Short Communication
Identification and antimicrobial susceptibility of serovar Choleraesuis in a Salmonella outbreak in central-western Albania
Liljana Lufo * ,
Gjena Dura ,
Andon Çuko ,
Luigj Turmalaj

Mac Vet Rev 2024; 47 (2): 191 - 197

10.2478/macvetrev-2024-0023

Received: 26 February 2024

Received in revised form: 12 August 2024

Accepted: 13 August 2024

Available Online First: 27 August 2024

Published on: 15 October 2024

Correspondence: Liljana Lufo, caraliljana@yahoo.com
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Abstract

Swine paratyphoid infection is caused by the swine-adapted Salmonella enterica serovar Choleraesuis. Infected individuals remain healthy carriers, and if the infection occurs at the end of the fattening period, it could pose a threat to human health. The present work aimed to assess antimicrobial susceptibility of S. enterica serovar Choleraesuis serotypes isolated from domestic pigs in central-western Albania, and to assess the presence and circulation of antibiotic-resistant paratyphoid Salmonella in Albania. Increasing mortality was reported in 6 farrow-to-finish pig farms located in the western and central parts of the country from December 2022 to April 2023. Post-mortem examination revealed macroscopic lesions in different organs indicating Salmonella infection. Four serovars Choleraesuis were isolated out of 24 different Salmonella spp. Multi-drug resistance (MDR), extensively drug-resistant (XDR), and Pan Drug Resistance (PDR) was calculated. Three out of four isolates showed MDR, and one out of four showed XDR. All S. enterica serovar Choleraesuis isolates showed resistance to at least two antimicrobials. Three isolates were observed to display MAR index values >0.2 indicating high-risk contaminated sources with frequent use of antibiotics. The predominant antimicrobial resistance was observed for amoxicillin, oxytetracycline, sulfamethoxazole, trimethoprim, spiramycin, colistin sulpha, and doxycycline. The findings emphasize the importance of strict biosecurity measures in affected pig farms, and prevention and control of S. enterica serovar Choleraesuis in the farm sanitary programs in Albania.

Keywords: paratyphoid, Choleraesuis, antimicrobial resistance, pigs, Salmonella


References

1. Al-Ansari, M.M., Aljubali, M.M., Somily, A.M., Albarrag, A.M., Masood, A. (2021). Isolation and molecular characterization of multidrug-resistant Salmonella enterica serovars. J Infect Public Health. 14(12): 1767-1776. https://doi.org/10.1016/j.jiph.2021.10.011 PMid:34690097
2. Griffith, R.W., Carlson, S.A., Krull, A.C. (2019). Salmonellosis, In J.J. Zimmerman, L.A. Karriker, A. Ramirez, K.J. Schwartz, G.W., Stevenson, J. Zhang (Eds.), Diseases of Swine, 11th ed (pp. 912-925). John Wiley & Sons, Inc https://doi.org/10.1002/9781119350927.ch59 
3. Fedorka-Cray, P.J., Gray, J.T., Wray, C. (2000). Salmonella infections in pigs, In P.A. Barrow, U. Methner (Eds.), Salmonella in domestic animals (pp. 1191-1207). CAB International: Wallingford https://doi.org/10.1079/9780851992617.0191 
4. BfR (The Federal Institute for Risk Assessment). (2016). Salmonella, Listeria and Co.: Old and new challenges for food safety,” 4th Symp. Zoonoses and Food Safety. BfR on findings and strategies to minimize foodborne diseases.
5. Li, H., Wu, Y., Feng, D., Jiang, Q., Li, S., Rong, J., et al. (2024). Centralized industrialization of pork in Europe and America contributes to the global spread of Salmonella enteric. Nat Nature Food 5, 413-422. https://doi.org/10.1038/s43016-024-00968-1 PMid:38724686 PMCid:PMC11132987
6. Kotorri, S., Boci, J., Muhedini, P. (2016). New outbreaks of salmonellosis in pig farms”. Albanian J Agric Sci. 14(2): 192-197.
7. INSTAT. (2021). Statistikat e Blegtorisë, Ministria e Bujqësisë dhe Zhvillimit Rural. c2021 [cited December 20]. https:// www.instat.gov.al
8. Brown, C.C., Baker, D.C., Barker, I.K. (2007). Alimentary system, In M.G. Maxie (Ed.), Jubb, Kennedy and Palmer’s Pathology of Domestic Animals, Vol 2, 5th ed. (pp. 193-199). Toronto: Saunders Elsevier
9. Arruda, B.L., Burrough, E.R., Schwartz, K.J. (2019). Salmonella enterica I 4, [5], 12:i:- associated with lesions typical of swine enteric salmonellosis. Emerg Infect Dis. 2(7): 1377-1379. https://doi.org/10.3201/eid2507.181453 PMid:31211677 PMCid:PMC6590737
10. Li, Y., Teng, L., Xu, X., Li, X., Peng, X., Zhou, X., Du, J., et al. (2022). A nontyphoidal Salmonella serovar domestication accompanying enhanced niche adaptation. EMBO Mol Med. 14(11): e16366. https://doi.org/10.15252/emmm.202216366 PMid:36172999 PMCid:PMC9641423
11. Teng, K.Ty., Aerts, M., Jaspers, S. et al. (2022). Patterns of antimicrobial resistance in Salmonella isolates from fattening pigs in Spain. BMC Vet Res. 18, 333. https://doi.org/10.1186/s12917-022-03377-3 PMid:36057710 PMCid:PMC9440507
12. Ma, F., Xu, S., Tang, Z., Li, Z., Zhang, L. (2021). Use of antimicrobials in food animals and impact of transmission of antimicrobial resistance on humans. Biosaf Health 3(1): 32 38. https://doi.org/10.1016/j.bsheal.2020.09.004
13. Davis, R., Brown, P.D. (2016). Multiple antibiotic resistance index, fitness and virulence potential in respiratory Pseudomonas aeruginosa from Jamaica. J Med Microbiol. 65(4): 261-271. https://doi.org/10.1099/jmm.0.000229 PMid:26860081
14. Nair, D.V.T., Venkitanarayanan, K., Johny, A.K. (2018). Antibiotic-resistant Salmonella in the food supply and the potential role of antibiotic alternatives for control. Foods 7(10): 167. https://doi.org/10.3390/foods7100167 PMid:30314348 PMCid:PMC6210005
15. Collignon, P., Athukorala, P-C., Senanayake, S., Khan, F. (2015). Antimicrobial resistance: the major contribution of poor governance and corruption to this growing problem. PLoS ONE 10(3): e0116746. https://doi.org/10.1371/journal.pone.0116746 PMid:25786027 PMCid:PMC4364737
16. Mthembu, T.P., Zishiri, O.T., El Zowalaty M.E. (2019). Molecular detection of multidrug-resistant Salmonella isolated from livestock production systems in South Africa. Infect Drug Resist. 14(12): 3537-3548. https://doi.org/10.2147/IDR.S211618 PMid:31814742 PMCid:PMC6861519
17. Soliani, L., Rugna, G., Prosperi, A., Chiapponi, C., Luppi, A. (2023). Salmonella infection in pigs: disease, prevalence, and a link between swine and human health. Pathogens 12(10): 1267. https://doi.org/10.3390/pathogens12101267 PMid:37887782 PMCid:PMC10610219
18. Magiorakos, A-P., Srinivasan, A., Carey, R.B., Carmeli, Y., Falagas, M.E., Giske, C.G., Harbarth, S., et al. (2012). Multidrug-resistant, extensively drug-resistant and pan drug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 18(3): 268-281. https://doi.org/10.1111/j.1469-0691.2011.03570.x PMid:21793988
19. Thenmozhi, S., Rajeswari, P., Suresh Kumar, B.T., Saipriyanga, V., Kalpana, M. (2014). Multi-drug resistant patterns of biofilm forming Aeromonas hydrophila from urine samples. Int J Pharm Sci Res. 5(7): 2908-2918.
20. Zhou, Z., Alikhan, N.F., Mohamed, K., Fan, Y., Agama Study Group, Achtman, M. (2020). The EnteroBase user’s guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res. 30(1): 138-152. https://doi.org/10.1101/gr.251678.119 PMid:31809257 PMCid:PMC6961584
21. Tang, B., Elbediwi, M., Nambiar, R.B., Yang, H., Lin, J., Yue, M. (2022). Genomic characterization of antimicrobial-resistant Salmonella enterica in duck, chicken, and pig farms and retail markets in Eastern China. Microbiol Spectr. 10(5): e0125722. https://doi.org/10.1128/spectrum.01257-22 PMid:36047803 PMCid:PMC9603869
22. Liu, Q., Chen, W., Elbediwi, M., Pan, H., Wang, L., Zhou, C., Zhao, B., et al. (2020). Characterization of Salmonella resistome and plasmidome in pork production system in Jiangsu, China. Front Vet Sci. 7, 572392. https://doi.org/10.3389/fvets.2020.00617 PMid:33062654 PMCid:PMC7517575
23. Dominguez, J.E., Redondo, L.M., Figueroa, E.R., Cejas, D., Gutkind, G.O., Chacana, P.A., Di Conza, J.A., Fernandez, M.M. (2018). Simultaneous carriage of mcr-1 and other antimicrobial resistance determinants in Escherichia coli from poultry. Front Microbiol. 9, 1679. https://doi.org/10.3389/fmicb.2018.01679 PMid:30090095 PMCid:PMC6068390
24. McDermott, P.F., Tyson, G.H., Kabera, C., Chen, Y., Li, C., Folster, J.P., et al. (2016). Whole-genome sequencing for detecting antimicrobial resistance in nontyphoidal Salmonella. Antimicrob Agents Chemother. 60(9): 5515-5520. https://doi.org/10.1128/AAC.01030-16 PMid:27381390 PMCid:PMC4997858


Copyright

© 2024 Lufo L. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Conflict of Interest Statement

The authors declared that they have no potential lict of interest with respect to the authorship and/or publication of this article.

Citation Information

Macedonian Veterinary Review. Volume 47, Issue 2, Pages 191-197, e-ISSN 1857-7415, p-ISSN 1409-7621, DOI: 10.2478/macvetrev-2024-0023