Serotyping of Listeria monocytogenes Isolates from Women with Spontaneous Abortion Using Polymerase Chain Reaction Method
-
Elnaz Ohadi
,
Hossein Goudarzi
,
Behrooz Sadeghi Kalani
,
Arezou Taherpour
,
Ali Shivaee
,
Gita Eslami
Abstract
Background: Listeria monocytogenes infection during pregnancy may cause spontaneous abortion or stillbirth, or the birth of babies with neonatal meningitis. The aim of this study was to serotype L. monocytogenes isolated from women with spontaneous abortion using polymerase chain reaction.
Methods: Vaginal swab samples were obtained from 96 women with spontaneous abortion. The microbial culture was performed on blood agar and PALCAM agar followed by differential biochemical tests for characterization of L. monocytogenes isolates. Besides, total DNA was extracted from each vaginal specimen, and PCR assay was then carried out using specific primers for target genes of this bacterial species.
Results: Microbial culture and PCR revealed 4 and 16 L. monocytogenes isolates (out of 96 vaginal specimens), respectively. There was a significant association between consuming unsterilized dairy products and the risk of Llisteria infection (P < 0.001). Various serotypes of L. monocytogenes were detected as follows; the serotypes 1/2b, 3b (31.25%), the serotypes 1/2c, 3c (31.25%), the serotypes 1/2a, 3a (25%), and the serotypes 4 (12.5%).
Conclusion: However, the difference between frequencies of observed serotypes was not statistically significant (P < 0.05). The 1/2b, 3b, and 1/2c, 3c serotypes of L. monocytogenes are more commonly seen in vaginal specimens of women with spontaneous abortion, and PCR technique as a convenient tool may be used for identifying of causative strains. However, further studies need to improve and optimize this approach.
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2. Kalani BS, Irajian G, Lotfollahi L, et al. Putative type II toxin-antitoxin systems in Listeria monocytogenes isolated from clinical, food, and animal samples in Iran. Microb Pathog 2018; 122:19-24.
3. Nightingale K, Schukken Y, Nightingale C, et al. Ecology and transmission of Listeria monocytogenes infecting ruminants and in the farm environment. Appl Environ Microbiol 2004; 70(8):4458-67.
4. Pizarro-Cerdá J, Kühbacher A, Cossart P. Entry of Listeria monocytogenes in mammalian epithelial cells: an updated view. Cold Spring Harb Perspect Med 2012; 2(11):a010009.
5. Tompkin R. Control of Listeria monocytogenes in the food-processing environment. J Food Prot 2002; 65(4):709-25.
6. Momtaz H, Yadollahi S. Molecular characterization of Listeria monocytogenes isolated from fresh seafood samples in Iran. Diagn Pathol 2013; 8(1):149.
7. Meloni D, Consolati SG, Mazza R, et al. Presence and molecular characterization of the major serovars of Listeria monocytogenes in ten Sardinian fermented sausage processing plants. Meat Sci 2014; 97(4):443-50.
8. Kalani BS, Pournajaf A, Sedighi M, et al. Genotypic characterization, invasion index and antimicrobial resistance pattern in Listeria monocytogenes strains isolated from clinical samples. J Acute Dis 2015; 4(2):141-6.
9. Bahador A, Kalani BS, Valian F, et al. Phenotypic and genotypic characteristics of Listeria monocytogenes isolated from dairy and meat products. Avicenna J Clin Microbiol Infect 2015; 2(3).e26905
10. Farber J, Peterkin P. Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 1991; 55(3):476-511.
11. Buchanan RL, Gorris LG, Hayman MM, et al. A review of Listeria monocytogenes: An update on outbreaks, virulence, dose-response, ecology, and risk assessments. Food Control 2017; 75:1-13.
12. Vázquez-Boland JA, Krypotou E, Scortti M. Listeria Placental Infection. mBio 2017; 8(3):e00949-17.
13. Lotfollahi L, Chaharbalesh A, Rezaee MA, et al. Prevalence, antimicrobial susceptibility and multiplex PCR-serotyping of Listeria monocytogenes isolated from humans, foods and livestock in Iran. Microb Pathog 2017; 107:425-9.
14. Sapuan S, Kortsalioudaki C, Anthony M, et al. Neonatal listeriosis in the UK 2004–2014. J Infect 2017; 74(3):236-42.
15. Fayol L, Beizig S, Le Monnier A, et al. Neonatal meningitis due to Listeria monocytogenes after 3 weeks of maternal treatment during pregnancy. Arch Pediatr 2009; 16(4):353-6.
16. Vázquez-Boland JA, Kuhn M, Berche P, et al. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 2001; 14(3):584-640.
17. Schwarzkopf A. Listeria monocytogenes--aspects of pathogenicity. Pathol Biol 1996; 44(9):769-74.
18. Portnoy DA, Chakraborty T, Goebel W, et al. Molecular determinants of Listeria monocytogenes pathogenesis. Infect Immun 1992; 60(4):1263.
19. Soni DK, Dubey SK. Phylogenetic analysis of the Listeria monocytogenes based on sequencing of 16S rRNA and hlyA genes. Mol Biol Rep 2014; 41(12):8219-29.
20. Soni DK, Singh M, Singh DV, et al. Virulence and genotypic characterization of Listeria monocytogenes isolated from vegetable and soil samples. BMC Microbiol 2014; 14(1):241.
21. Seeliger H, Hönne K. Serotyping of Listeria monocytogenes and related species. Methods Microbiol 1979; 13:31-49.
22. Aarts H, Hakemulder L, Van Hoef A. Genomic typing of Listeria monocytogenes strains by automated laser fluorescence analysis of amplified fragment length polymorphism fingerprint patterns. Int J Food Microbiol 1999; 49(1):95-102.
23. Graves LM, Swaminathan B, Reeves MW, et al. Comparison of ribotyping and multilocus enzyme electrophoresis for subtyping of Listeria monocytogenes isolates. J Clin Microbiol 1994; 32(12):2936-43.
24. Rasmussen OF, Skouboe P, Dons L, et al. Listeria monocytogenes exists in at least three evolutionary lines: evidence from flagellin, invasive associated protein and listeriolysin O genes. Microbiol 1995; 141(9):2053-61.
25. Borucki MK, Call DR. Listeria monocytogenes serotype identification by PCR. J Clin Microbiol 2003; 41(12):5537-40.
26. Tappero JW, Schuchat A, Deaver KA, et al. Reduction in the incidence of human listeriosis in the United States: effectiveness of prevention efforts? JAMA 1995; 273(14):1118-22.
27. Eslami G, Goudarzi H, Ohadi E, et al. Identification of Listeria monocytogenes virulence factors in women with abortion by polymerase chain reaction. Arch Clin Infect Dis 2014; 9(3).e19931.
28. Doumith M, Buchrieser C, Glaser P, et al. Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol 2004; 42(8):3819-22.
29. Mohammadzadeh R, Shivaee A, Ohadi E, et al. In silico insight into the dominant type II toxin–antitoxin systems and Clp proteases in Listeria monocytogenes and designation of derived peptides as a novel approach to interfere with this system. Int J Pept Res Ther 2019:1-11.
30. Aurora R, Prakash A, Prakash S. Genotypic characterization of Listeria monocytogenes isolated from milk and ready-to-eat indigenous milk products. Food Control 2009; 20(9):835-9.
31. Shalaby MA, Mohamed MS, Mansour MA, et al. Comparison of polymerase chain reaction and conventional methods for diagnosis of Listeria monocytogenes isolated from different clinical specimens and food stuffs. Clin Lab 2010; 57(11-12):919-24.
32. Shayan R, Satari M, Forouzandeh M. Isolation and identification of Listeria monocytogenes in vaginal samples by PCR. Modares J Med 2009; 12(1):51-58.
33. Jeffers GT, Bruce JL, McDonough PL, et al. Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiol 2001; 147(5):1095-104.
34. Liu D. Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen. J Med Microbiol 2006; 55(6):645-59.
35. Lotfollahi L, Nowrouzi J, Irajian G, et al. Prevalence and antimicrobial resistance profiles of Listeria monocytogenes in spontaneous abortions in humans. Afr J Microbiol Res 2011; 5(14):1990-3.
36. Jamshidi M, Jahromi AS, Davoodian P, et al. Seropositivity for Listeria monocytogenes in women with spontaneous abortion: a case-control study in Iran. Taiwan J Obstet Gynecol 2009; 48(1):46-8.
37. Althaus D, Lehner A, Brisse S, et al. Characterization of Listeria monocytogenes strains isolated during 2011–2013 from human infections in Switzerland. Foodborne Pathog Dis 2014; 11(10):753-8.
38. Indrawattana N, Nibaddhasobon T, Sookrung N, et al. Prevalence of Listeria monocytogenes in raw meats marketed in Bangkok and characterization of the isolates by phenotypic and molecular methods. J Health Popul Nutr 2011; 29(1):26.
2. Kalani BS, Irajian G, Lotfollahi L, et al. Putative type II toxin-antitoxin systems in Listeria monocytogenes isolated from clinical, food, and animal samples in Iran. Microb Pathog 2018; 122:19-24.
3. Nightingale K, Schukken Y, Nightingale C, et al. Ecology and transmission of Listeria monocytogenes infecting ruminants and in the farm environment. Appl Environ Microbiol 2004; 70(8):4458-67.
4. Pizarro-Cerdá J, Kühbacher A, Cossart P. Entry of Listeria monocytogenes in mammalian epithelial cells: an updated view. Cold Spring Harb Perspect Med 2012; 2(11):a010009.
5. Tompkin R. Control of Listeria monocytogenes in the food-processing environment. J Food Prot 2002; 65(4):709-25.
6. Momtaz H, Yadollahi S. Molecular characterization of Listeria monocytogenes isolated from fresh seafood samples in Iran. Diagn Pathol 2013; 8(1):149.
7. Meloni D, Consolati SG, Mazza R, et al. Presence and molecular characterization of the major serovars of Listeria monocytogenes in ten Sardinian fermented sausage processing plants. Meat Sci 2014; 97(4):443-50.
8. Kalani BS, Pournajaf A, Sedighi M, et al. Genotypic characterization, invasion index and antimicrobial resistance pattern in Listeria monocytogenes strains isolated from clinical samples. J Acute Dis 2015; 4(2):141-6.
9. Bahador A, Kalani BS, Valian F, et al. Phenotypic and genotypic characteristics of Listeria monocytogenes isolated from dairy and meat products. Avicenna J Clin Microbiol Infect 2015; 2(3).e26905
10. Farber J, Peterkin P. Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 1991; 55(3):476-511.
11. Buchanan RL, Gorris LG, Hayman MM, et al. A review of Listeria monocytogenes: An update on outbreaks, virulence, dose-response, ecology, and risk assessments. Food Control 2017; 75:1-13.
12. Vázquez-Boland JA, Krypotou E, Scortti M. Listeria Placental Infection. mBio 2017; 8(3):e00949-17.
13. Lotfollahi L, Chaharbalesh A, Rezaee MA, et al. Prevalence, antimicrobial susceptibility and multiplex PCR-serotyping of Listeria monocytogenes isolated from humans, foods and livestock in Iran. Microb Pathog 2017; 107:425-9.
14. Sapuan S, Kortsalioudaki C, Anthony M, et al. Neonatal listeriosis in the UK 2004–2014. J Infect 2017; 74(3):236-42.
15. Fayol L, Beizig S, Le Monnier A, et al. Neonatal meningitis due to Listeria monocytogenes after 3 weeks of maternal treatment during pregnancy. Arch Pediatr 2009; 16(4):353-6.
16. Vázquez-Boland JA, Kuhn M, Berche P, et al. Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 2001; 14(3):584-640.
17. Schwarzkopf A. Listeria monocytogenes--aspects of pathogenicity. Pathol Biol 1996; 44(9):769-74.
18. Portnoy DA, Chakraborty T, Goebel W, et al. Molecular determinants of Listeria monocytogenes pathogenesis. Infect Immun 1992; 60(4):1263.
19. Soni DK, Dubey SK. Phylogenetic analysis of the Listeria monocytogenes based on sequencing of 16S rRNA and hlyA genes. Mol Biol Rep 2014; 41(12):8219-29.
20. Soni DK, Singh M, Singh DV, et al. Virulence and genotypic characterization of Listeria monocytogenes isolated from vegetable and soil samples. BMC Microbiol 2014; 14(1):241.
21. Seeliger H, Hönne K. Serotyping of Listeria monocytogenes and related species. Methods Microbiol 1979; 13:31-49.
22. Aarts H, Hakemulder L, Van Hoef A. Genomic typing of Listeria monocytogenes strains by automated laser fluorescence analysis of amplified fragment length polymorphism fingerprint patterns. Int J Food Microbiol 1999; 49(1):95-102.
23. Graves LM, Swaminathan B, Reeves MW, et al. Comparison of ribotyping and multilocus enzyme electrophoresis for subtyping of Listeria monocytogenes isolates. J Clin Microbiol 1994; 32(12):2936-43.
24. Rasmussen OF, Skouboe P, Dons L, et al. Listeria monocytogenes exists in at least three evolutionary lines: evidence from flagellin, invasive associated protein and listeriolysin O genes. Microbiol 1995; 141(9):2053-61.
25. Borucki MK, Call DR. Listeria monocytogenes serotype identification by PCR. J Clin Microbiol 2003; 41(12):5537-40.
26. Tappero JW, Schuchat A, Deaver KA, et al. Reduction in the incidence of human listeriosis in the United States: effectiveness of prevention efforts? JAMA 1995; 273(14):1118-22.
27. Eslami G, Goudarzi H, Ohadi E, et al. Identification of Listeria monocytogenes virulence factors in women with abortion by polymerase chain reaction. Arch Clin Infect Dis 2014; 9(3).e19931.
28. Doumith M, Buchrieser C, Glaser P, et al. Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J Clin Microbiol 2004; 42(8):3819-22.
29. Mohammadzadeh R, Shivaee A, Ohadi E, et al. In silico insight into the dominant type II toxin–antitoxin systems and Clp proteases in Listeria monocytogenes and designation of derived peptides as a novel approach to interfere with this system. Int J Pept Res Ther 2019:1-11.
30. Aurora R, Prakash A, Prakash S. Genotypic characterization of Listeria monocytogenes isolated from milk and ready-to-eat indigenous milk products. Food Control 2009; 20(9):835-9.
31. Shalaby MA, Mohamed MS, Mansour MA, et al. Comparison of polymerase chain reaction and conventional methods for diagnosis of Listeria monocytogenes isolated from different clinical specimens and food stuffs. Clin Lab 2010; 57(11-12):919-24.
32. Shayan R, Satari M, Forouzandeh M. Isolation and identification of Listeria monocytogenes in vaginal samples by PCR. Modares J Med 2009; 12(1):51-58.
33. Jeffers GT, Bruce JL, McDonough PL, et al. Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiol 2001; 147(5):1095-104.
34. Liu D. Identification, subtyping and virulence determination of Listeria monocytogenes, an important foodborne pathogen. J Med Microbiol 2006; 55(6):645-59.
35. Lotfollahi L, Nowrouzi J, Irajian G, et al. Prevalence and antimicrobial resistance profiles of Listeria monocytogenes in spontaneous abortions in humans. Afr J Microbiol Res 2011; 5(14):1990-3.
36. Jamshidi M, Jahromi AS, Davoodian P, et al. Seropositivity for Listeria monocytogenes in women with spontaneous abortion: a case-control study in Iran. Taiwan J Obstet Gynecol 2009; 48(1):46-8.
37. Althaus D, Lehner A, Brisse S, et al. Characterization of Listeria monocytogenes strains isolated during 2011–2013 from human infections in Switzerland. Foodborne Pathog Dis 2014; 11(10):753-8.
38. Indrawattana N, Nibaddhasobon T, Sookrung N, et al. Prevalence of Listeria monocytogenes in raw meats marketed in Bangkok and characterization of the isolates by phenotypic and molecular methods. J Health Popul Nutr 2011; 29(1):26.
| Files | ||
| Issue | Vol 8 No 3-4 (2019) | |
| Section | Original Articles | |
| Keywords | ||
| Listeria monocytogenes Polymerase chain reaction Serotyping Spontaneous abortion. | ||
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How to Cite
1.
Ohadi E, Goudarzi H, Sadeghi Kalani B, Taherpour A, Shivaee A, Eslami G. Serotyping of Listeria monocytogenes Isolates from Women with Spontaneous Abortion Using Polymerase Chain Reaction Method. J Med Bacteriol. 2019;8(3-4):8-17.
