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Open Access 01-12-2024 | Research

Arcobacter species isolated from human stool samples, animal products, ready-to-eat salad mixes, and ambient water: prevalence, antimicrobial susceptibility, and virulence gene profiles

Authors: Hossein Niyayesh, Ebrahim Rahimi, Amir Shakerian, Faham Khamesipour

Published in: BMC Infectious Diseases | Issue 1/2024

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Abstract

Introduction

Arcobacter species are emerging foodborne pathogens increasingly associated with human illness worldwide. They are commonly found in the gastrointestinal tracts of animals and are frequently isolated from various food sources, including raw meat, poultry, and seafood. The aim of this study is to investigate the antimicrobial resistance patterns of Arcobacter spp. isolated from human stool samples, animal products, ready-to-eat salad mixes, and ambient water, assess the presence of resistance genes, and explore their potential implications for public health.

Methods

In this study, a total of 683 samples were collected from the Shahrekord area over a 12-month period. Samples were obtained from human stool, chicken meat, raw cow milk, RTE salad mixes, and environmental water sources. Two different methods were used to detect Arcobacter, depending on the sample type: bacteriological isolation and identification, and molecular identification. After identification, antimicrobial susceptibility testing was conducted. Polymerase chain reaction (PCR) was used to identify ten putative Arcobacter virulence and resistance genes.

Findings

The results revealed that Arcobacter spp. were present in 26.06% (178 out of 683) of the tested samples, with varying isolation rates across different sample types. A. butzleri being the most commonly isolated species across all sample types, while A. cryaerophilus was restricted to RTE salads, surface waters, and chicken meat. Notably, A. skirrowii was only isolated from chicken meat and environmental water. The differences of Arcobacter spp. in prevalence between the sample types were statistically significant (p < 0.05), and no significant seasonal variation was found across the sampling periods (p > 0.05). PCR analysis for ten putative virulence genes indicated that the cadF gene was present in all Arcobacter isolates. Similarly, 83.33% of the tested strains harbored the ciaB gene, while other genes were less frequently detected. Regarding resistance genes, tet(O) (7.69%) was the most identified gene, followed by blaOXA-61 (4.37%).

Conclusion

In conclusion, this study highlights the alarming prevalence of antimicrobial resistance in Arcobacter spp. Monitoring Arcobacter spp. resistance can be achieved through surveillance, risk assessments, antibiotic stewardship in agriculture, public education, research collaborations, rapid diagnostics, and harmonized policies, all aimed at reducing contamination and safeguarding public health effectively.
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Literature
1.
go back to reference Nelapati S, Tumati SR, Thirtham MR, Ramani Pushpa RN, Kamisetty AK, Ch BK. Occurrence, virulence gene and antimicrobial susceptibility profiles of Arcobacter sp. isolated from catla (Catla catla) in India. Lett Appl Microbiol. 2020;70:365–71.CrossRefPubMed Nelapati S, Tumati SR, Thirtham MR, Ramani Pushpa RN, Kamisetty AK, Ch BK. Occurrence, virulence gene and antimicrobial susceptibility profiles of Arcobacter sp. isolated from catla (Catla catla) in India. Lett Appl Microbiol. 2020;70:365–71.CrossRefPubMed
2.
go back to reference Girbau C, Guerra C, Martínez-Malaxetxebarria I, Alonso R, Fernández-Astorga A. Prevalence of ten putative virulence genes in the emerging foodborne pathogen Arcobacter isolated from food products. Food Microbiol. 2015;52:146–9.CrossRefPubMed Girbau C, Guerra C, Martínez-Malaxetxebarria I, Alonso R, Fernández-Astorga A. Prevalence of ten putative virulence genes in the emerging foodborne pathogen Arcobacter isolated from food products. Food Microbiol. 2015;52:146–9.CrossRefPubMed
3.
go back to reference Elmali M, Can HY. Occurence and antimicrobial resistance of Arcobacter species in food and slaughterhouse samples. Food Sci Technol. 2017;37:280–5.CrossRef Elmali M, Can HY. Occurence and antimicrobial resistance of Arcobacter species in food and slaughterhouse samples. Food Sci Technol. 2017;37:280–5.CrossRef
4.
go back to reference Lameei A, Rahimi E, Shakerian A, Momtaz H. Genotyping, antibiotic resistance and prevalence of Arcobacter species in milk and dairy products. Vet Med Sci. 2022;8:1841–9.CrossRefPubMedPubMedCentral Lameei A, Rahimi E, Shakerian A, Momtaz H. Genotyping, antibiotic resistance and prevalence of Arcobacter species in milk and dairy products. Vet Med Sci. 2022;8:1841–9.CrossRefPubMedPubMedCentral
5.
go back to reference Hänel I, Müller E, Santamarina BG, Tomaso H, Hotzel H, Busch A. Antimicrobial Susceptibility and Genomic Analysis of Aliarcobacter cibarius and Aliarcobacter thereius, Two Rarely Detected Aliarcobacter Species. Front Cell Infect Microbiol. 2021;11:532989. https://doi.org/10.3389/fcimb.2021.532989. Hänel I, Müller E, Santamarina BG, Tomaso H, Hotzel H, Busch A. Antimicrobial Susceptibility and Genomic Analysis of Aliarcobacter cibarius and Aliarcobacter thereius, Two Rarely Detected Aliarcobacter Species. Front Cell Infect Microbiol. 2021;11:532989. https://​doi.​org/​10.​3389/​fcimb.​2021.​532989.
6.
go back to reference Jribi H, Sellami H, Amor SB, Ducournau A, Sifré E, Benejat L, Mégraud F, Gdoura R. Occurrence and antibiotic resistance of Arcobacter species isolates from poultry in Tunisia. J Food Prot. 2020;83:2080–6.CrossRefPubMed Jribi H, Sellami H, Amor SB, Ducournau A, Sifré E, Benejat L, Mégraud F, Gdoura R. Occurrence and antibiotic resistance of Arcobacter species isolates from poultry in Tunisia. J Food Prot. 2020;83:2080–6.CrossRefPubMed
7.
go back to reference Uljanovas D, Gölz G, Brückner V, Grineviciene A, Tamuleviciene E, Alter T, Malakauskas M. Prevalence, antimicrobial susceptibility and virulence gene profiles of Arcobacter species isolated from human stool samples, foods of animal origin, ready-to-eat salad mixes and environmental water. Gut Pathog. 2021;13:1–16.CrossRef Uljanovas D, Gölz G, Brückner V, Grineviciene A, Tamuleviciene E, Alter T, Malakauskas M. Prevalence, antimicrobial susceptibility and virulence gene profiles of Arcobacter species isolated from human stool samples, foods of animal origin, ready-to-eat salad mixes and environmental water. Gut Pathog. 2021;13:1–16.CrossRef
9.
go back to reference Fernandez H, Villanueva MP, Mansilla I, Gonzalez M, Latif F. Arcobacter butzleri and A. cryaerophilus in human, animals and food sources, in southern Chile. Braz J Microbiol. 2015;46:145–7.CrossRefPubMedPubMedCentral Fernandez H, Villanueva MP, Mansilla I, Gonzalez M, Latif F. Arcobacter butzleri and A. cryaerophilus in human, animals and food sources, in southern Chile. Braz J Microbiol. 2015;46:145–7.CrossRefPubMedPubMedCentral
10.
go back to reference Morejón IFB, González A, Ferrús MA. Detection, identification, and antimicrobial susceptibility of Arcobacter spp. isolated from shellfish in Spain. Foodborne Pathog Dis. 2017;14:238–43.CrossRefPubMed Morejón IFB, González A, Ferrús MA. Detection, identification, and antimicrobial susceptibility of Arcobacter spp. isolated from shellfish in Spain. Foodborne Pathog Dis. 2017;14:238–43.CrossRefPubMed
11.
go back to reference Brückner V, Fiebiger U, Ignatius R, Friesen J, Eisenblätter M, Höck M, Alter T, Bereswill S, Gölz G, Heimesaat MM. Prevalence and antimicrobial susceptibility of Arcobacter species in human stool samples derived from out-and inpatients: the prospective German Arcobacter prevalence study Arcopath. Gut Pathog. 2020;12:1–8. Brückner V, Fiebiger U, Ignatius R, Friesen J, Eisenblätter M, Höck M, Alter T, Bereswill S, Gölz G, Heimesaat MM. Prevalence and antimicrobial susceptibility of Arcobacter species in human stool samples derived from out-and inpatients: the prospective German Arcobacter prevalence study Arcopath. Gut Pathog. 2020;12:1–8.
12.
go back to reference Emma Y, Angela H, Theo J, Natalie N, Sophia K. Search for Campylobacter reveals high prevalence and pronounced genetic diversity of Arcobacter butzleri in floodwater samples associated with Hurricane Florence in North Carolina, USA. 2020. Emma Y, Angela H, Theo J, Natalie N, Sophia K. Search for Campylobacter reveals high prevalence and pronounced genetic diversity of Arcobacter butzleri in floodwater samples associated with Hurricane Florence in North Carolina, USA. 2020.
13.
go back to reference Ferreira S, Queiroz JA, Oleastro M, Domingues FC. Insights in the pathogenesis and resistance of Arcobacter: a review. Crit Rev Microbiol. 2016;42:364–83.PubMed Ferreira S, Queiroz JA, Oleastro M, Domingues FC. Insights in the pathogenesis and resistance of Arcobacter: a review. Crit Rev Microbiol. 2016;42:364–83.PubMed
14.
go back to reference Hsu T-T, Lee J. Global Distribution and Prevalence of A rcobacter in Food and Water. Zoonoses Public Health. 2015;62:579–89.CrossRefPubMed Hsu T-T, Lee J. Global Distribution and Prevalence of A rcobacter in Food and Water. Zoonoses Public Health. 2015;62:579–89.CrossRefPubMed
16.
go back to reference Perez-Cataluna A, Tapiol J, Benavent C, Sarvise C, Gomez F, Martinez B, Terron-Puig M, Recio G, Vilanova A, Pujol I. Antimicrobial susceptibility, virulence potential and sequence types associated with Arcobacter strains recovered from human faeces. J Med Microbiol. 2017;66:1736–43.CrossRefPubMed Perez-Cataluna A, Tapiol J, Benavent C, Sarvise C, Gomez F, Martinez B, Terron-Puig M, Recio G, Vilanova A, Pujol I. Antimicrobial susceptibility, virulence potential and sequence types associated with Arcobacter strains recovered from human faeces. J Med Microbiol. 2017;66:1736–43.CrossRefPubMed
17.
go back to reference Rathlavath S, Kohli V, Singh AS, Lekshmi M, Tripathi G, Kumar S, Nayak BB. Virulence genotypes and antimicrobial susceptibility patterns of Arcobacter butzleri isolated from seafood and its environment. Int J Food Microbiol. 2017;263:32–7.CrossRefPubMed Rathlavath S, Kohli V, Singh AS, Lekshmi M, Tripathi G, Kumar S, Nayak BB. Virulence genotypes and antimicrobial susceptibility patterns of Arcobacter butzleri isolated from seafood and its environment. Int J Food Microbiol. 2017;263:32–7.CrossRefPubMed
18.
go back to reference Korczak BM, Stieber R, Emler S, Burnens AP, Frey J, Kuhnert P. Genetic relatedness within the genus Campylobacter inferred from rpoB sequences. Int J Syst Evol Microbiol. 2006;56:937–45.CrossRefPubMed Korczak BM, Stieber R, Emler S, Burnens AP, Frey J, Kuhnert P. Genetic relatedness within the genus Campylobacter inferred from rpoB sequences. Int J Syst Evol Microbiol. 2006;56:937–45.CrossRefPubMed
21.
go back to reference Marta C, Giovanni N, Angela M, Loredana C, Elisabetta B, Laura D, Anna M, Gianfranco S, Antonio P. Large genetic diversity of Arcobacter butzleri isolated from raw milk in Southern Italy. Food Microbiol. 2020;89:103403.CrossRefPubMed Marta C, Giovanni N, Angela M, Loredana C, Elisabetta B, Laura D, Anna M, Gianfranco S, Antonio P. Large genetic diversity of Arcobacter butzleri isolated from raw milk in Southern Italy. Food Microbiol. 2020;89:103403.CrossRefPubMed
22.
go back to reference Van den Abeele A-M, Vogelaers D, Van Hende J, Houf K. Prevalence of Arcobacter species among humans, Belgium, 2008–2013. Emerg Infect Dis. 2014;20:1731.PubMedPubMedCentral Van den Abeele A-M, Vogelaers D, Van Hende J, Houf K. Prevalence of Arcobacter species among humans, Belgium, 2008–2013. Emerg Infect Dis. 2014;20:1731.PubMedPubMedCentral
23.
go back to reference Kayman T, Abay S, Hizlisoy H, Atabay HI, Diker KS, Aydin F. Emerging pathogen Arcobacter spp. in acute gastroenteritis: molecular identification, antibiotic susceptibilities and genotyping of the isolated arcobacters. J Med Microbiol. 2012;61:1439–44.CrossRefPubMed Kayman T, Abay S, Hizlisoy H, Atabay HI, Diker KS, Aydin F. Emerging pathogen Arcobacter spp. in acute gastroenteritis: molecular identification, antibiotic susceptibilities and genotyping of the isolated arcobacters. J Med Microbiol. 2012;61:1439–44.CrossRefPubMed
24.
go back to reference Patyal A, Rathore RS, Mohan HV, Dhama K, Kumar A. Prevalence of Arcobacter spp. in humans, animals and foods of animal origin including sea food from India. Transbound Emerg Dis. 2011;58:402–10.CrossRefPubMed Patyal A, Rathore RS, Mohan HV, Dhama K, Kumar A. Prevalence of Arcobacter spp. in humans, animals and foods of animal origin including sea food from India. Transbound Emerg Dis. 2011;58:402–10.CrossRefPubMed
25.
go back to reference Chieffi D, Fanelli F, Fusco V. Arcobacter butzleri: Up-to-date taxonomy, ecology, and pathogenicity of an emerging pathogen. Compr Rev Food Sci Food Saf. 2020;19:2071–109.CrossRefPubMed Chieffi D, Fanelli F, Fusco V. Arcobacter butzleri: Up-to-date taxonomy, ecology, and pathogenicity of an emerging pathogen. Compr Rev Food Sci Food Saf. 2020;19:2071–109.CrossRefPubMed
26.
go back to reference Shange N, Gouws P, Hoffman LC. Campylobacter and Arcobacter species in food-producing animals: prevalence at primary production and during slaughter. World J Microbiol Biotechnol. 2019;35:1–16.CrossRef Shange N, Gouws P, Hoffman LC. Campylobacter and Arcobacter species in food-producing animals: prevalence at primary production and during slaughter. World J Microbiol Biotechnol. 2019;35:1–16.CrossRef
27.
go back to reference Nieva-Echevarria B, Martinez-Malaxetxebarria I, Girbau C, Alonso R, Fernández-Astorga A. Prevalence and genetic diversity of Arcobacter in food products in the north of Spain. J Food Prot. 2013;76:1447–50.CrossRefPubMed Nieva-Echevarria B, Martinez-Malaxetxebarria I, Girbau C, Alonso R, Fernández-Astorga A. Prevalence and genetic diversity of Arcobacter in food products in the north of Spain. J Food Prot. 2013;76:1447–50.CrossRefPubMed
28.
go back to reference Shah AH, Saleha AA, Zunita Z, Murugaiyah M. Arcobacter–An emerging threat to animals and animal origin food products? Trends Food Sci Technol. 2011;22:225–36.CrossRef Shah AH, Saleha AA, Zunita Z, Murugaiyah M. Arcobacter–An emerging threat to animals and animal origin food products? Trends Food Sci Technol. 2011;22:225–36.CrossRef
29.
go back to reference Kim NH, Park SM, Kim HW, Cho TJ, Kim SH, Choi C, Rhee MS. Prevalence of pathogenic Arcobacter species in South Korea: comparison of two protocols for isolating the bacteria from foods and examination of nine putative virulence genes. Food Microbiol. 2019;78:18–24.CrossRefPubMed Kim NH, Park SM, Kim HW, Cho TJ, Kim SH, Choi C, Rhee MS. Prevalence of pathogenic Arcobacter species in South Korea: comparison of two protocols for isolating the bacteria from foods and examination of nine putative virulence genes. Food Microbiol. 2019;78:18–24.CrossRefPubMed
30.
go back to reference Mottola A, Bonerba E, Bozzo G, Marchetti P, Celano GV, Colao V, Terio V, Tantillo G, Figueras MJ, Di Pinto A. Occurrence of emerging food-borne pathogenic Arcobacter spp. isolated from pre-cut (ready-to-eat) vegetables. Int J Food Microbiol. 2016;236:33–7.CrossRefPubMed Mottola A, Bonerba E, Bozzo G, Marchetti P, Celano GV, Colao V, Terio V, Tantillo G, Figueras MJ, Di Pinto A. Occurrence of emerging food-borne pathogenic Arcobacter spp. isolated from pre-cut (ready-to-eat) vegetables. Int J Food Microbiol. 2016;236:33–7.CrossRefPubMed
31.
go back to reference Webb AL, Taboada EN, Selinger LB, Boras VF, Inglis GD. Prevalence and diversity of waterborne Arcobacter butzleri in southwestern Alberta. Canada Can J Microbiol. 2017;63:330–40.CrossRefPubMed Webb AL, Taboada EN, Selinger LB, Boras VF, Inglis GD. Prevalence and diversity of waterborne Arcobacter butzleri in southwestern Alberta. Canada Can J Microbiol. 2017;63:330–40.CrossRefPubMed
32.
go back to reference Laishram M, Rathlavath S, Lekshmi M, Kumar S, Nayak BB. Isolation and characterization of Arcobacter spp. from fresh seafood and the aquatic environment. Int J Food Microbiol. 2016;232:87–9.CrossRefPubMed Laishram M, Rathlavath S, Lekshmi M, Kumar S, Nayak BB. Isolation and characterization of Arcobacter spp. from fresh seafood and the aquatic environment. Int J Food Microbiol. 2016;232:87–9.CrossRefPubMed
33.
go back to reference Gabucci C, Baldelli G, Amagliani G, Schiavano GF, Savelli D, Russo I, Di Lullo S, Blasi G, Napoleoni M, Leoni F, Primavilla S, Massacci FR, Garofolo G, Petruzzelli A. Widespread Multidrug Resistance of Arcobacter butzleri Isolated from Clinical and Food Sources in Central Italy. Antibiotics (Basel). 2023;12(8):1292. https://doi.org/10.3390/antibiotics12081292. PMID: 37627712; PMCID: PMC10451661.CrossRefPubMed Gabucci C, Baldelli G, Amagliani G, Schiavano GF, Savelli D, Russo I, Di Lullo S, Blasi G, Napoleoni M, Leoni F, Primavilla S, Massacci FR, Garofolo G, Petruzzelli A. Widespread Multidrug Resistance of Arcobacter butzleri Isolated from Clinical and Food Sources in Central Italy. Antibiotics (Basel). 2023;12(8):1292. https://​doi.​org/​10.​3390/​antibiotics12081​292. PMID: 37627712; PMCID: PMC10451661.CrossRefPubMed
40.
41.
go back to reference Piva S, Gariano GR, Bonilauri P, Giacometti F, Decastelli L, Florio D, Massella E, Serraino A. Occurrence of putative virulence genes on Arcobacter butzleri isolated from three different environmental sites throughout the dairy chain. J Appl Microbiol. 2017;122:1071–7.CrossRefPubMed Piva S, Gariano GR, Bonilauri P, Giacometti F, Decastelli L, Florio D, Massella E, Serraino A. Occurrence of putative virulence genes on Arcobacter butzleri isolated from three different environmental sites throughout the dairy chain. J Appl Microbiol. 2017;122:1071–7.CrossRefPubMed
42.
go back to reference Miller WG, Parker CT, Rubenfield M, Mendz GL, Wösten MM, Ussery DW, Stolz JF, Binnewies TT, Hallin PF, Wang G. The complete genome sequence and analysis of the epsilonproteobacterium Arcobacter butzleri. PLoS One. 2007;2:e1358.CrossRefPubMedPubMedCentral Miller WG, Parker CT, Rubenfield M, Mendz GL, Wösten MM, Ussery DW, Stolz JF, Binnewies TT, Hallin PF, Wang G. The complete genome sequence and analysis of the epsilonproteobacterium Arcobacter butzleri. PLoS One. 2007;2:e1358.CrossRefPubMedPubMedCentral
Metadata
Title
Arcobacter species isolated from human stool samples, animal products, ready-to-eat salad mixes, and ambient water: prevalence, antimicrobial susceptibility, and virulence gene profiles
Authors
Hossein Niyayesh
Ebrahim Rahimi
Amir Shakerian
Faham Khamesipour
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2024
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-024-10256-9

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