Antimicrobial Susceptibility, Serotyping, and Molecular Characterization of Antibiotic Resistance Genes in Listeria monocytogenes Isolated from Pregnant Women with a History of Abortion
-
Siamak HEIDARZADEH
,
Mohammad Reza POURMAND
,
Saeedeh HASANVAND
,
Reyhaneh PIRJANI
,
Davoud AFSHAR
,
Matina NOORI
,
Mohammad Mehdi SOLTAN DALLAL
Abstract
Background: Listeria monocytogenes show high mortality among pregnant women and newborns. This study aimed to detect L. monocytogenes in pregnant women with a history of abortion and assess the serotypes, antibiotic susceptibility patterns, and its resistance genes.
Methods: Overall, 400 vaginal swabs were taken from pregnant women with a history of abortion in the past few years in a tertiary care hospital in Tehran, Iran, during 2015-2018. Antibiotics susceptibility to a panel of 10 antibiotics was determined using the standard disk diffusion method and the isolates serotyped by the agglutination method. The antimicrobial-resistant isolates were also screened for the presence of tetM, ermB and dfrD genes by PCR.
Results: Overall, 22 L. monocytogenes isolates were identified. High rates of resistance were observed for trimethoprim (50%; n=11), sulphamethoxazole (50%; n=11), tetracycline (45.45%; n=10) and gentamicin (36.36%; n=8). From 22 L. monocytogenes isolates, 13 (59.10 %), 5 (22.73%), 3 (13.63%) and 1 (4.54%) belonged to serotypes 4b, 1/2a, 1/2b, and 3c, respectively. The genetic determinant tetM was detected in 70% of the tetracycline-resistant isolates. Out of 11 trimethoprim-resistant isolates, 27.27% isolates contained dfrD. Moreover, the ermB gene was found in 83.33% of the erythromycin-resistant isolates.
Conclusion: Ampicillin and partly penicillin consider to be suitable antimicrobial agents to treat human listeriosis. Moreover, due to resistance against many antibiotics, it is necessary to continue monitoring and managing antimicrobial resistance.
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6. Aljicevic M, Beslagic E, Zvizdic S, et al (2005). [Listeria monocytogenes in women of reproductive age]. Med Arh,59(5):297-298.
7. Jamshidi M, Jahromi AS, Davoodian P, et al (2009). Seropositivity for Listeria monocytogenes in women with spontaneous abortion: a case-control study in Iran. Taiwan J Obstet Gynecol, 48(1):46-8.
8. Gómez D, Azón E, Marco N, et al (2014). Antimicrobial resistance of Listeria monocytogenes and Listeria innocua from meat products and meat-processing environment. Food Microbiol,42:61-65.
9. Morvan A, Moubareck C, Leclercq A, et al (2010). Antimicrobial resistance of Listeria monocytogenes strains isolated from humans in France. Antimicrob Agents Chemother, 54(6): 2728–2731.
10. Moreno LZ, Paixao R, Gobbi DD, et al (2014). Characterization of antibiotic resistance in Listeria spp. isolated from slaughterhouse environments, pork and human infections. J Infect Dev Ctries, 8(4):416-23.
11. Charpentier E, Gerbaud G, Courvalin P (1999). Conjugative mobilization of the rolling-circle plasmid pIP823 from Listeria monocytogenes BM4293 among gram-positive and gram-negative bacteria. J Bacteriol, 181(11):3368-74.
12. Godreuil S, Galimand M, Gerbaud G, et al (2003). Efflux pump Lde is associated with fluoroquinolone resistance in Listeria monocytogenes. Antimicrob Agents Chemother, 47(2): 704–708.
13. Srinivasan V, Nam HM, Nguyen LT, et al (2005). Prevalence of antimicrobial resistance genes in Listeria monocytogenes isolated from dairy farms. Foodborne Pathog Dis, 2(3):201-11.
14. Wang G, Qian W, Zhang X, et al (2015). Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from ready-to-eat meat products in Nanjing, China. Food Control,50:202-208.
15. Poyart-Salmeron C, Carlier C, Trieu-Cuot P, et al (1990). Transferable plasmid-mediated antibiotic resistance in Listeria monocytogenes. Lancet, 335(8703):1422-6.
16. Charpentier E, Courvalin P (1999). Antibiotic resistance in Listeria spp. Antimicrob Agents Chemother,43(9):2103-2108.
17. Gasanov U, Hughes D, Hansbro PM (2005). Methods for the isolation and identification of Listeria spp. and Listeria monocytogenes: a review. FEMS Microbiol Rev, 29(5):851-75.
18. Park SH, Chang PS, Ryu S, et al (2014). Development of a novel selective and differential medium for the isolation of Listeria monocytogenes. Appl Environ Microbiol,80(3):1020-1025.
19. Liu D, Lawrence ML, Austin FW, et al (2007). A multiplex PCR for species- and virulence-specific determination of Listeria monocytogenes. J Microbiol Methods,71(2):133-40.
20. Okada Y, Monden S, Igimi S, et al (2012). The occurrence of Listeria monocytogenes in imported ready-to-eat foods in Japan. J Vet Med Sci,74(3):373-5.
21. de Vasconcelos Byrne V, Hofer E, Vallim DC, et al (2016). Occurrence and antimicrobial resistance patterns of Listeria monocytogenes isolated from vegetables. Braz J Microbiol,47(2):438-443.
22. Caplan ME, Mateescu LA, Dimov TV, et al (2014). Antibiotic Susceptibility Profiles of Listeria monocytogenes Strains Isolated from Food Products and Clinical Samples. Romanian Review of Laboratory Medicine,22(2):255-261.
23. Ranjbar R, Halaji MJBph (2018). Epidemiology of Listeria monocytogenes prevalence in foods, animals and human origin from Iran: a systematic review and meta-analysis. BMC Public Health,18:1057.
24. Rodas-Suarez OR, Flores-Pedroche JF, Betancourt-Rule JM, et al (2006). Occurrence and antibiotic sensitivity of Listeria monocytogenes strains isolated from oysters, fish, and estuarine water. Appl Environ Microbiol,72(11):7410-7412.
25. Bahador A, Kalani BS, Valian F, et al (2015). Phenotypic and Genotypic Characteristics of Listeria monocytogenes Isolated From Dairy and Meat Products. Avicenna J Clin Microbiol Infect, 2(3): 26905.
26. Jamali H, Radmehr B, Thong KL (2013). Prevalence, characterisation, and antimicrobial resistance of Listeria species and Listeria monocytogenes isolates from raw milk in farm bulk tanks. Food Control,34:121-125.
27. Dehkordi FS, Barati S, Momtaz H, et al (2013). Comparison of Shedding, and Antibiotic Resistance Properties of Listeria monocytogenes Isolated From Milk, Feces, Urine, and Vaginal Secretion of Bovine, Ovine, Caprine, Buffalo, and Camel Species in Iran. Jundishapur Journal of Microbiology,6(3):284-294.
28. Rahimi E, Momtaz H, Sharifzadeh A, et al (2012). Prevalence and antimicrobial resistance of Listeria species isolated from traditional dairy products in Charar Mahal & Bakhtiary, Iran. Bulgarian Journal of Veterinary Medicine,15:115-122.
29. Jamali H, Paydar M, Ismail S, et al (2015). Prevalence, antimicrobial susceptibility and virulotyping of Listeria species and Listeria monocytogenes isolated from open-air fish markets. BMC Microbiol,15:144.
30. Abdollahzadeh E, Ojagh SM, Hosseini H, et al (2016). Antimicrobial resistance of Listeria monocytogenes isolated from seafood and humans in Iran. Microb Pathog,100:70-74.
31. Sadeghi Kalani B, Pournajaf A, Sedighi M, et al (2015). Genotypic characterization, invasion index and antimicrobial resistance pattern in Listeria monocytogenes strains isolated from clinical samples. Journal of Acute Disease,4:141-146.
32. Altuntas EG, Kocan D, Cosansu S, et al (2012). Antibiotic and bacteriocin sensitivity of Listeria monocytogenes strains isolated from different foods. Food and Nutrition Sciences, 3(3):363-368.
33. Pesavento G, Ducci B, Nieri D, et al (2010). Prevalence and antibiotic susceptibility of Listeria spp. isolated from raw meat and retail foods. Food Control,21:708-713.
34. Adzitey F, Rahmat Ali GR, Huda N, et al (2013). Prevalence, antibiotic resistance and genetic diversity of Listeria monocytogenes isolated from ducks, their rearing and processing environments in Penang, Malaysia. Food Control,32:607-614.
35. Dutta NK, Mazumdar K, Park JH (2009). In vitro synergistic effect of gentamicin with the anti-inflammatory agent diclofenac against Listeria monocytogenes. Lett Appl Microbiol,48(6):783-5.
36. Charpentier E, Gerbaud G, Jacquet C, et al (1995). Incidence of antibiotic resistance in Listeria species. J Infect Dis,172(1):277-81.
37. Granier SA, Moubareck C, Colaneri C, et al (2011). Antimicrobial resistance of Listeria monocytogenes isolates from food and the environment in France over a 10-year period. Appl Environ Microbiol,77(8):2788-2790.
38. Haubert L, Mendonca M, Lopes GV, et al (2016). Listeria monocytogenes isolates from food and food environment harbouring tetM and ermB resistance genes. Lett Appl Microbiol,62(1):23-29.
39. Bertsch D, Anderegg J, Lacroix C, et al (2013). pDB2011, a 7.6 kb multidrug resistance plasmid from Listeria innocua replicating in Gram-positive and Gram-negative hosts. Plasmid,70:284-287.
40. Roberts MC, Facinelli B, Giovanetti E, et al (1996). Transferable erythromycin resistance in Listeria spp. isolated from food. Appl Environ Microbiol,62(1):269-270.
41. El-Banna T, Sonbol F, Zaki M, et al (2016). Clinical and Environmental Prevalence and Antibiotic Susceptibility of Listeria monocytogenes in Dakahlea Governorate, Egypt. Clin Microbiol,5:2-9.
42. Nugent RP, Krohn MA, Hillier SL (1991). Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol,29(2):297-301.
43. Almeida RM, Barbosa AV, Lisboa RC, et al (2017). Virulence genes and genetic relationship of L. monocytogenes isolated from human and food sources in Brazil. Braz J Infect Dis,21(3):282-289.
44. Camargo AC, Vallim DC, Hofer E, et al (2016). Molecular Serogrouping of Listeria monocytogenes from Brazil Using PCR. J Food Prot,79(1):144-147.
45. Cartwright EJ, Jackson KA, Johnson SD, et al (2013). Listeriosis outbreaks and associated food vehicles, United States, 1998-2008. Emerg Infect Dis,19(1):1-9; quiz 184.
2. Chen J, Luo X, Jiang L, et al (2009). Molecular characteristics and virulence potential of Listeria monocytogenes isolates from Chinese food systems. Food Microbiol, 26(1):103-11.
3. Awofisayo A, Amar C, Ruggles R, et al (2015). Pregnancy-associated listeriosis in England and Wales. Epidemiol Infect, 143(2):249-56.
4. Mateus T, Silva J, Maia RL, et al(2013). Listeriosis during pregnancy: a public health concern. ISRN Obstet Gynecol, 2013:851712.
5. Vazquez-Boland JA, Krypotou E, Scortti M (2017). Listeria Placental Infection. mBio, 8(3):e00949-17.
6. Aljicevic M, Beslagic E, Zvizdic S, et al (2005). [Listeria monocytogenes in women of reproductive age]. Med Arh,59(5):297-298.
7. Jamshidi M, Jahromi AS, Davoodian P, et al (2009). Seropositivity for Listeria monocytogenes in women with spontaneous abortion: a case-control study in Iran. Taiwan J Obstet Gynecol, 48(1):46-8.
8. Gómez D, Azón E, Marco N, et al (2014). Antimicrobial resistance of Listeria monocytogenes and Listeria innocua from meat products and meat-processing environment. Food Microbiol,42:61-65.
9. Morvan A, Moubareck C, Leclercq A, et al (2010). Antimicrobial resistance of Listeria monocytogenes strains isolated from humans in France. Antimicrob Agents Chemother, 54(6): 2728–2731.
10. Moreno LZ, Paixao R, Gobbi DD, et al (2014). Characterization of antibiotic resistance in Listeria spp. isolated from slaughterhouse environments, pork and human infections. J Infect Dev Ctries, 8(4):416-23.
11. Charpentier E, Gerbaud G, Courvalin P (1999). Conjugative mobilization of the rolling-circle plasmid pIP823 from Listeria monocytogenes BM4293 among gram-positive and gram-negative bacteria. J Bacteriol, 181(11):3368-74.
12. Godreuil S, Galimand M, Gerbaud G, et al (2003). Efflux pump Lde is associated with fluoroquinolone resistance in Listeria monocytogenes. Antimicrob Agents Chemother, 47(2): 704–708.
13. Srinivasan V, Nam HM, Nguyen LT, et al (2005). Prevalence of antimicrobial resistance genes in Listeria monocytogenes isolated from dairy farms. Foodborne Pathog Dis, 2(3):201-11.
14. Wang G, Qian W, Zhang X, et al (2015). Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from ready-to-eat meat products in Nanjing, China. Food Control,50:202-208.
15. Poyart-Salmeron C, Carlier C, Trieu-Cuot P, et al (1990). Transferable plasmid-mediated antibiotic resistance in Listeria monocytogenes. Lancet, 335(8703):1422-6.
16. Charpentier E, Courvalin P (1999). Antibiotic resistance in Listeria spp. Antimicrob Agents Chemother,43(9):2103-2108.
17. Gasanov U, Hughes D, Hansbro PM (2005). Methods for the isolation and identification of Listeria spp. and Listeria monocytogenes: a review. FEMS Microbiol Rev, 29(5):851-75.
18. Park SH, Chang PS, Ryu S, et al (2014). Development of a novel selective and differential medium for the isolation of Listeria monocytogenes. Appl Environ Microbiol,80(3):1020-1025.
19. Liu D, Lawrence ML, Austin FW, et al (2007). A multiplex PCR for species- and virulence-specific determination of Listeria monocytogenes. J Microbiol Methods,71(2):133-40.
20. Okada Y, Monden S, Igimi S, et al (2012). The occurrence of Listeria monocytogenes in imported ready-to-eat foods in Japan. J Vet Med Sci,74(3):373-5.
21. de Vasconcelos Byrne V, Hofer E, Vallim DC, et al (2016). Occurrence and antimicrobial resistance patterns of Listeria monocytogenes isolated from vegetables. Braz J Microbiol,47(2):438-443.
22. Caplan ME, Mateescu LA, Dimov TV, et al (2014). Antibiotic Susceptibility Profiles of Listeria monocytogenes Strains Isolated from Food Products and Clinical Samples. Romanian Review of Laboratory Medicine,22(2):255-261.
23. Ranjbar R, Halaji MJBph (2018). Epidemiology of Listeria monocytogenes prevalence in foods, animals and human origin from Iran: a systematic review and meta-analysis. BMC Public Health,18:1057.
24. Rodas-Suarez OR, Flores-Pedroche JF, Betancourt-Rule JM, et al (2006). Occurrence and antibiotic sensitivity of Listeria monocytogenes strains isolated from oysters, fish, and estuarine water. Appl Environ Microbiol,72(11):7410-7412.
25. Bahador A, Kalani BS, Valian F, et al (2015). Phenotypic and Genotypic Characteristics of Listeria monocytogenes Isolated From Dairy and Meat Products. Avicenna J Clin Microbiol Infect, 2(3): 26905.
26. Jamali H, Radmehr B, Thong KL (2013). Prevalence, characterisation, and antimicrobial resistance of Listeria species and Listeria monocytogenes isolates from raw milk in farm bulk tanks. Food Control,34:121-125.
27. Dehkordi FS, Barati S, Momtaz H, et al (2013). Comparison of Shedding, and Antibiotic Resistance Properties of Listeria monocytogenes Isolated From Milk, Feces, Urine, and Vaginal Secretion of Bovine, Ovine, Caprine, Buffalo, and Camel Species in Iran. Jundishapur Journal of Microbiology,6(3):284-294.
28. Rahimi E, Momtaz H, Sharifzadeh A, et al (2012). Prevalence and antimicrobial resistance of Listeria species isolated from traditional dairy products in Charar Mahal & Bakhtiary, Iran. Bulgarian Journal of Veterinary Medicine,15:115-122.
29. Jamali H, Paydar M, Ismail S, et al (2015). Prevalence, antimicrobial susceptibility and virulotyping of Listeria species and Listeria monocytogenes isolated from open-air fish markets. BMC Microbiol,15:144.
30. Abdollahzadeh E, Ojagh SM, Hosseini H, et al (2016). Antimicrobial resistance of Listeria monocytogenes isolated from seafood and humans in Iran. Microb Pathog,100:70-74.
31. Sadeghi Kalani B, Pournajaf A, Sedighi M, et al (2015). Genotypic characterization, invasion index and antimicrobial resistance pattern in Listeria monocytogenes strains isolated from clinical samples. Journal of Acute Disease,4:141-146.
32. Altuntas EG, Kocan D, Cosansu S, et al (2012). Antibiotic and bacteriocin sensitivity of Listeria monocytogenes strains isolated from different foods. Food and Nutrition Sciences, 3(3):363-368.
33. Pesavento G, Ducci B, Nieri D, et al (2010). Prevalence and antibiotic susceptibility of Listeria spp. isolated from raw meat and retail foods. Food Control,21:708-713.
34. Adzitey F, Rahmat Ali GR, Huda N, et al (2013). Prevalence, antibiotic resistance and genetic diversity of Listeria monocytogenes isolated from ducks, their rearing and processing environments in Penang, Malaysia. Food Control,32:607-614.
35. Dutta NK, Mazumdar K, Park JH (2009). In vitro synergistic effect of gentamicin with the anti-inflammatory agent diclofenac against Listeria monocytogenes. Lett Appl Microbiol,48(6):783-5.
36. Charpentier E, Gerbaud G, Jacquet C, et al (1995). Incidence of antibiotic resistance in Listeria species. J Infect Dis,172(1):277-81.
37. Granier SA, Moubareck C, Colaneri C, et al (2011). Antimicrobial resistance of Listeria monocytogenes isolates from food and the environment in France over a 10-year period. Appl Environ Microbiol,77(8):2788-2790.
38. Haubert L, Mendonca M, Lopes GV, et al (2016). Listeria monocytogenes isolates from food and food environment harbouring tetM and ermB resistance genes. Lett Appl Microbiol,62(1):23-29.
39. Bertsch D, Anderegg J, Lacroix C, et al (2013). pDB2011, a 7.6 kb multidrug resistance plasmid from Listeria innocua replicating in Gram-positive and Gram-negative hosts. Plasmid,70:284-287.
40. Roberts MC, Facinelli B, Giovanetti E, et al (1996). Transferable erythromycin resistance in Listeria spp. isolated from food. Appl Environ Microbiol,62(1):269-270.
41. El-Banna T, Sonbol F, Zaki M, et al (2016). Clinical and Environmental Prevalence and Antibiotic Susceptibility of Listeria monocytogenes in Dakahlea Governorate, Egypt. Clin Microbiol,5:2-9.
42. Nugent RP, Krohn MA, Hillier SL (1991). Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol,29(2):297-301.
43. Almeida RM, Barbosa AV, Lisboa RC, et al (2017). Virulence genes and genetic relationship of L. monocytogenes isolated from human and food sources in Brazil. Braz J Infect Dis,21(3):282-289.
44. Camargo AC, Vallim DC, Hofer E, et al (2016). Molecular Serogrouping of Listeria monocytogenes from Brazil Using PCR. J Food Prot,79(1):144-147.
45. Cartwright EJ, Jackson KA, Johnson SD, et al (2013). Listeriosis outbreaks and associated food vehicles, United States, 1998-2008. Emerg Infect Dis,19(1):1-9; quiz 184.
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| Issue | Vol 50 No 1 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v50i1.5084 | |
| Keywords | ||
| Listeria monocytogenes Genes Pregnant women | ||
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How to Cite
1.
HEIDARZADEH S, POURMAND MR, HASANVAND S, PIRJANI R, AFSHAR D, NOORI M, SOLTAN DALLAL MM. Antimicrobial Susceptibility, Serotyping, and Molecular Characterization of Antibiotic Resistance Genes in Listeria monocytogenes Isolated from Pregnant Women with a History of Abortion. Iran J Public Health. 2020;50(1):170-179.
