Prevalence, species diversity, and antimicrobial susceptibility of Campylobacter strains in patients with diarrhea and poultry meat samples: one-year prospective study
-
Atena Sadeghi
,
Leila Ganji
,
Fereshteh Fani
,
Gholamreza Pouladfar
,
Parisa Eslami
,
Fatemeh Doregiraee
,
Parviz Owlia
,
Masoud Alebouyeh
Abstract
Background and Objectives: Source tracking of antimicrobial resistance in Campylobacter is useful for control measures. In this study, Campylobacter-associated diarrhea and homology in antimicrobial resistance of humans and poultry meat isolates were investigated.
Materials and Methods: A total of 400 stools of patients and 100 poultry meat samples were analyzed. Susceptibility of the isolates was detected by disk diffusion, Etest, and agar dilution methods. Mismatch amplification mutation assay was used for the detection of mutations in the gyrA quinolone resistance determining region (QRDR).
Results: Campylobacter spp., including C. jejuni, C. coli, and C. lari, were detected in 35% of the chicken meat and 6.75% of the stool samples, respectively. The QRDR mutation was detected in most of the stool and chicken meat samples. Although the frequency of resistance to tetracycline (53.5% and 62.8%), erythromycin (39.2% and 37.1%), and gentamicin (32.1% and 31.4%) was relatively similar, higher frequency of resistance to ciprofloxacin (51.4% vs 28.6%) and nalidixic acid (42.15% vs 28.6%) among the chicken meat, and ampicillin (50% and 17.1%) among the human stool was detected.
Conclusion: High percentage of poultry meat samples is contaminated with different Campylobacter species, which shows homology with the patients’ isolates in Tehran.
1. Besharati S, Sadeghi A, Ahmadi F, Tajeddin E, Salehi RM, Fani F, et al. Serogroups, and drug resistance of nontyphoidal Salmonella in symptomatic patients with community-acquired diarrhea and chicken meat samples in Tehran. Iran J Vet Res 2020; 21: 269-278.
2. Naumova EN, Jagai JS, Matyas B, DeMaria A Jr, MacNeill IB, Griffiths J. Seasonality in six enterically transmitted diseases and ambient temperature. Epidemiol Infect 2007; 135: 281-292.
3. Alegbeleye OO, Singleton I, Sant'Ana AS. Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: A review. Food Microbiol 2018; 73: 177-208.
4. Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, et al. Global regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 2012; 379: 2151-2161.
5. Skarp CPA, Hänninen ML, Rautelin HIK. Campylobacteriosis: the role of poultry meat. Clin Microbiol Infect 2016; 22: 103-109.
6. Igwaran A, Okoh AI. Human campylobacteriosis: A public health concern of global importance. Heliyon 2019; 5(11): e02814.
7. Jazayeri Moghadas A, Irajian G, Kalantari F, Monem M, Salehian A, Rahbar H, et al. Prevalence of Campylobacter jejuni in diarrheic children in Semnan (Iran). Koomesh 2008; 9: 297-300.
8. Hermans D, Pasmans F, Messens W, Martel A, Van Immerseel F, Rasschaert G, et al. Poultry as a host for the zoonotic pathogen Campylobacter jejuni. Vector Borne Zoonotic Dis 2012; 12: 89-98.
9. EFSA Panel On Biological Hazards ((BIOHAZ). Scientific opinion on Campylobacter in broiler meat production: control options and performance objectives and/or targets at different stages of the food chain. EFSA J 2011; 9: 2105.
10. Agunos A, Waddell L, Léger D, Taboada E. A systematic review characterizing on-farm sources of Campylobacter spp. for broiler chickens. PLoS One 2014; 9(8): e104905.
11. Cha W, Mosci RE, Wengert SL, Venegas Vargas C, Rust SR, Bartlett PC, et al. Comparing the genetic diversity and antimicrobial resistance profiles of Campylobacter jejuni recovered from cattle and humans. Front Microbiol 2017; 8: 818.
12. Tang M, Zhou Q, Zhang X, Zhou S, Zhang J, Tang X, et al. Antibiotic resistance profiles and molecular mechanisms of Campylobacter from chicken and pig in China. Front Microbiol 2020; 11: 592496.
13. Zirnstein G, Li Y, Swaminathan B, Angulo F. Ciprofloxacin resistance in Campylobacter jejuni isolates: detection of gyrA resistance mutations by mismatch amplification mutation assay PCR and DNA sequence analysis. J Clin Microbiol 1999; 37: 3276-3280.
14. Lehtopolku M, Nakari UM, Kotilainen P, Huovinen P, Siitonen A, Hakanen AJ. Antimicrobial susceptibilities of multidrug-resistant Campylobacter jejuni and C. coli strains: in vitro activities of 20 antimicrobial agent. Antimicrob Agents Chemother 2010; 54: 1232-1236.
15. Di Giannatale E, Calistri P, Di Donato G, Decastelli L, Goffredo E, Adriano D, et al. Thermotolerant Campylobacter spp. in chicken and bovine meat in Italy: Prevalence, level of contamination and molecular characterization of isolates. PLoS One 2019; 14(12): e0225957.
16. Sadkowska-Todys M, Kucharczyk B. Campylobacteriosis in Poland in 2010. Przegl Epidemiol 2013; 67: 227-229, 341-342.17. Kubota K, Kasuga F, Iwasaki E, Inagaki S, Sakurai Y, Komatsu M, et al. Estimating the burden of acute
gastroenteritis and foodborne illness caused by Campylobacter, Salmonella, and Vibrio parahaemolyticus by using population-based telephone survey data, Miyagi Prefecture, Japan, 2005 to 2006. J Food Prot 2011; 74: 1592-1598.
18. Thépault A, Rose V, Quesne S, Poezevara T, Béven V, Hirchaud E, et al. Ruminant and chicken: important sources of campylobacteriosis in France despite a variation of source attribution in 2009 and 2015. Sci Rep 2018; 8: 9305.
19. Bian X, Garber JM, Cooper KK, Huynh S, Jones J, Mills MK, et al. Campylobacter abundance in breastfed infants and identification of a new species in the global enterics multicenter study. mSphere 2020; 5(1): e 00735-19.
20. Nichols GL. Fly transmission of Campylobacter. Emerg Infect Dis 2005; 11: 361-364.
21. Divsalar G, Kaboosi H, Khoshbakht R, Shirzad-Aski H, Ghadikolaii FP. Antimicrobial resistances, and molecular typing of Campylobacter jejuni isolates, separated from food-producing animals and diarrhea patients in Iran. Comp Immunol Microbiol Infect Dis 2019; 65: 194-200.
22. Raeisi M, Khoshbakht R, Ghaemi EA, Bayani M, Hashemi M, Seyedghasemi NS, et al. Antimicrobial resistance and virulence-associated genes of Campylobacter spp. isolated from raw milk, fish, poultry, and red meat. Microb Drug Resist 2017; 23: 925-933.
23. Maktabi S, Ghorbanpoor M, Hossaini M, Motavalibashi A. Detection of multi-antibiotic resistant Campylobacter coli and Campylobacter jejuni in beef, mutton, chicken and water buffalo meat in Ahvaz, Iran. Vet Res Forum 2019; 10: 37-42.
24. Bullman S, Corcoran D, O'Leary J, O'Hare D, Lucey B, Sleator RD. Emerging dynamics of human campylobacteriosis in Southern Ireland. FEMS Immunol Med Microbiol 2011; 63: 248-253.
25. Mukherjee P, Ramamurthy T, Bhattacharya MK, Rajendran K, Mukhopadhyay AK. Campylobacter jejuni in hospitalized patients with diarrhea, Kolkata, India. Emerg Infect Dis 2013; 19: 1155-1156.
26. OzFoodNet Working Group. Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: annual report of the OzFoodNet network, 2010. Commun Dis Intell Q Rep 2012; 36: E213-41.
27. Swierczewski BE, Odundo EA, Koech MC, Ndonye JN, Kirera RK, Odhiambo CP, et al. Enteric pathogen surveillance in a case-control study of acute diarrhoea in the town of Kisii, Kenya. J Med Microbiol 2013; 62: 1774-1776.
28. Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM. Global epidemiology of Campylobacter infection. Clin Microbiol Rev 2015; 28: 687-720.
29. Szczepanska B, Andrzejewska M, Spica D, Klawe JJ. Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from children and environmental sources in urban and suburban areas. BMC Microbiol 2017; 17: 80.
30. Rawat N, Maansi, Kumar D, Upadhyay AK. Virulence typing and antibiotic susceptibility profiling of thermophilic Campylobacters isolated from poultry, animal, and human species. Vet World 2018; 11: 1698-1705.
31. Ma H, Su Y, Ma L, Ma L, Li P, Du X, et al. Prevalence and characterization of Campylobacter jejuni isolated from retail chicken in Tianjin, China. J Food Prot 2017; 80: 1032-1040.32. Han J, Wang Y, Sahin O, Shen Z, Guo B, Shen J, et
al. A fluoroquinolone resistance associated mutation in gyrA Affects DNA supercoiling in Campylobacter jejuni. Front Cell Infect Microbiol 2012; 2: 21.
33. Garcia-Migura L, Hendriksen RS, Fraile L, Aarestrup FM. Antimicrobial resistance of zoonotic and commensal bacteria in Europe: the missing link between consumption and resistance in veterinary medicine. Vet Microbiol 2014; 170: 1-9.
Union Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2013. EFSA J 2015; 13: 4036.
35. Yan M, Sahin O, Lin J, Zhang Q. Role of the CmeABC efflux pump in the emergence of fluoroquinolone-resistant Campylobacter under selection pressure. J Antimicrob Chemother 2006; 58: 1154-1159.
36. Schiaffino F, Colston JM, Paredes-Olortegui M, François R, Pisanic N, Burga R, et al. Antibiotic resistance of Campylobacter species in a pediatric cohort study. Antimicrob Agents Chemother 2019; 63(2): e01911-18.
37. Wagner J, Jabbusch M, Eisenblätter M, Hahn H, Wendt C, Ignatius R. Susceptibilities of Campylobacter jejuni isolates from Germany to ciprofloxacin, moxifloxacin, erythromycin, clindamycin, and tetracycline.
Antimicrob Agents Chemother 2003; 47: 2358-2361.
38. Du Y, Wang C, Ye Y, Liu Y, Wang A, Li Y, et al. Molecular identification of multidrug-resistant Campylobacter species from diarrheal patients and poultry meat in Shanghai, China. Front Microbiol 2018; 9: 1-8.
39. Sjögren E, Lindblom GB, Kaijser B. Norfloxacin resistance in Campylobacter jejuni and Campylobacter coli isolates from Swedish patients. J Antimicrob Chemother 1997; 40: 257-261.
40. Nannapaneni R, Story R, Wiggins KC, Johnson MG. Concurrent quantitation of total Campylobacter and total ciprofloxacin-resistant Campylobacter loads in rinses from retail raw chicken carcasses from 2001 to 2003 by direct plating at 42 degrees C. Appl Environ Microbiol 2005; 71: 4510-4515.
41. Logan JM, Edwards KJ, Saunders NA, Stanley J. Rapid identification of Campylobacter spp. by melting peak analysis of biprobes in real-time PCR. J Clin Microbiol 2001; 39: 2227-2232.
42. van de Giessen AW, Tilburg JJ, Ritmeester WS, van der Plas J. Reduction of Campylobacter infections in broiler flocks by application of hygiene measures. Epidemiol Infect 1998; 121: 57-66.
43. Yamazaki-Matsune W, Taguchi M, Seto K, Kawahara R, Kawatsu K, Kumeda Y, et al. Development of a multiplex PCR assay for identification of Campylobacter coli, Campylobacter fetus, Campylobacter hyointestinalis subsp. hyointestinalis, Campylobacter jejuni, Campylobacter lari and Campylobacter upsaliensis. J Med Microbiol 2007; 56: 1467-1473.
44. Wang G, Clark CG, Taylor TM, Pucknell C, Barton C, Price L, et al. Colony multiplex PCR assay for identification and differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. J Clin Microbiol 2002; 40: 4744-4747.
45. Zirnstein G, Li Y, Swaminathan B, Angulo F. Ciprofloxacin resistance in Campylobacter jejuni isolates: detection of gyrA resistance mutations by mismatch amplification mutation assay PCR and DNA sequence analysis. J Clin Microbiol 1999; 37: 3276-3280.
2. Naumova EN, Jagai JS, Matyas B, DeMaria A Jr, MacNeill IB, Griffiths J. Seasonality in six enterically transmitted diseases and ambient temperature. Epidemiol Infect 2007; 135: 281-292.
3. Alegbeleye OO, Singleton I, Sant'Ana AS. Sources and contamination routes of microbial pathogens to fresh produce during field cultivation: A review. Food Microbiol 2018; 73: 177-208.
4. Liu L, Johnson HL, Cousens S, Perin J, Scott S, Lawn JE, et al. Global regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet 2012; 379: 2151-2161.
5. Skarp CPA, Hänninen ML, Rautelin HIK. Campylobacteriosis: the role of poultry meat. Clin Microbiol Infect 2016; 22: 103-109.
6. Igwaran A, Okoh AI. Human campylobacteriosis: A public health concern of global importance. Heliyon 2019; 5(11): e02814.
7. Jazayeri Moghadas A, Irajian G, Kalantari F, Monem M, Salehian A, Rahbar H, et al. Prevalence of Campylobacter jejuni in diarrheic children in Semnan (Iran). Koomesh 2008; 9: 297-300.
8. Hermans D, Pasmans F, Messens W, Martel A, Van Immerseel F, Rasschaert G, et al. Poultry as a host for the zoonotic pathogen Campylobacter jejuni. Vector Borne Zoonotic Dis 2012; 12: 89-98.
9. EFSA Panel On Biological Hazards ((BIOHAZ). Scientific opinion on Campylobacter in broiler meat production: control options and performance objectives and/or targets at different stages of the food chain. EFSA J 2011; 9: 2105.
10. Agunos A, Waddell L, Léger D, Taboada E. A systematic review characterizing on-farm sources of Campylobacter spp. for broiler chickens. PLoS One 2014; 9(8): e104905.
11. Cha W, Mosci RE, Wengert SL, Venegas Vargas C, Rust SR, Bartlett PC, et al. Comparing the genetic diversity and antimicrobial resistance profiles of Campylobacter jejuni recovered from cattle and humans. Front Microbiol 2017; 8: 818.
12. Tang M, Zhou Q, Zhang X, Zhou S, Zhang J, Tang X, et al. Antibiotic resistance profiles and molecular mechanisms of Campylobacter from chicken and pig in China. Front Microbiol 2020; 11: 592496.
13. Zirnstein G, Li Y, Swaminathan B, Angulo F. Ciprofloxacin resistance in Campylobacter jejuni isolates: detection of gyrA resistance mutations by mismatch amplification mutation assay PCR and DNA sequence analysis. J Clin Microbiol 1999; 37: 3276-3280.
14. Lehtopolku M, Nakari UM, Kotilainen P, Huovinen P, Siitonen A, Hakanen AJ. Antimicrobial susceptibilities of multidrug-resistant Campylobacter jejuni and C. coli strains: in vitro activities of 20 antimicrobial agent. Antimicrob Agents Chemother 2010; 54: 1232-1236.
15. Di Giannatale E, Calistri P, Di Donato G, Decastelli L, Goffredo E, Adriano D, et al. Thermotolerant Campylobacter spp. in chicken and bovine meat in Italy: Prevalence, level of contamination and molecular characterization of isolates. PLoS One 2019; 14(12): e0225957.
16. Sadkowska-Todys M, Kucharczyk B. Campylobacteriosis in Poland in 2010. Przegl Epidemiol 2013; 67: 227-229, 341-342.17. Kubota K, Kasuga F, Iwasaki E, Inagaki S, Sakurai Y, Komatsu M, et al. Estimating the burden of acute
gastroenteritis and foodborne illness caused by Campylobacter, Salmonella, and Vibrio parahaemolyticus by using population-based telephone survey data, Miyagi Prefecture, Japan, 2005 to 2006. J Food Prot 2011; 74: 1592-1598.
18. Thépault A, Rose V, Quesne S, Poezevara T, Béven V, Hirchaud E, et al. Ruminant and chicken: important sources of campylobacteriosis in France despite a variation of source attribution in 2009 and 2015. Sci Rep 2018; 8: 9305.
19. Bian X, Garber JM, Cooper KK, Huynh S, Jones J, Mills MK, et al. Campylobacter abundance in breastfed infants and identification of a new species in the global enterics multicenter study. mSphere 2020; 5(1): e 00735-19.
20. Nichols GL. Fly transmission of Campylobacter. Emerg Infect Dis 2005; 11: 361-364.
21. Divsalar G, Kaboosi H, Khoshbakht R, Shirzad-Aski H, Ghadikolaii FP. Antimicrobial resistances, and molecular typing of Campylobacter jejuni isolates, separated from food-producing animals and diarrhea patients in Iran. Comp Immunol Microbiol Infect Dis 2019; 65: 194-200.
22. Raeisi M, Khoshbakht R, Ghaemi EA, Bayani M, Hashemi M, Seyedghasemi NS, et al. Antimicrobial resistance and virulence-associated genes of Campylobacter spp. isolated from raw milk, fish, poultry, and red meat. Microb Drug Resist 2017; 23: 925-933.
23. Maktabi S, Ghorbanpoor M, Hossaini M, Motavalibashi A. Detection of multi-antibiotic resistant Campylobacter coli and Campylobacter jejuni in beef, mutton, chicken and water buffalo meat in Ahvaz, Iran. Vet Res Forum 2019; 10: 37-42.
24. Bullman S, Corcoran D, O'Leary J, O'Hare D, Lucey B, Sleator RD. Emerging dynamics of human campylobacteriosis in Southern Ireland. FEMS Immunol Med Microbiol 2011; 63: 248-253.
25. Mukherjee P, Ramamurthy T, Bhattacharya MK, Rajendran K, Mukhopadhyay AK. Campylobacter jejuni in hospitalized patients with diarrhea, Kolkata, India. Emerg Infect Dis 2013; 19: 1155-1156.
26. OzFoodNet Working Group. Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: annual report of the OzFoodNet network, 2010. Commun Dis Intell Q Rep 2012; 36: E213-41.
27. Swierczewski BE, Odundo EA, Koech MC, Ndonye JN, Kirera RK, Odhiambo CP, et al. Enteric pathogen surveillance in a case-control study of acute diarrhoea in the town of Kisii, Kenya. J Med Microbiol 2013; 62: 1774-1776.
28. Kaakoush NO, Castaño-Rodríguez N, Mitchell HM, Man SM. Global epidemiology of Campylobacter infection. Clin Microbiol Rev 2015; 28: 687-720.
29. Szczepanska B, Andrzejewska M, Spica D, Klawe JJ. Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from children and environmental sources in urban and suburban areas. BMC Microbiol 2017; 17: 80.
30. Rawat N, Maansi, Kumar D, Upadhyay AK. Virulence typing and antibiotic susceptibility profiling of thermophilic Campylobacters isolated from poultry, animal, and human species. Vet World 2018; 11: 1698-1705.
31. Ma H, Su Y, Ma L, Ma L, Li P, Du X, et al. Prevalence and characterization of Campylobacter jejuni isolated from retail chicken in Tianjin, China. J Food Prot 2017; 80: 1032-1040.32. Han J, Wang Y, Sahin O, Shen Z, Guo B, Shen J, et
al. A fluoroquinolone resistance associated mutation in gyrA Affects DNA supercoiling in Campylobacter jejuni. Front Cell Infect Microbiol 2012; 2: 21.
33. Garcia-Migura L, Hendriksen RS, Fraile L, Aarestrup FM. Antimicrobial resistance of zoonotic and commensal bacteria in Europe: the missing link between consumption and resistance in veterinary medicine. Vet Microbiol 2014; 170: 1-9.
Union Summary Report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2013. EFSA J 2015; 13: 4036.
35. Yan M, Sahin O, Lin J, Zhang Q. Role of the CmeABC efflux pump in the emergence of fluoroquinolone-resistant Campylobacter under selection pressure. J Antimicrob Chemother 2006; 58: 1154-1159.
36. Schiaffino F, Colston JM, Paredes-Olortegui M, François R, Pisanic N, Burga R, et al. Antibiotic resistance of Campylobacter species in a pediatric cohort study. Antimicrob Agents Chemother 2019; 63(2): e01911-18.
37. Wagner J, Jabbusch M, Eisenblätter M, Hahn H, Wendt C, Ignatius R. Susceptibilities of Campylobacter jejuni isolates from Germany to ciprofloxacin, moxifloxacin, erythromycin, clindamycin, and tetracycline.
Antimicrob Agents Chemother 2003; 47: 2358-2361.
38. Du Y, Wang C, Ye Y, Liu Y, Wang A, Li Y, et al. Molecular identification of multidrug-resistant Campylobacter species from diarrheal patients and poultry meat in Shanghai, China. Front Microbiol 2018; 9: 1-8.
39. Sjögren E, Lindblom GB, Kaijser B. Norfloxacin resistance in Campylobacter jejuni and Campylobacter coli isolates from Swedish patients. J Antimicrob Chemother 1997; 40: 257-261.
40. Nannapaneni R, Story R, Wiggins KC, Johnson MG. Concurrent quantitation of total Campylobacter and total ciprofloxacin-resistant Campylobacter loads in rinses from retail raw chicken carcasses from 2001 to 2003 by direct plating at 42 degrees C. Appl Environ Microbiol 2005; 71: 4510-4515.
41. Logan JM, Edwards KJ, Saunders NA, Stanley J. Rapid identification of Campylobacter spp. by melting peak analysis of biprobes in real-time PCR. J Clin Microbiol 2001; 39: 2227-2232.
42. van de Giessen AW, Tilburg JJ, Ritmeester WS, van der Plas J. Reduction of Campylobacter infections in broiler flocks by application of hygiene measures. Epidemiol Infect 1998; 121: 57-66.
43. Yamazaki-Matsune W, Taguchi M, Seto K, Kawahara R, Kawatsu K, Kumeda Y, et al. Development of a multiplex PCR assay for identification of Campylobacter coli, Campylobacter fetus, Campylobacter hyointestinalis subsp. hyointestinalis, Campylobacter jejuni, Campylobacter lari and Campylobacter upsaliensis. J Med Microbiol 2007; 56: 1467-1473.
44. Wang G, Clark CG, Taylor TM, Pucknell C, Barton C, Price L, et al. Colony multiplex PCR assay for identification and differentiation of Campylobacter jejuni, C. coli, C. lari, C. upsaliensis, and C. fetus subsp. fetus. J Clin Microbiol 2002; 40: 4744-4747.
45. Zirnstein G, Li Y, Swaminathan B, Angulo F. Ciprofloxacin resistance in Campylobacter jejuni isolates: detection of gyrA resistance mutations by mismatch amplification mutation assay PCR and DNA sequence analysis. J Clin Microbiol 1999; 37: 3276-3280.
| Files | ||
| Issue | Vol 14 No 3 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i3.9775 | |
| Keywords | ||
| Foodborne diseases; Campylobacter; Drug resistance; Diarrhea; Poultry | ||
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How to Cite
1.
Sadeghi A, Ganji L, Fani F, Pouladfar G, Eslami P, Doregiraee F, Owlia P, Alebouyeh M. Prevalence, species diversity, and antimicrobial susceptibility of Campylobacter strains in patients with diarrhea and poultry meat samples: one-year prospective study. Iran J Microbiol. 2022;14(3):362-372.
