A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance

Saleh Mohammed Jajere

doi:10.14202/vetworld.2019.504-521

journal article Open Access Apr 01, 2019

A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance

Saleh Mohammed Jajere

Veterinary World Vol. 12 No. 4 pp. 504-521 · Veterinary World

View at Publisher Save 10.14202/vetworld.2019.504-521

Abstract

Salmonella genus represents the most common foodborne pathogens frequently isolated from food-producing animals that is responsible for zoonotic infections in humans and animal species including birds. Thus, Salmonella infections represent a major concern to public health, animals, and food industry worldwide. Salmonella enterica represents the most pathogenic specie and includes >2600 serovars characterized thus far. Salmonella can be transmitted to humans along the farm-to-fork continuum, commonly through contaminated foods of animal origin, namely poultry and poultry-related products (eggs), pork, fish etc. Some Salmonella serovars are restricted to one specific host commonly referred to as "host-restricted" whereas others have broad host spectrum known as "host-adapted" serovars. For Salmonella to colonize its hosts through invading, attaching, and bypassing the host's intestinal defense mechanisms such as the gastric acid, many virulence markers and determinants have been demonstrated to play crucial role in its pathogenesis; and these factors included flagella, capsule, plasmids, adhesion systems, and type 3 secretion systems encoded on the Salmonella pathogenicity island (SPI)-1 and SPI- 2, and other SPIs. The epidemiologically important non-typhoidal Salmonella (NTS) serovars linked with a high burden of foodborne Salmonella outbreaks in humans worldwide included Typhimurium, Enteritidis, Heidelberg, and Newport. The increased number of NTS cases reported through surveillance in recent years from the United States, Europe and low- and middle-income countries of the world suggested that the control programs targeted at reducing the contamination of food animals along the food chain have largely not been successful. Furthermore, the emergence of several clones of Salmonella resistant to multiple antimicrobials worldwide underscores a significant food safety hazard. In this review, we discussed on the historical background, nomenclature and taxonomy, morphological features, physical and biochemical characteristics of NTS with a particular focus on the pathogenicity and virulence factors, host specificity, transmission, and antimicrobial resistance including multidrug resistance and its surveillance.

Topics

No keywords indexed for this article. Browse by subject →

References

186

[1]

Lee, K.M., Runyon, M., Herrmanm, T.J., Phillips, R. and Hsieh, J. (2015) Review of Salmonella detection and identification methods: Aspects of rapid emergency response and food safety. Food Control, 47(2015): 264-276. 10.1016/j.foodcont.2014.07.011

[2]

Newell, D.G., Koopmans, M., Verhoef, L., Duizer, E., Aidara-Kane, A., Sprong, H., Opsteegh, M., Langelaar, M., Threfall, J., Scheutz, F., van der Giessen, J. and Kruse, H. (2010) Food-borne diseases the challenges of 20 years ago still persist while new ones continue to emerge. Int. J. Food Microbiol., 139(1): S3-S15. 10.1016/j.ijfoodmicro.2010.01.021

[3]

Putturu, R., Eevuri, T., Ch, B. and Nelapati, K. (2015) Salmonella enteritidis-foodborne pathogen-a review. Int. J. Pharm Biol. Sci., 5(1): 86-95.

[4]

Alzwghaibi, A.B., Yahyaraeyat, R., Fasaei, B.N., Langeroudi, A.G. and Salehi, T.Z. (2018) Rapid molecular identification and differentiation of common Salmonella serovars isolated from poultry, domestic animals and foodstuff using multiplex PCR assay. Arch. Microbiol., 200(7): 1009-1016. 10.1007/s00203-018-1501-7

[5]

Eguale, T. (2018) Non-typhoidal Salmonella serovars in poultry farms in central Ethiopia: Prevalence and antimicrobial resistance BMC Vet. Res., 14(1): 217. 10.1186/s12917-018-1539-4

[6]

Zishiri, O.T., Mkhize, N. and Mukaratirwa, S. (2016) Prevalence of virulence and antimicrobial resistance genes in Salmonella spp. isolated from commercial chickens and human clinical isolates from South Africa and Brazil. Onderstepoort J. Vet. Res., 83(1): e1-e11 10.4102/ojvr.v83i1.1067

[7]

Velasquez, C.G., MacKlin, K.S., Kumar, S., Bailey, M., Ebner, P.E., Oliver, H.F., Martin-Gonzalez, F.S. and Singh, M. (2018) Prevalence and antimicrobial resistance patterns of Salmonella isolated from poultry farms in Southeastern United States. Poult. Sci., 97(6): 2144-2152. 10.3382/ps/pex449

[8]

Ed-dra, A., Filali, F.R., Karraouan, B., El Allaoui, A., Aboulkacem, A. and Bouchrif, B. (2017) Prevalence, molecular and antimicrobial resistance of Salmonella isolated from sausages in Meknes, Morocco. Microb. Pathog., 105: 340-345. 10.1016/j.micpath.2017.02.042

[9]

Odoch, T., Wasteson, Y., L’Abée-Lund, T., Muwonge, A., Kankya, C., Nyakarahuka, L., Tegule, S. and Skjerve, E. (2017) Prevalence, antimicrobial susceptibility and risk factors associated with non-typhoidal Salmonella on Ugandan layer hen farms. BMC Vet. Res., 13(1): 365. 10.1186/s12917-017-1291-1

[10]

Mezal, E.H., Sabol, A., Khan, M.A., Ali, N., Stefanova, R. and Khan, A.A. (2014) Isolation and molecular characterization of Salmonella enterica serovar Enteritidis from poultry house and clinical samples during 2010. Food Microbiol., 38: 67-74. 10.1016/j.fm.2013.08.003

[11]

Xiong, D., Song, L., Pan, Z. and Jiao, X. (2018) Identification and discrimination of Salmonella enterica serovar Gallinarum biovars Pullorum and Gallinarum based on a one-step multiplex PCR assay. Front. Microbiol., 9: 1718. 10.3389/fmicb.2018.01718

[12]

Penha Filho, R.A.C., Ferreira, J.C., Kanashiro, A.M.I., Darini, A.L.C. and Berchieri, J.A. (2016) Antimicrobial susceptibility of Salmonella gallinarum and Salmonella Pullorum isolated from ill poultry in Brazil. Ciência Rural, 46(3): 513-518. 10.1590/0103-8478cr20150398

[13]

Eriksson, H., Söderlund, R., Ernholm, L., Melin, L. and Jansson, D.S. (2018) Diagnostics, epidemiological observations and genomic subtyping in an outbreak of pullorum disease in non-commercial chickens. Vet. Microbiol., 217: 47-52. 10.1016/j.vetmic.2018.02.025

[14]

Yue, M. and Schifferli, D.M. (2013) Allelic variation in Salmonella: An underappreciated driver of adaptation and virulence. Front. Microbiol., 4: 419. 10.3389/fmicb.2013.00419

[15]

Niki, M., Shakeel, A., Zahid, K. and Konstantinos, C.K (2017) Prevalence, Risks and Antibiotic Resistance of Salmonella in Poultry Production Chain. In: Current Topics in Salmonella and Salmonellosis. InTechOpen, London, United Kingdom p216-234. 10.5772/67438

[16]

Elkenany, R.M., Eladl, A.H. and El-Shafei, R.A. (2018) Genetic characterization of class 1 integrons among multidrug-resistant Salmonella serotypes in broiler chicken farms. J. Glob. Antimicrob. Resist., 14: 202-208. 10.1016/j.jgar.2018.04.009

[17]

Liljebjelke, K.A., Hofacre, C.L., White, D.G., Ayers, S., Lee, M.D. and Maurer, J.J. (2017) Diversity of antimicrobial resistance phenotypes in Salmonella isolated from commercial poultry farms. Front. Vet. Sci., 4: 96. 10.3389/fvets.2017.00096

[18]

Iwamoto, M., Reynolds, J., Karp, B.E., Tate, H., Fedorka-Cray, P.J., Plumblee, J.R., Hoekstra, R.M., Whichard, J.M. and Mahon, B.E. (2017) Ceftriaxone-resistant nontyphoidal Salmonella from humans, retail meats, and food animals in the United States, 1996-2013. Foodborne Pathog. Dis., 14(2): 74-83. 10.1089/fpd.2016.2180

[19]

Faruq, A.A., Hassan, M.M., Uddin, M.M., Rahman, M.L., Rakib, T.M., Alam, M. and Islam, A. (2016) Prevalence and multidrug resistance pattern of Salmonella isolated from resident wild birds of Bangladesh. Int. J. One Health, 2: 35-41. 10.14202/ijoh.2016.35-41

[20]

Omoshaba, E.O., Olufemi, F.O., Ojo, O.E., Sonibare, A.O. and Agbaje, M. (2017) Multidrug-resistant Salmonellae isolated in Japanese quails reared in Abeokuta, Nigeria. Trop. Anim. Health Prod., 49(7): 1455-1460. 10.1007/s11250-017-1347-z

[21]

Migura-Garcia, L., Ramos, R. and Cerdà-Cuéllar, M. (2017) Antimicrobial resistance of Salmonella serovars and Campylobacter spp. Isolated from an opportunistic gull species, yellow-legged gull ( Larus michahellis). J. Wildl. Dis., 53(1): 148-152. 10.7589/2016-03-051

[22]

Anjum, M.F., Duggett, N.A., AbuOun, M., Randall, L., Nunez-Garcia, J., Ellis, R.J., Rogers, J., Horton, R., Brena, C., Williamson, S., Martelli, F., Davies, R. and Teale, C. (2016) Colistin resistance in Salmonella and Escherichia coli isolates from a pig farm in Great Britain. J. Antimicrob. Chemother., 71(8): 2306-2313. 10.1093/jac/dkw149

[23]

Phoon, Y.W., Chan, Y.Y.C. and Koh, T.H. (2015) Isolation of multidrug-resistant Salmonella in Singapore. Singapore Med. J., 56(8): 142-144. 10.11622/smedj.2015129

[24]

Andoh, L.A., Ahmed, S., Olsen, J.E., Obiri-Danso, K., Newman, M.J., Opintan, J.A., Barco, L. and Dalsgaard, A. (2017) Prevalence and characterization of Salmonella among humans in Ghana. Trop. Med. Health, 45: 3. 10.1186/s41182-017-0043-z

[25]

Afema, J.A., Mather, A.E. and Sischo, W.M. (2015) Antimicrobial resistance profiles diversity in Salmonella from humans cattle, 2004-2011. Zoonoses Public Health, 62(7): 506-517. 10.1111/zph.12172

[26]

Brands, D.A., Inman, A.E., Gerba, C.P., Maré, C.J., Billington, S.J., Saif, L.A., Levine, J.F. and Joens, L.A. (2005) Prevalence of Salmonella spp. In oysters in the United States. Appl. Environ. Microbiol., 71(2): 893-897. 10.1128/aem.71.2.893-897.2005

[27]

Chao, G., Zhou, X., Jiao, X., Qian, X. and Xu, L. (2007) Prevalence and antimicrobial resistance of foodborne pathogens isolated from food products in China. Foodborne Pathog. Dis., 4(3): 277-284. 10.1089/fpd.2007.0088

[28]

Gebreyes, W.A. and Thakur, S. (2005) Multidrug-resistant Salmonella enterica serovar Muenchen from pigs and humans and potential interserovar transfer of antimicrobial resistance. Antimicrob. Agents Chemother., 49(2): 503-511. 10.1128/aac.49.2.503-511.2005

[29]

Glenn, L.M., Lindsey, R.L., Folster, J.P., Pecic, G., Boerlin, P., Gilmour, M.W., Harbottle, H., Zhao, S., McDermott, P.F. and Fedorka-Cray, P.J. (2013) Antimicrobial resistance genes in multidrug-resistant Salmonella enterica isolated from animals, retail meats, and humans in the United States and Canada. Microb. Drug Resist., 19(3): 175-184. 10.1089/mdr.2012.0177

[30]

Voss-Rech, D., Potter, L., Vaz, C.S.L., Pereira, D.I.B., Sangioni, L.A., Vargas, Á.C. and de Avila, B.S. (2017) Antimicrobial resistance in nontyphoidal Salmonella isolated from human and poultry-related samples in Brazil: 20-year meta-analysis. Foodborne Pathog. Dis., 14(2): 116-124. 10.1089/fpd.2016.2228

[31]

Michael, G.B. and Schwarz, S. (2016) Antimicrobial resistance in zoonotic nontyphoidal Salmonella: An alarming trend? Clin. Microbiol. Infect., 22(12): 968-974 10.1016/j.cmi.2016.07.033

[32]

Shrestha, K.L., Pant, N.D., Bhandari, R., Khatri, S., Shrestha, B. and Lekhak, B. (2016) Re-emergence of the susceptibility of the Salmonella spp. Isolated from blood samples to conventional first-line antibiotics. Antimicrob. Resist. Infect. Control,. 5(2016): 22. 10.1186/s13756-016-0121-8

[33]

Angelo, K.M., Reynolds, J., Karp, B.E., Hoekstra, R.M., Scheel, C.M. and Friedman C. (2016) Antimicrobial resistance among nontyphoidal Salmonella isolated from blood in the United States, 2003-2013. J. Infect. Dis., 214(10): 1565-1570. 10.1093/infdis/jiw415

[34]

Majowicz, S.E., Musto, J., Scallan, E., Angulo, F.J., Kirk, M., O’Brien, S.J., Jones, T.F., Fazil, A. and Hoekstra, R.M (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis., 50(6): 882-889. 10.1086/650733

[35]

Antimicrobial resistance: a global multifaceted phenomenon

Francesca Prestinaci, Patrizio Pezzotti, Annalisa Pantosti

Pathogens and Global Health 10.1179/2047773215y.0000000030

[36]

Li, B., Liu, C., Liu, L., Li, S., Fan, N., Hou, H., Jin, J. and Xing, Y. (2018) Prevalence and etiologic agent of Salmonella in livestock and poultry meats in Huai’an City during 2015-2016. Wei Sheng Yan Jiu, 47(2): 260-300.

[37]

Adhikari, S.K., Gyawali, A., Shrestha, S., Shrestha, S.P., Prajapati, M. and Raj, D. (2018) Molecular confirmation of Salmonella Typhimurium in poultry from Kathmandu valley. J. Nepal Agric. Res. Counc., 4(1): 86-89. 10.3126/jnarc.v4i1.19694

[38]

Shah, D.H., Paul, N.C., Sischo, W.C., Crespo, R. and Guard, J (2017) Microbiology and food safety: Population dynamics and antimicrobial resistance of the most prevalent poultry-associated Salmonella serotypes. Poult. Sci., 96(3): 687-702. 10.3382/ps/pew342

[39]

Tarabees, R., Elsayed, M.S.A., Shawish, R., Basiouni, S. and Shehata, A.A. (2017) Isolation and characterization of Salmonella Enteritidis and Salmonella Typhimurium from chicken meat in Egypt. J. Infect. Dev. Ctries., 11(4): 314-319. 10.3855/jidc.8043

[40]

Fagbamila, I.O., Barco, L., Mancin, M, Abdu, P.A., Kabir, J., Umoh, J., Ricci, A. and Muhammad, M. (2017) Salmonella serovars and their distribution in Nigerian commercial chicken layer farms. PLoS One, 12(3): e0173097. 10.1371/journal.pone.0173097

[41]

Krawiec, M., Kuczkowski, M., Kruszewicz, A.G. and Wieliczko, A. (2015) Prevalence and genetic characteristics of Salmonella in free-living birds in Poland. BMC Vet. Res., 11: 15. 10.1186/s12917-015-0332-x

[42]

Myšková, P. and Íšková, R.K. (2017) Prevalence and characteristics of Salmonella in retail poultry and pork meat in the Czech Republic in 2013-2014. Czech J. Food Sci., 35(2): 106-112. 10.17221/260/2016-cjfs

[43]

Rönnqvist, M., Välttilä, V., Ranta, J. and Tuominen, P. (2018) Salmonella risk to consumers via pork is related to the Salmonella prevalence in pig feed. Food Microbiol., 71(2018): 93-97. 10.1016/j.fm.2017.03.017

[44]

Cummings, K.J., Rodriguez-Rivera, L.D., Grigar, M.K., Rankin, S.C., Mesenbrink, B.T., Leland, B.R. and Bodenchuk, M.J. (2016) Prevalence and characterization of Salmonella isolated from feral pigs throughout Texas. Zoonoses Public Health, 63(6): 436-441. 10.1111/zph.12244

[45]

Afema, J.A. and Sischo, W.M. (2016) Salmonella in wild birds utilizing protected and human-impacted habitats, Uganda. Ecohealth, 13(3): 558-569. 10.1007/s10393-016-1149-1

[46]

Mustaffa, S.S., Saleha, A.A. and Jalila, A. (2014) Occurrence of antibiotic-resistant Salmonella and Campylobacter in wild birds. J. Vet. Malaysia, 26(2): 17-19.

[47]

Botti, V., Valérie, N.F., Domenis, L., Orusa, R., Pepe, E., Robetto, S. and Guidetti, C (2013) Salmonella spp. And antibiotic-resistant strains in wild mammals and birds in North-Western Italy from 2002 to 2010. Vet. Ital., 49(2): 195-202.

[48]

Grigar, M.K., Cummings, K.J., Rodriguez-Rivera, L.D., Rankin, S.C., Johns, K., Hamer, G.L. and Hamer, S.A. (2016) Salmonella surveillance among great-tailed grackles (Quiscalus mexicanus) and other urban bird species in eastern Texas. Vector-Borne Zoonotic Dis., 16(12): 752-757. 10.1089/vbz.2016.2000

[49]

Lawson, B., De Pinna, E., Horton, R.A, Macgregor, S.K., John, S.K., Chantrey, J., Duff, J.P. and Kirkwood, J.K. (2014) Epidemiological evidence that garden birds are a source of human salmonellosis in England and Wales. PLoS One, 9(2): e88968. 10.1371/journal.pone.0088968

[50]

Matias, C.A.R., Pereira, I.A., Reis, E.M.F., Rodrigues, D.P. and Siciliano, S. (2016) Frequency of zoonotic bacteria among illegally traded wild birds in Rio de Janeiro. Braz. J Microbiol., 47(4): 882-888. 10.1016/j.bjm.2016.07.012

Showing 50 of 186 references

Cited By

463

Comparative genomic profiling of virulence genes in human clinical isolates of Salmonella enterica serovars Typhimurium and Enteritidis

Hamid Reza Sodagari, Ihab Habib · 2025

Frontiers in Cellular and Infection...

Integrating serotyping, MLST, and phenotypic data: decoding the evolutionary drivers of Salmonella pathogenicity and drug resistance

Wanting Hong, Zheng Yang · 2025

Applied and Environmental Microbiol...

Prevalence and Antimicrobial Resistance of Salmonella Strains Isolated from Chicken Samples in Southern Italy

Pietro Di Taranto, Fiorenza Petruzzi · 2025

Microorganisms

Salmonella in the environment: A review on ecology, antimicrobial resistance, seafood contaminations, and human health implications

Mohammad Maruf Billah, Md Saydur Rahman · 2024

Journal of Hazardous Materials Adva...

Antibacterial effect of curcumin on Salmonella Typhimurium: In vitro and food model studies

G Terzi Gulel, S Kanat · 2024

Veterinární medicína

Defense mechanisms of Salmonella against antibiotics: a review

Anuradha Jeewantha Punchihewage-Don, Priyanka Nilmini Ranaweera · 2024

Frontiers in Antibiotics

Multiplex PCR-based genotyping of Salmonella Enteritidis and Salmonella Typhimurium from food sources and assessment of their antimicrobial resistance profiles in Egypt

Deng Barac, Ahmed Abdel-Mawgood · 2024

Molecular Biology Reports

Novel Lactobacillaceae strains and consortia to produce propionate‐containing fermentates as biopreservatives

Ena Buljubašić, Maria Florencia Bambace · 2024

Microbial Biotechnology

Prevalence and Antimicrobial Resistance Profile of Salmonella Isolated from Human, Animal and Environment Samples in South Asia: A 10-Year Meta-analysis

Himel Talukder, Shamsul Alam Roky · 2023

Journal of Epidemiology and Global...

Genomic and Evolutionary Analysis of Salmonella enterica Serovar Kentucky Sequence Type 198 Isolated From Livestock In East Africa

Mauro de Mesquita Sousa Saraiva, Valdinete Pereira Benevides · 2022

Frontiers in Cellular and Infection...

Determination of the Salmonella intracellular lifestyle by the diversified interaction of Type III secretion system effectors and host GTPases

Kun Meng, Ping Zhu · 2022

WIREs Mechanisms of Disease

Repurposing of FDA approved drugs and their validation against potential drug targets for Salmonella enterica through molecular dynamics simulation

Akanksha Kesharwani, Dheeraj Kumar Chaurasia · 2021

Journal of Biomolecular Structure a...

Detection of mobile genetic elements associated with antibiotic resistance in Salmonella enterica using a newly developed web tool: MobileElementFinder

Markus H K Johansson, Valeria Bortolaia · 2020

Journal of Antimicrobial Chemothera...

Metrics

463

Citations

186

References

Details

Published: Apr 01, 2019
Vol/Issue: 12(4)
Pages: 504-521
License: View

Authors

S

Saleh Mohammed Jajere

Department of Veterinary Public Health and Preventive Medicine, Faculty of Veterinary Medicine, University of Maiduguri, PMB 1069, Maiduguri, Borno State, Nigeria.

Cite This Article

Saleh Mohammed Jajere (2019). A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. Veterinary World, 12(4), 504-521. https://doi.org/10.14202/vetworld.2019.504-521

A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance

You May Also Like