan cheese factories. Ann. Agric. Environ. Med. 2014;21(4).
9. Gahan CG, Hill C. Gastrointestinal phase of Listeria monocytogenes infection. J. Appl. Microbiol. 2005;98(6):1345-53.
10. Fallah AA, Saei-Dehkordi SS, Mahzounieh M. Occurrence and antibiotic resistance profiles of Listeria monocytogenes isolated from seafood products and market and processing environments in Iran. Food control. 2013;34(2):630-6.
11. Ooi ST, Lorber B. Gastroenteritis due to Listeria monocytogenes. Clin. Infect. Dis. 2005;40(9):1327-32.
12. Akrami-Mohajeri F, Derakhshan Z, Ferrante M, Hamidiyan N, Soleymani M, Conti GO, Tafti RD. The prevalence and antimicrobial resistance of Listeria spp in raw milk and traditional dairy products delivered in Yazd, central Iran (2016). Food Chem. Toxicol. 2018;114:141-4.
13. Mateus T, Silva J, Maia RL, Teixeira P. Listeriosis during pregnancy: a public health concern. Int. Scholarly Res. Not. 2013;2013.
14. Mansouri-Najand L, Kianpour M, Sami M, Jajarmi M. Prevalence of Listeria monocytogenes in raw milk in Kerman, Iran. In Vet. Res. Vet Res Forum. 2015;6(3):223-6.
15. Vilar MJ, Yus E, Sanjuan ML, Diéguez FJ, Rodríguez-Otero JL. Prevalence of and risk factors for Listeria species on dairy farms. J. Dairy Sci. 2007;90(11):5083-8.
16. Abdimoghadam Z, Shamloo E, Atefi M. Frequency of Listeria species in raw milk and traditional dairy products in Isfahan, Iran. Iran. J. Nutr. Sci. Food Technol. 2015;10(3):101-7.
17. Rahimi E, Momtaz H, Sharifzadeh A, Behzadnia A, Ashtari MS, Esfahani SZ, Riahi M, Momeni M. Prevalence and antimicrobial resistance of Listeria species isolated from traditional dairy products in Chahar Mahal & Bakhtiyari, Iran. Bulg. J. Vet. Med. 2012;15(2).
18. Rahimi E, Ameri M, Momtaz H. Prevalence and antimicrobial resistance of Listeria species isolated from milk and dairy products in Iran. Food Control. 2010;21(11):1448-52.
19. Shamloo Aghakhani E, Jalali M, Mirlohi M, Abdi Moghadam Z, Shamloo Aghakhani E, Reza Maracy M, Yaran M. Prevalence of Listeria Species in Raw Milk in Isfahan, Iran. J. Isfahan Med. Sch. 2012;30(204).
20. Kargar M, Ghasemi A. A survey on prevalence rate & antibiotic resistance of Listeria monocytogenes in fresh cheese of Marvdasht,(2007).
21. Jami S, Jamshidi A, Khanzadi S. The presence of Listeria monocytogenesin raw milk samples in Mashhad, Iran. Iran. J. Vet. Res. 2010;11(4):363-7.
22. Olsen JE, Aabo S, Hill W, Notermans S, Wernars K, Granum PE, Popovic T, Rasmussen HN, Olsvik Ø. Probes and polymerase chain reaction for detection of food-borne bacterial pathogens. Int. J. Food Microbiol. 1995;28(1):1-78.
23. Mirzaei H. Microbiological changes in Lighvan cheese throughout its manufacture and ripening. Afr. J. Microbiol. Res. 2011;5(13):1609-14.
24. Abdi R, Sheikh-Zeinoddin M, Soleimanian-Zad S. Identification of lactic acid bacteria isolated from traditional Iranian Lighvan cheese. Pak. J. Biol. Sci. 2006;9:99-103.
25. Maktabi S, Jamnejad A, Faramarzian K. Contamination of household refrigerators by Listeria species in Ahvaz, Iran. Jundishapur J Microbiol. 2013;6(3):301-5.
26. Shahab Lavasani AR, Ehsani MR, Mirdamadi S, Ebrahim Zadeh Mousavi MA. Changes in physicochemical and organoleptic properties of traditional Iranian cheese Lighvan during ripening. Int. J. Dairy Technol. 2012;65(1):64-70.
27. Cottin J, Picard-Bonnaud F, Carbonnelle B. Study of Listeria monocytogenes survival during the preparation and the conservation of two kinds of dairy product. Acta Microbiol. Hung. 1990;37(1):119-22.
28. Benkerroum N, Oubel H, Sandine WE. Effect of nisin on yogurt starter, and on growth and survival of Listeria monocytogenes during fermentation and storage of yogurt. Int. J. Food Saf. 2003;1:1-5.
29. Bialvaei AZ, Sheikhalizadeh V, Mojtahedi A, Irajian G. Epidemiological burden of Listeria monocytogenes in Iran. Iran. J. Basic Med. Sci. 2018;21(8):770.
30. Rahimi E, Yazdi F, Farzinezhadizadeh H. Prevalence and antimicrobial resistance of Listeria species isolated from different types of raw meat in Iran. J. Food Prot. 2012;75(12):2223-7.
31. Saei-Dehkordi S. Frequency of Listeria species contamination in raw meat of cattle collected from abattoirs and butcher shops of Chaharmahal and Bakhtiary Province. J. Food Microbiol. 2020;7(1):32 -40 [in persian]
32. Rahimi E, Momtaz H, Hemmatzadeh F. The prevalence of Escherichia coli O157: H7, Listeria monocytogenes and Campylobacter spp. on bovine carcasses in Isfahan, Iran. Iran. J. Vet. Res. 2008 Dec 30;9(4):365-70.
33. Jalali M, Abedi D. Prevalence of Listeria species in food products in Isfahan, Iran. Int. J. food microbial. 2008 Mar 20;122(3):336-40.
34. Rostami F, Shaygannia SH, Madahi H, Rahimi E, Jalali M, Dehkordi FS. Prevalence and antibiotic resistance of Listeria species isolated from chicken nuggets from Isfahan Province. Innov. Food Sci. 2014;7:97-103. [in persian]
35. Mansouri-Najand L, Hamzeh Aliabad S, Fatemi N. Molecular identification of Listeria monocytogenes in raw hamburgers from Kerman, South-East of Iran. J. Food Qual. Hazards Control. 2017;4(4):109-12.
36. Rahimi E, Shakerian A, Raissy M. Prevalence of Listeria species in fresh and frozen fish and shrimp in Iran. Ann. Microbiol. 2012;62(1):37-40.
37. Rezai R, Ahmadi E, Salimi B. Prevalence and antimicrobial resistance profile of Listeria species isolated from farmed and on-sale rainbow trout (Oncorhynchus mykiss) in Western Iran. J. food prot. 2018;81(6):886-91.
38. Jamali H, Paydar M, Ismail S, Looi CY, Wong WF, Radmehr B, Abedini A. Prevalence, antimicrobial susceptibility and virulotyping of Listeria species and Listeria monocytogenes isolated from open-air fish markets. BMC Microbiol. 2015;15(1):1-7.
39. Zarei M, Maktabi S, Ghorbanpour M. Prevalence of Listeria monocytogenes, Vibrio parahaemolyticus, Staphylococcus aureus, and Salmonella spp. in seafood products using multiplex polymerase chain reaction. Foodborne Pathog. Dis. 2012;9(2):108-12.
40. Momtaz H, Yadollahi S. Molecular characterization of Listeria monocytogenes isolated from fresh seafood samples in Iran. Diagn. Pathol. 2013;8(1):1-6.
41. Maktabi S, Fazlara A, Ebrahimian S. Incidence of Listeria species in farmed tropical fish in Khuzestan, Iran. World J. Fish Mar. Sci. 2011;3:206-9.
42. Modaresi R, Mardani K, Tukmechi A, Ownagh A. Prevalence of Listeria spp. in fish obtained from Urmia fish markets. Afr. J. Microbiol. Res. 2011;5(30):5398-401.
43. Sohrabi R, Tajbakhsh F, Tajbakhsh E, Momeni M. Prevalence of Listeria spp in chicken, Turkey and ostrich meat from Isfahan, Iran. Glob Vet. 2013;11:80-3.
44. Zeinali T, Jamshidi A, Bassami M, Rad M. Isolation and identification of Listeria spp. in chicken carcasses marketed in northeast of Iran. Int. Food Res. J. 2017;24(2):881.
45. Fallah AA, Saei-Dehkordi SS, Rahnama M, Tahmasby H, Mahzounieh M. Prevalence and antimicrobial resistance patterns of Listeria species isolated from poultry products marketed in Iran. Food Control. 2012;28(2):327-32.
46. Osaili TM, Alaboudi AR, Nesiar EA. Prevalence of Listeria spp. and antibiotic susceptibility of Listeria monocytogenes isolated from raw chicken and ready-to-eat chicken products in Jordan. Food control. 2011;22(3-4):586-90.
47. Hosseinzadeh S, Shekarforoush SS, Ansari-Lari M, EsalatPanah-Fard Jahromi M, Berizi E, Abdollahi M. Prevalence and risk factors for listeria monocytogenes in broiler flocks in Shiraz, southern Iran. Foodborne Pathog. Dis. 2012;9(6):568-72.
48. Kaneko KI, Hayashidani H, Ohtomo Y, Kosuge J, Kato M, Takahashi K, Shiraki Y, Ogawa M. Bacterial contamination of ready-to-eat foods and fresh products in retail shops and food factories. J. food prot. 1999;62(6):644-9.
49. Ghasemian SH, Jalali M, Hosseini A, Narimani T, Sharifzadeh A, Raheimi E. The prevalence of bacterial contamination of table eggs from retails markets by Salmonella spp., Listeria monocytogenes, Campylobacter jejuni and Escherichia coli in Shahrekord, Iran. Jundishapur J Microbiol. 4(4):249-253.
50. Babazadeh Naseri A, Soltan Dallal MM. Frequency, antimicrobial susceptibility and serotyping of Listeria monocytogenes isolated from food samples in Tehran, Iran. J. Gorgan Univ. Med. Sci. 2019;21(1):101-7.
51. Jamali H, Paydar M, Looi CY, Wong WF. Prevalence of Listeria species and Listeria monocytogenes serotypes in ready mayonnaise salads and salad vegetables in Iran. Afr. J. Microbiol. Res. 2013;7(19):1903-6.
52. Akya A, Najafi F, Moradi J, Mohebi Z, Adabagher S. Prevalence of food contamination with Listeria spp. in Kermanshah, Islamic Republic of Iran. EMHJ-Eastern Mediterranean Health J. 2013;19(5):474-477.
53. Guerini MN, Brichta-Harhay DM, Shackelford SD, Arthur TM, Bosilevac JM, Kalchayanand N, Wheeler TL, Koohmaraie M. Listeria prevalence and Listeria monocytogenes serovar diversity at cull cow and bull processing plants in the United States. J. food prot. 2007;70(11):2578-82.
54. Ranjbar R, Halaji M. Epidemiology of Listeria monocytogenes prevalence in foods, animals and human origin from Iran: a systematic review and meta-analysis. BMC public health. 2018;18(1):1-2.
55. Wang W, Zhou X, Suo Y, Deng X, Cheng M, Shi C, Shi X. Prevalence, serotype diversity, biofilm-forming ability and eradication of Listeria monocytogenes isolated from diverse foods in Shanghai, China. Food Control. 2017;73:1068-73.
56. Kevenk TO, Terzi Gulel G. Prevalence, antimicrobial resistance and serotype distribution of Listeria monocytogenes isolated from raw milk and dairy products. J. Food Saf. 2016;36(1):11-8.
57. Haley BJ, Sonnier J, Schukken YH, Karns JS, Van Kessel JA. Diversity of Listeria monocytogenes within a US dairy herd, 2004–2010. Foodborne Pathog. Dis. 2015;12(10):844-50.
58. Almeida RM, Barbosa AV, Lisbôa RD, Santos AF, Hofer E, Vallim DC, Hofer CB. Virulence genes and genetic relationship of isolated from human and food sources in Brazil. Braz. J. Infect. Dis. 2017;21:282-9.
59. Boscher E, Houard E, Denis M. Prevalence and distribution of Listeria monocytogenes serotypes and pulsotypes in sows and fattening pigs in farrow-to-finish farms (France, 2008). J. food prot. 2012;75(5):889-95.
60. Hasegawa M, Iwabuchi E, Yamamoto S, Muramatsu M, Takashima I, Hirai K. Prevalence and characteristics of Listeria monocytogenes in feces of black beef cattle reared in three geographically distant areas in Japan. Foodborne Pathog. Dis. 2014;11(2):96-103.
61. Khademi F, Sahebkar A. A systematic review and meta-analysis on the prevalence of antibiotic-resistant Listeria species in food, animal and human specimens in Iran. J. Food Sci. Technol. 2019;56(12):5167-83.
62. Heidarzadeh S, Dallal MM, Pourmand MR, Pirjani R, Foroushani AR, Noori M, Naseri AB. Prevalence, antimicrobial susceptibility, serotyping and virulence genes screening of Listeria monocytogenes strains at a tertiary care hospital in Tehran, Iran. Iran. J. microbiol. 2018;10(5):307.
63. Lotfollahi L, Chaharbalesh A, Rezaee MA, Hasani A. Prevalence, antimicrobial susceptibility and multiplex PCR-serotyping of Listeria monocytogenes isolated from humans, foods and livestock in Iran. Microb. Pathog. 2017;107:425-9.
64. Alidoosti HA, Razzaghi Manesh MR, Mashhady Rafie SI, Dadar MO. Prevalence of Listeria monocytogenes in dogs in Isfahan, Iran. Bulg. J. Vet. Med. 2014;17:69-73.
65. Abdollahzadeh E, Ojagh SM, Hosseini H, Ghaemi EA, Irajian G, Heidarlo MN. Antimicrobial resistance of Listeria monocytogenes isolated from seafood and humans in Iran. Microb. Pathog. 2016;100:70-4.
66. Allen KJ, Wałecka-Zacharska E, Chen JC, Katarzyna KP, Devlieghere F, Van Meervenne E, Osek J, Wieczorek K, Bania J. Listeria monocytogenes–An examination of food chain factors potentially contributing to antimicrobial resistance. Food Microbiol. 2016;54:178-89.
67. Doménech E, Jimenez-Belenguer A, Amoros JA, Ferrus MA, Escriche I. Prevalence and antimicrobial resistance of Listeria monocytogenes and Salmonella strains isolated in ready-to-eat foods in Eastern Spain. Food Control. 2015;47:120-5.
68. Lungu B, O'Bryan CA, Muthaiyan A, Milillo SR, Johnson MG, Crandall PG, Ricke SC. Listeria monocytogenes: antibiotic resistance in food production. Foodborne Pathog. Dis. 2011;8(5):569-78.
69. Gómez D, Azón E, Marco N, Carramiñana JJ, Rota C, Ariño A, Yangüela J. Antimicrobial resistance of Listeria monocytogenes and Listeria innocua from meat products and meat-processing environment. Food microbiol. 2014;42:61-5.
70. Olaimat AN, Al‐Holy MA, Shahbaz HM, Al‐Nabulsi AA, Abu Ghoush MH, Osaili TM, Ayyash MM, Holley RA. Emergence of antibiotic resistance in Listeria monocytogenes isolated from food products: a comprehensive review. Compr. Rev. Food Sci. Food Saf. 2018;17(5):1277-92.
71. Rezaei Z, Khanzadi S, Salari A. A survey on biofilm formation of Lactobacillus rhamnosus (PTCC 1637) and Lac- tobacillus plantarum (PTCC 1745) as a survival strategy of probiotics against antibiotic in vitro and yogurt. J Food Process Preserv. 2021;00:e1599.
72. Rezaei Z, Khanzadi S, Salari A. Biofilm formation and antagonistic activity of Lacticaseibacillus rhamnosus (PTCC1712) and Lactiplantibacillus plantarum (PTCC1745). AMB Express. 2021;11(1):156.