High prevalence of antibiotic resistance and biofilm formation in Salmonella Gallinarum
-
Reza Khaltabadi Farahani
,
Mina Ebrahimi-Rad
,
Nader Shahrokhi
,
Amir Hossien Khaltabadi Farahani
,
Seyed Ali Ghafouri
,
Maryam Rezaei
,
Safoora Gharibzadeh
,
Arash Ghalyanchi Langeroudi
,
Parastoo Ehsani
Abstract
Background and Objectives: Antibiotic resistance is an indicator of the passively acquired and circulating resistance genes. Salmonella Gallinarum significantly affects the poultry food industry. The present study is the first study of the S. Gallinarum biofilm in Iran, which is focused on the characterization of the S. Gallinarum serovars and their acquired antibiotic resistance genes circulating in poultry fields in central and northwestern Iran.
Materials and Methods: Sixty isolates of S. Gallinarum serovar were collected from feces of live poultry. The bacteria were isolated using biochemical tests and confirmed by Multiplex PCR. Biofilm formation ability and the antibacterial resistance were evaluated using both phenotypic and genotypic methods. The data were analyzed using SPSS software.
Results: According to Multiplex PCR for ratA, SteB, and rhs genes, all 60 S. Gallinarum serovars were Gallinarum biovars. In our study, the antibiotic resistance rate among isolated strains was as follows: Penicillin (100%), nitrofurantoin (80%), nalidixic acid (45%), cefoxitin (35%), neomycin sulfate (30%), chloramphenicol (20%), and ciprofloxacin (5%). All isolates were susceptible to imipenem, ertapenem, ceftriaxone, ceftazidime, and ceftazidime+clavulanic acid. All sixty isolates did not express the resistance genes IMP, VIM, NDM, DHA, blaOXA48, and qnrA. On the other hand, they expressed GES (85%), qnrB (75%), Fox M (70%), SHV (60%), CITM (20%), KPC (15%), FOX (10%), MOXM (5%), and qnrS (5%). All S. Gallinarum isolates formed biofilm and expressed sdiA gene.
Conclusion: Considering that the presence of this bacteria is equal to the death penalty to the herd, the distribution of resistance genes could be a critical alarm for pathogen monitoring programs in the region. This study showed a positive correlation between biofilm formation and 50% of tested resistance genes. Also, it was found that the most common circulating S. gallinarum biovars are multidrug-resistant.
1. Shivaprasad HL. Fowl typhoid and pullorum disease. Rev Sci Tech 2000; 19: 405-424.
2. Foley SL, Johnson TJ, Ricke SC, Nayak R, Danzeisen J. Salmonella pathogenicity and host adaptation in chicken-associated serovars. Microbiol Mol Biol Rev 2013; 77: 582-607.
3. Song L, Tan R, Xiong D, Jiao X, Pan Z. Accurate identification and discrimination of Salmonella enterica serovar Gallinarum biovars Gallinarum and Pullorum by a multiplex PCR based on the new genes of torT and I137_14430. Front Vet Sci 2023; 10: 1220118.
4. Batista DF, de Freitas Neto OC, de Almeida AM, Barrow PA, de Oliveira Barbosa F, Berchieri Junior A. Molecular identification of Salmonella enterica subsp. enterica serovar Gallinarum biovars Gallinarum and Pullorum by a duplex PCR assay. J Vet Diagn Invest 2016; 28: 419-422.
5. Zhou X, Kang X, Zhou K, Yue M. A global dataset for prevalence of Salmonella Gallinarum between 1945 and 2021. Sci Data 2022; 9: 495.
6. Sharma D, Misba L, Khan AU. Antibiotics versus biofilm: an emerging battleground in microbial communities. Antimicrob Resist Infect Control 2019; 8: 76.
7. Lizcano A, Chin T, Sauer K, Tuomanen EI, Orihuela CJ. Early biofilm formation on microtiter plates is not correlated with the invasive disease potential of Streptococcus pneumoniae. Microb Pathog 2010; 48: 124-130.
8. Stepanović S, Cirković I, Ranin L, Svabić-Vlahović M. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol 2004; 38: 428-432.
9. Youn SY, Jeong OM, Choi BK, Jung SC, Kang MS. Comparison of the antimicrobial and sanitizer resistance of Salmonella isolates from chicken Slaughter processes in Korea. J Food Sci 2017; 82: 711-717.
10. Ghasemmahdi H, Tajik H, Moradi M, Mardani K, Modaresi R, Badali A, et al. Antibiotic resistance pattern and biofilm formation ability of clinically isolates of Salmonella enterica serotype typhimurium. Int J Enteric Pathog 2015; 3(2): e27372.
11. Rabsch W, Hargis BM, Tsolis RM, Kingsley RA, Hinz KH, Tschäpe H, et al. Competitive exclusion of Salmonella enteritidis by Salmonella gallinarum in poultry. Emerg Infect Dis 2000; 6: 443-448.
12. Nhung NT, Chansiripornchai N, Carrique-Mas JJ. Antimicrobial resistance in bacterial poultry pathogens: A Review. Front Vet Sci 2017; 4: 126.
13. Cao J, Xu L, Yuan M, Ke B, Xiang D, Ke C, et al. TaqMan probe real-time PCR detection of foodborne Salmonella enterica and its six serovars. Int J Curr Microbiol App Sci 2013; 2: 1-12.
14. Pugliese N, Circella E, Pazzani C, Pupillo A, Camarda A. Validation of a seminested PCR approach for rapid detection of Salmonella enterica subsp. enterica serovar Gallinarum. J Microbiol Methods 2011; 85: 22-27.
15. Zhu C, Yue M, Rankin S, Weill F-X, Frey J, Schifferli DM. One-step identification of five prominent chicken Salmonella serovars and biotypes. J Clin Microbiol 2015; 53: 3881-3883.
16. Batista DF, de Freitas Neto OC, Lopes PD, de Almeida AM, Barrow PA, Berchieri A Jr. Polymerase chain reaction assay based on ratA gene allows differentiation between Salmonella enterica subsp. enterica serovar Gallinarum biovars Gallinarum and Pullorum. J Vet Diagn Invest 2013; 25: 259-262.
17. Zhu Y, Peng L, Chen D, Yu G. Intercalation Pseudocapacitance in Ultrathin VOPO4 nanosheets: toward high-rate Alkali-Ion-based electrochemical energy storage. Nano Lett 2016; 16: 742-747.
18. Batista DFA (2013). Análise comparativa dos genomas de Salmonella enterica subsp. enterica sorovar Gallinarum biovares Gallinarum 287/91 e Pullorum 449/87 para identificação de regiões de diferenças (RODs).
19. Migratory birds wintering in Iran increased by 26.5%, Tehran Times 31 December. Tehran Times, 2018.
20. Poirel L, Walsh TR, Cuvillier V, Nordmann P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis 2011; 70: 119-123.
21. Doyle D, Peirano G, Lascols C, Lloyd T, Church DL, Pitout JD. Laboratory detection of Enterobacteriaceae that produce carbapenemases. J Clin Microbiol 2012; 50: 3877-3880.
22. Du J, Li P, Liu H, Lü D, Liang H, Dou Y. Phenotypic and molecular characterization of multidrug resistant Klebsiella pneumoniae isolated from a university teaching hospital, China. PLoS One 2014; 9(4): e95181.
23. Silagyi K, Kim S-H, Lo YM, Wei C-I. Production of biofilm and quorum sensing by Escherichia coli O157:H7 and its transfer from contact surfaces to meat, poultry, ready-to-eat deli, and produce products. Food Microbiol 2009; 26: 514-519.
24. Stepanovic S, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 2000; 40: 175-179.
25. Saffar H, Asgari Niaraki N, Ghahroudi Tali A, Baseri Z, Abdollahi A, Yalfani R. Prevalence of AmpC β-lactamase in clinical isolates of Escherichia coli, Klebsiella spp., and Proteus mirabilis in a tertiary Hospital in Tehran, Iran. Jundishapur J Microbiol 2016; 9(12): e39121.
26. Turki Y, Mehr I, Ouzari H, Khessairi A, Hassen A. Molecular typing, antibiotic resistance, virulence gene and biofilm formation of different Salmonella enterica serotypes. J Gen Appl Microbiol 2014; 60: 123-130.
27. Davarzani F, Saidi N, Besharati S, Saderi H, Rasooli I, Owlia P. Evaluation of antibiotic resistance pattern, alginate and biofilm production in clinical isolates of Pseudomonas aeruginosa. Iran J Public Health 2021; 50: 341-349.
28. Soria MC, Soria MA, Bueno DJ, Terzolo HR. Comparison of 3 culture methods and PCR assays for Salmonella gallinarum and Salmonella pullorum detection in poultry feed. Poult Sci 2013; 92: 1505-1515.
29. Oliveira SD, Santos LR, Schuch DM, Silva AB, Salle CT, Canal CW. Detection and identification of salmonellas from poultry-related samples by PCR. Vet Microbiol 2002; 87: 25-35.
30. Xiong D, Song L, Pan Z, Jiao X. Identification and discrimination of Salmonella enterica serovar Gallinarum biovars Pullorum and Gallinarum based on a one-step multiplex PCR assay. Front Microbiol 2018; 9: 1718.
31. Kumar A, Balachandran Y, Gupta S, Khare S, Suman. Quick PCR based diagnosis of typhoid using specific genetic markers. Biotechnol Lett 2010; 32: 707-712.
32. Paiva J, Cavallini JS, Silva MD, Almeida MA, Ângela HL, Berchieri Junior A. Molecular differentiation of Salmonella Gallinarum and Salmonella Pullorum by RFLP of fliC gene from Brazilian isolates. Braz J Poult Sci 2009; 11: 271-275.
33. Hur J, Kim JH, Park JH, Lee YJ, Lee J-H. Molecular and virulence characteristics of multi-drug resistant Salmonella Enteritidis strains isolated from poultry. Vet J 2011; 189: 306-311.
34. Kelly BG, Vespermann A, Bolton DJ. Horizontal gene transfer of virulence determinants in selected bacterial foodborne pathogens. Food Chem Toxicol 2009; 47: 969-977.
35. Sedighi M, Halajzadeh M, Ramazanzadeh R, Amirmozafari N, Heidary M, Pirouzi S. Molecular detection of β-lactamase and integron genes in clinical strains of Klebsiella pneumoniae by multiplex polymerase chain reaction. Rev Soc Bras Med Trop 2017; 50: 321-328.
36. Sawa T, Kooguchi K, Moriyama K. Molecular diversity of extended-spectrum β-lactamases and carbapenemases, and antimicrobial resistance. J Intensive Care 2020; 8: 13.
37. Jacoby GA, Walsh KE, Mills DM, Walker VJ, Oh H, Robicsek A, et al. qnrB, another plasmid-mediated gene for quinolone resistance. Antimicrob Agents Chemother 2006; 50: 1178-1182.
38. Sarker BR, Ghosh S, Chowdhury S, Dutta A, Chandra Deb L, Krishna Sarker B, et al. Prevalence and antimicrobial susceptibility profiles of non-typhoidal Salmonella isolated from chickens in Rajshahi, Bangladesh. Vet Med Sci 2021; 7: 820-830.
39. Penha Filho RAC, FerreiraI JC, Kanashiro AMI, da Costa Darini AL, JuniorId AB. Antimicrobial susceptibility of Salmonella Gallinarum and Salmonella Pullorum isolated from ill poultry in Brazil. Cienc Rural 2016; 46: 513-518.
40. Folster JP, Rickert R, Barzilay EJ, Whichard JM. Identification of the aminoglycoside resistance determinants armA and rmtC among non-Typhi Salmonella isolates from humans in the United States. Antimicrob Agents Chemother 2009; 53: 4563-4564.
41. Thai TH, Hirai T, Lan NT, Yamaguchi R. Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. Int J Food Microbiol 2012; 156: 147-151.
42. Arslan S, Eyi A. Occurrence and antimicrobial resistance profiles of Salmonella species in retail meat products. J Food Prot 2010; 73: 1613-1617.
43. Putturu R, Thirtham M, Eevuri TR. Antimicrobial sensitivity and resistance of Salmonella enteritidis isolated from natural samples. Vet World 2013; 6: 185-188.
44. Parvej MS, Nazir KH, Rahman MB, Jahan M, Khan MF, Rahman M. Prevalence and characterization of multi-drug resistant Salmonella Enterica serovar Gallinarum biovar Pullorum and Gallinarum from chicken. Vet World 2016; 9: 65-70.
45. Yasmin S, Nawaz M, Ahmad Anjum A, Ashraf K, Ullah N, Mustafa A, et al. Antibiotic susceptibility pattern of Salmonellae isolated from poultry from different Districts of Punjab, Pakistan. Pak Vet J 2020; 40: 98-102.
46. Seo KW, Kim JJ, Mo IP, Lee YJ. Molecular characteristic of antimicrobial resistance of Salmonella Gallinarum isolates from chickens in Korea, 2014 to 2018. Poult Sci 2019; 98: 5416-5423.
47. Castanon JI. History of the use of antibiotic as growth promoters in European poultry feeds. Poult Sci 2007; 86: 2466-2471.
48. Harrell JE, Hahn MM, D'Souza SJ, Vasicek EM, Sandala JL, Gunn JS, et al. Salmonella biofilm formation, chronic infection, and immunity within the intestine and hepatobiliary tract. Front Cell Infect Microbiol 2021; 10: 624622.
2. Foley SL, Johnson TJ, Ricke SC, Nayak R, Danzeisen J. Salmonella pathogenicity and host adaptation in chicken-associated serovars. Microbiol Mol Biol Rev 2013; 77: 582-607.
3. Song L, Tan R, Xiong D, Jiao X, Pan Z. Accurate identification and discrimination of Salmonella enterica serovar Gallinarum biovars Gallinarum and Pullorum by a multiplex PCR based on the new genes of torT and I137_14430. Front Vet Sci 2023; 10: 1220118.
4. Batista DF, de Freitas Neto OC, de Almeida AM, Barrow PA, de Oliveira Barbosa F, Berchieri Junior A. Molecular identification of Salmonella enterica subsp. enterica serovar Gallinarum biovars Gallinarum and Pullorum by a duplex PCR assay. J Vet Diagn Invest 2016; 28: 419-422.
5. Zhou X, Kang X, Zhou K, Yue M. A global dataset for prevalence of Salmonella Gallinarum between 1945 and 2021. Sci Data 2022; 9: 495.
6. Sharma D, Misba L, Khan AU. Antibiotics versus biofilm: an emerging battleground in microbial communities. Antimicrob Resist Infect Control 2019; 8: 76.
7. Lizcano A, Chin T, Sauer K, Tuomanen EI, Orihuela CJ. Early biofilm formation on microtiter plates is not correlated with the invasive disease potential of Streptococcus pneumoniae. Microb Pathog 2010; 48: 124-130.
8. Stepanović S, Cirković I, Ranin L, Svabić-Vlahović M. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol 2004; 38: 428-432.
9. Youn SY, Jeong OM, Choi BK, Jung SC, Kang MS. Comparison of the antimicrobial and sanitizer resistance of Salmonella isolates from chicken Slaughter processes in Korea. J Food Sci 2017; 82: 711-717.
10. Ghasemmahdi H, Tajik H, Moradi M, Mardani K, Modaresi R, Badali A, et al. Antibiotic resistance pattern and biofilm formation ability of clinically isolates of Salmonella enterica serotype typhimurium. Int J Enteric Pathog 2015; 3(2): e27372.
11. Rabsch W, Hargis BM, Tsolis RM, Kingsley RA, Hinz KH, Tschäpe H, et al. Competitive exclusion of Salmonella enteritidis by Salmonella gallinarum in poultry. Emerg Infect Dis 2000; 6: 443-448.
12. Nhung NT, Chansiripornchai N, Carrique-Mas JJ. Antimicrobial resistance in bacterial poultry pathogens: A Review. Front Vet Sci 2017; 4: 126.
13. Cao J, Xu L, Yuan M, Ke B, Xiang D, Ke C, et al. TaqMan probe real-time PCR detection of foodborne Salmonella enterica and its six serovars. Int J Curr Microbiol App Sci 2013; 2: 1-12.
14. Pugliese N, Circella E, Pazzani C, Pupillo A, Camarda A. Validation of a seminested PCR approach for rapid detection of Salmonella enterica subsp. enterica serovar Gallinarum. J Microbiol Methods 2011; 85: 22-27.
15. Zhu C, Yue M, Rankin S, Weill F-X, Frey J, Schifferli DM. One-step identification of five prominent chicken Salmonella serovars and biotypes. J Clin Microbiol 2015; 53: 3881-3883.
16. Batista DF, de Freitas Neto OC, Lopes PD, de Almeida AM, Barrow PA, Berchieri A Jr. Polymerase chain reaction assay based on ratA gene allows differentiation between Salmonella enterica subsp. enterica serovar Gallinarum biovars Gallinarum and Pullorum. J Vet Diagn Invest 2013; 25: 259-262.
17. Zhu Y, Peng L, Chen D, Yu G. Intercalation Pseudocapacitance in Ultrathin VOPO4 nanosheets: toward high-rate Alkali-Ion-based electrochemical energy storage. Nano Lett 2016; 16: 742-747.
18. Batista DFA (2013). Análise comparativa dos genomas de Salmonella enterica subsp. enterica sorovar Gallinarum biovares Gallinarum 287/91 e Pullorum 449/87 para identificação de regiões de diferenças (RODs).
19. Migratory birds wintering in Iran increased by 26.5%, Tehran Times 31 December. Tehran Times, 2018.
20. Poirel L, Walsh TR, Cuvillier V, Nordmann P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis 2011; 70: 119-123.
21. Doyle D, Peirano G, Lascols C, Lloyd T, Church DL, Pitout JD. Laboratory detection of Enterobacteriaceae that produce carbapenemases. J Clin Microbiol 2012; 50: 3877-3880.
22. Du J, Li P, Liu H, Lü D, Liang H, Dou Y. Phenotypic and molecular characterization of multidrug resistant Klebsiella pneumoniae isolated from a university teaching hospital, China. PLoS One 2014; 9(4): e95181.
23. Silagyi K, Kim S-H, Lo YM, Wei C-I. Production of biofilm and quorum sensing by Escherichia coli O157:H7 and its transfer from contact surfaces to meat, poultry, ready-to-eat deli, and produce products. Food Microbiol 2009; 26: 514-519.
24. Stepanovic S, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 2000; 40: 175-179.
25. Saffar H, Asgari Niaraki N, Ghahroudi Tali A, Baseri Z, Abdollahi A, Yalfani R. Prevalence of AmpC β-lactamase in clinical isolates of Escherichia coli, Klebsiella spp., and Proteus mirabilis in a tertiary Hospital in Tehran, Iran. Jundishapur J Microbiol 2016; 9(12): e39121.
26. Turki Y, Mehr I, Ouzari H, Khessairi A, Hassen A. Molecular typing, antibiotic resistance, virulence gene and biofilm formation of different Salmonella enterica serotypes. J Gen Appl Microbiol 2014; 60: 123-130.
27. Davarzani F, Saidi N, Besharati S, Saderi H, Rasooli I, Owlia P. Evaluation of antibiotic resistance pattern, alginate and biofilm production in clinical isolates of Pseudomonas aeruginosa. Iran J Public Health 2021; 50: 341-349.
28. Soria MC, Soria MA, Bueno DJ, Terzolo HR. Comparison of 3 culture methods and PCR assays for Salmonella gallinarum and Salmonella pullorum detection in poultry feed. Poult Sci 2013; 92: 1505-1515.
29. Oliveira SD, Santos LR, Schuch DM, Silva AB, Salle CT, Canal CW. Detection and identification of salmonellas from poultry-related samples by PCR. Vet Microbiol 2002; 87: 25-35.
30. Xiong D, Song L, Pan Z, Jiao X. Identification and discrimination of Salmonella enterica serovar Gallinarum biovars Pullorum and Gallinarum based on a one-step multiplex PCR assay. Front Microbiol 2018; 9: 1718.
31. Kumar A, Balachandran Y, Gupta S, Khare S, Suman. Quick PCR based diagnosis of typhoid using specific genetic markers. Biotechnol Lett 2010; 32: 707-712.
32. Paiva J, Cavallini JS, Silva MD, Almeida MA, Ângela HL, Berchieri Junior A. Molecular differentiation of Salmonella Gallinarum and Salmonella Pullorum by RFLP of fliC gene from Brazilian isolates. Braz J Poult Sci 2009; 11: 271-275.
33. Hur J, Kim JH, Park JH, Lee YJ, Lee J-H. Molecular and virulence characteristics of multi-drug resistant Salmonella Enteritidis strains isolated from poultry. Vet J 2011; 189: 306-311.
34. Kelly BG, Vespermann A, Bolton DJ. Horizontal gene transfer of virulence determinants in selected bacterial foodborne pathogens. Food Chem Toxicol 2009; 47: 969-977.
35. Sedighi M, Halajzadeh M, Ramazanzadeh R, Amirmozafari N, Heidary M, Pirouzi S. Molecular detection of β-lactamase and integron genes in clinical strains of Klebsiella pneumoniae by multiplex polymerase chain reaction. Rev Soc Bras Med Trop 2017; 50: 321-328.
36. Sawa T, Kooguchi K, Moriyama K. Molecular diversity of extended-spectrum β-lactamases and carbapenemases, and antimicrobial resistance. J Intensive Care 2020; 8: 13.
37. Jacoby GA, Walsh KE, Mills DM, Walker VJ, Oh H, Robicsek A, et al. qnrB, another plasmid-mediated gene for quinolone resistance. Antimicrob Agents Chemother 2006; 50: 1178-1182.
38. Sarker BR, Ghosh S, Chowdhury S, Dutta A, Chandra Deb L, Krishna Sarker B, et al. Prevalence and antimicrobial susceptibility profiles of non-typhoidal Salmonella isolated from chickens in Rajshahi, Bangladesh. Vet Med Sci 2021; 7: 820-830.
39. Penha Filho RAC, FerreiraI JC, Kanashiro AMI, da Costa Darini AL, JuniorId AB. Antimicrobial susceptibility of Salmonella Gallinarum and Salmonella Pullorum isolated from ill poultry in Brazil. Cienc Rural 2016; 46: 513-518.
40. Folster JP, Rickert R, Barzilay EJ, Whichard JM. Identification of the aminoglycoside resistance determinants armA and rmtC among non-Typhi Salmonella isolates from humans in the United States. Antimicrob Agents Chemother 2009; 53: 4563-4564.
41. Thai TH, Hirai T, Lan NT, Yamaguchi R. Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. Int J Food Microbiol 2012; 156: 147-151.
42. Arslan S, Eyi A. Occurrence and antimicrobial resistance profiles of Salmonella species in retail meat products. J Food Prot 2010; 73: 1613-1617.
43. Putturu R, Thirtham M, Eevuri TR. Antimicrobial sensitivity and resistance of Salmonella enteritidis isolated from natural samples. Vet World 2013; 6: 185-188.
44. Parvej MS, Nazir KH, Rahman MB, Jahan M, Khan MF, Rahman M. Prevalence and characterization of multi-drug resistant Salmonella Enterica serovar Gallinarum biovar Pullorum and Gallinarum from chicken. Vet World 2016; 9: 65-70.
45. Yasmin S, Nawaz M, Ahmad Anjum A, Ashraf K, Ullah N, Mustafa A, et al. Antibiotic susceptibility pattern of Salmonellae isolated from poultry from different Districts of Punjab, Pakistan. Pak Vet J 2020; 40: 98-102.
46. Seo KW, Kim JJ, Mo IP, Lee YJ. Molecular characteristic of antimicrobial resistance of Salmonella Gallinarum isolates from chickens in Korea, 2014 to 2018. Poult Sci 2019; 98: 5416-5423.
47. Castanon JI. History of the use of antibiotic as growth promoters in European poultry feeds. Poult Sci 2007; 86: 2466-2471.
48. Harrell JE, Hahn MM, D'Souza SJ, Vasicek EM, Sandala JL, Gunn JS, et al. Salmonella biofilm formation, chronic infection, and immunity within the intestine and hepatobiliary tract. Front Cell Infect Microbiol 2021; 10: 624622.
| Files | ||
| Issue | Vol 15 No 5 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i5.13869 | |
| Keywords | ||
| Salmonella; Poultry disease; Antibiotic resistance | ||
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How to Cite
1.
Khaltabadi Farahani R, Ebrahimi-Rad M, Shahrokhi N, Khaltabadi Farahani AH, Ghafouri SA, Rezaei M, Gharibzadeh S, Ghalyanchi Langeroudi A, Ehsani P. High prevalence of antibiotic resistance and biofilm formation in Salmonella Gallinarum. Iran J Microbiol. 2023;15(5):631-641.
