Abstract
The global rise in seafood consumption has increased the incidence of aquatic food-associated bacterial infections, with Salmonella spp. being of great concern. While numerous Salmonella serotypes exist, Salmonella enterica serovar Typhimurium and Salmonella enterica serovar Enteritidis have garnered significant attention as foodborne pathogens. The pathogenicity of Salmonella is attributed to its ability to express a wide array of virulence factors. These factors aid Salmonella's colonization, invasion, and survival in aquatic environments and the human gastrointestinal tracts. In addition, the emergence of antimicrobial resistance in Salmonella strains isolated from aquatic food is a significant challenge for the seafood industry. Given the increasing evidence of Salmonella's prevalence, virulence, and antimicrobial resistance isolated from various types of aquatic food, it is crucial to address this issue to safeguard public health. Comprehensive surveillance programs, implementation of good aquaculture and hygiene practices, and adherence to strict food safety regulations are essential in preventing and controlling Salmonella contamination in aquatic food. This review emphasized the occurrence, virulence, and antimicrobial resistance observed in Salmonella strains obtained from different varieties of aquatic food products.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data sharing does not apply to this article as no new data were created or analyzed in this study.
References
Agmas B, Gelaw G, Adugna M, Teshome Y (2022) Occurrence, Associated Risk Factors and Drug Resistance Profiles of Salmonella Isolated from Fish Value Chain, Northwest Ethiopia. Ethiop J Agric Sci 32:79–88
Aissa RB, Al-Gallas N, Troudi H, Belhadj N, Belhadj A (2007) Trends in Salmonella enterica serotypes isolated from human, food, animal, and environment in Tunisia, 1994–2004. J Infect 55:324–339. https://doi.org/10.1016/j.**f.2007.06.007
Akiyama T, Khan AA, Cheng CM, Stefanova R (2011) Molecular characterization of Salmonella enterica serovar Saintpaul isolated from imported seafood, pepper, environmental and clinical samples. Food Microbiol 28:1124–1128. https://doi.org/10.1016/j.fm.2011.03.003
Allam SA, Mostafa NY, Kirrella GAK, Eleiwa NZ, El-Magd MA (2019) Molecular detection of invA and hilA virulent genes in salmonella serovars isolated from fresh water fish. Slov Vet Res 56:693–698
Amagliani G, Brandi G, Schiavano GF (2012) Incidence and role of Salmonella in seafood safety. Food Res Int 45:780–788. https://doi.org/10.1016/j.foodres.2011.06.022
Antunes P, Machado J, Peixe L (2006) Characterization of antimicrobial resistance and class 1 and 2 integrons in Salmonella enterica isolates from different sources in Portugal. J Antimicrob Chemother 58:297–304. https://doi.org/10.1093/jac/dkl242
Ashton PM, Nair S, Peters TM, Bale JA, Powell DG, Painset A, Tewolde R, Schaefer U, Jenkins C, Dallman TJ, de Pinna EM (2016) Identification of Salmonella for public health surveillance using whole genome sequencing. PeerJ 4:1–18. https://doi.org/10.7717/peerj.1752
Bang IS, Frye JG, McClelland M, Velayudhan J, Fang FC (2005) Alternative sigma factor interactions in Salmonella: σE and σH promote antioxidant defences by enhancing σS levels. Mol Microbiol 56:811–823. https://doi.org/10.1111/j.1365-2958.2005.04580.x
Bangtrakulnonth A, Pornreongwong S, Pulsrikarn C, Sawanpanyalert P, Hendriksen RS, Wong D, Fo ML, Aarestrup FM (2004) Salmonella serovars from humans and other sources in Thailand, 1993–2002. Emerg Infect Dis 10:131–136
Beshiru A, Igbinosa IH, Igbinosa EO (2019) Prevalence of antimicrobial resistance and virulence gene elements of Salmonella serovars from ready-to-eat (RTE) shrimps. Front Microbiol 10:1–11. https://doi.org/10.3389/fmicb.2019.01613
Bhowmick PP, Devegowda D, Karunasagar I (2011a) Viruloty** of seafood associated Salmonella enterica subsp. enterica isolated from Southwest coast of India. Res Artic Biotechnol Bioinf Bioeng 1:63–69
Bhowmick PP, Devegowda D, Ruwandeepika HAD, Karunasagar I, Karunasagar I (2011b) Presence of Salmonella pathogenicity island 2 genes in seafood-associated Salmonella serovars and the role of the sseC gene in survival of Salmonella enterica serovar Weltevreden in epithelial cells. Microbiology 157:160–168. https://doi.org/10.1099/mic.0.043596-0
Blanc-Potard AB (1997) Groisman EA (1997) The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 16:5376–5385. https://doi.org/10.1093/emboj/16.17.5376
Bouchrif B, Paglietti B, Murgia M, Piana A, Cohen N, Ennaji MM, Rubino S, Timinouni M (2009) Prevalence and antibiotic-resistance of Salmonella isolated from food in Morocco. J Infect Dev Ctries 3:35–40. https://doi.org/10.3855/jidc.103
Boutaib R, Bouchrif B, Abid M, Karraouan B, Khaddor M (2015) Multidrug Resistance of Salmonella Isolated from Shellfish Samples, Morocco. Br Microbiol Res J 8:663–669. https://doi.org/10.9734/BMRJ/2015/18501
Bradford MA, Humphrey TJ, Lappin-Scott HM (1997) The cross-contamination and survival of Salmonella enteritidis PT4 on sterile and non-sterile foodstuffs. Lett Appl Microbiol 24:261–264. https://doi.org/10.1046/j.1472-765X.1997.00127.x
BRASIL. Ministério da Saúde. Secretaria de Vigilância em Saúde (2011) Manual técnico de diagnóstico laboratorial de Salmonella spp.: diagnóstico laboratorial do gênero Salmonella / Ministério da Saúde. Secretaria de Vigilância em Saúde, Fundação Oswaldo Cruz. Laboratório de Referência Nacional de Enteroinfecções Bacterianas, Instituto Adolfo Lutz. - Brasília. Available from: https://www.gov.br/saude/pt-br/centrais-deconteudo/publicacoes/svsa/doencas-diarreicas-agudas/manual-tecnico-de-diagnostico-laboratorial-das-salmonellaspp.pdf/view. Accessed 2 Nov 2023
Broughton EI, Walker DG (2009) Prevalence of antibiotic-resistant Salmonella in fish in Guangdong, China. Foodborne Pathog Dis 6:519–521. https://doi.org/10.1089/fpd.2008.0196
Budiati T, Rusul G, Wan-Abdullah WN, Arip YM, Ahmad R, Thong KL (2013) Prevalence, antibiotic resistance and plasmid profiling of Salmonella in catfish (Clarias gariepinus) and tilapia (Tilapia mossambica) obtained from wet markets and ponds in Malaysia. Aquaculture 372–375:127–132. https://doi.org/10.1016/j.aquaculture.2012.11.003
Busani L, Graziani C, Battisti A, Franco A, Ricci A, Vio D, Digiannatale E, Paterlini F, d’Incau M, Owczarek S, Caprioli A (2004) Antibiotic resistance in Salmonella enterica serotypes Typhimurium, Enteritidis and Infantis from human infections, foodstuffs and farm animals in Italy. Epidemiol Infect 132:245–251. https://doi.org/10.1017/S0950268803001936
CDC Centers for Disease Control and Prevention (2008). Outbreak of Salmonella serotype Saintpaul infections associated with multiple raw produce items in United States. MMWR 57, 929e934. Available from https://www.cdc.gov/mmwr/preview/mmwrhtml/mm5734a1.htm. Accessed 2 Nov 2023
CDC Centers for Disease Control and Prevention (2009). Outbreak of Salmonella serotype Saintpaul infections associated with eating alfalfa sprouts United States. MMWR 58, 1e3. Available from https://www.cdc.gov/mmwr/preview/mmwrhtml/mm5818a4.htm. Accessed 2 Nov 2023
CDC Centers for Disease Control and Prevention (2014) Antibiotic resistance in foodborne germs is an ongoing threat. Available from https://www.cdc.gov/salmonella/heidelberg-10-13/index.html. Accessed 2 Nov 2023
CDC Centers for Disease Control and Prevention (2021) Salmonella outbreak linked to seafood. Available from https://www.cdc.gov/foodcore/successes/colorado-stops-outbreak.html. Accessed 2 Nov 2023
CDC Centers for Disease Control and Prevention (2023), National Center for Emerging and Zoonotic Infectious Diseases (NCEZID), Division of Foodborne, Waterborne, and Environmental Diseases (DFWED) Available from https://www.cdc.gov/salmonella. Accessed 2 Nov 2023
Chakravortty D, Hansen-Wester I, Hensel M (2002) Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J Exp Med 195:1155–1166. https://doi.org/10.1084/jem.20011547
Chamberlain JS, Gibbs RA, Rainer JE, Nguyen PN, Thomas C (1988) Deletion screening of the Duchenne muscular dystrophy locus via multiplex DNA amplification. Nucleic Acids Res 16:11141–11156. https://doi.org/10.1093/nar/16.23.11141
Clavijo RI, Loui C, Andersen GL, Riley LW, Lu S (2006) Identification of genes associated with survival of Salmonella enterica serovar Enteritidis in chicken egg albumen. Appl Environ Microbiol 72:1055–1064. https://doi.org/10.1128/AEM.72.2.1055-1064.2006
Clegg S, Gerlach GF (1987) Enterobacterial fimbriae. J Bacteriol 169:934–938
Connell SR, Trieber CA, Dinos GP, Einfeldt E, Taylor DE, Nierhaus KH (2003) Mechanism of Tet (O)-mediated tetracycline resistance. EMBO J 22:945–953. https://doi.org/10.1093/emboj/cdg093
Cunha-Neto A, Panzenhagen P, Carvalho L, Rodrigues D, Conte-Júnior C, Figueiredo E (2019) Occurrence and antimicrobial resistance profile of Salmonella isolated from native fish slaughtered and commercialized in Brazil. J Food Saf Food Qual 70:94–98. https://doi.org/10.2376/0003-925X-70-94
da Silveira CS, de Sousa OV, Evangelista-Barreto NS (2016) Propagation of antimicrobial resistant Salmonella Spp. in bivalve mollusks from estuary areas of Bahia. Brazil Rev Caatinga 29:450–457. https://doi.org/10.1590/1983-21252016v29n222rc
Das PK, Mandal A, Rahman MM, Sarkar SL, Jahid IK, Hossain MA, Alam AS, Roy PC (2022) Salmonella enterica Serovar Typhimurium and Enteritidis Isolated from Raw Shrimp in Bangladesh: An Investigation Based on Molecular Characteristics, Survival, Virulence, Antibiotic Resistance, and Biofilm Formation Attributes. J Food Qual. https://doi.org/10.1155/2022/3420364
David OM, Wandili S, Kakai R, Waindi EN (2009) Isolation of Salmonella and Shigella from fish harvested from the Winam Gulf of Lake Victoria, Kenya. J Inf Dev Ctries 3:099–104. https://doi.org/10.3855/jidc.56
De Boer E, Hahne M (1990) Cross contamination with Campylobacter jejuni and Salmonella spp. from raw chicken products during food preparation. J Food Prot 53:1067–1068. https://doi.org/10.4315/0362-028X-53.12.1067
Deekshit VK, Kumar BK, Rai P, Srikumar S, Karunasagar I, Karunasagar I (2012) Detection of class 1 integrons in Salmonella Weltevreden and silent antibiotic resistance genes in some seafood-associated nontyphoidal isolates of Salmonella in south-west coast of India. J Appl Microbiol 112:1113–1122. https://doi.org/10.1111/j.1365-2672.2012.05290.x
Deekshit VK, Kumar BK, Rai P, Rohit A, Karunasagar I (2013) Simultaneous detection of Salmonella pathogenicity island 2 and its antibiotic resistance genes from seafood. J Microbiol Methods 93:233–238. https://doi.org/10.1016/j.mimet.2013.03.015
Deekshit VK, Kumar BK, Rai P, Karunasagar I (2015) Differential expression of virulence genes and role of gyrA mutations in quinolone resistant and susceptible strains of Salmonella Weltevreden and Newport isolated from seafood. J Appl Microbiol 119:970–980. https://doi.org/10.1111/jam.12924
Deekshit VK, Kumar BK, Rai P, Karunasagar I (2016) Antibiotic resistance and molecular characterization of seafood isolates of nontyphoidal Salmonella by PFGE. Proc Food Sci 6:334–338. https://doi.org/10.1016/j.profoo.2016.02.067
Deng X, Ran L, Wu S, Ke B, He D, Yang X, Zhang Y, Ke C, Klena JD, Yan M, Feng Z (2012) Laboratory-based surveillance of non-typhoidal Salmonella infections in Guangdong Province, China. Foodborne Pathog Dis 9:305–312. https://doi.org/10.1089/fpd.2011.1008
Dib AL, Agabou A, Chahed A, Kurekci C, Moreno E, Espigares M, Espigares E (2018) Isolation, molecular characterization and antimicrobial resistance of enterobacteriaceae isolated from fish and seafood. Food Control 88:54–60. https://doi.org/10.1016/j.foodcont.2018.01.005
Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193. https://doi.org/10.1128/cmr.15.2.167-193.2002
Doublet B, Lailler R, Meunier D, Brisabois A, Boyd D, Mulvey MR, Chaslus-Dancla E, Cloeckaert (2003) Variant Salmonella genomic island 1 antibiotic resistance gene cluster in Salmonella enterica serovar Albany. Emerg Infect Dis 9:585–591
EFSA, European Food Safety Authority (2010) The community summary report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks in the European Union in 2008. EFSA J 8:1496
Ekpo U, Umana S, Essien J, Bassey M, Uko M, Abiaobo N (2017) Virulence Factors And Antibiogram Of Bacteria From Fresh Aquatic Produce From Open Air Market Centre In Okepedi, Itu, Akwa Ibom State. J Appl Life Sci Int 14:1–8. https://doi.org/10.9734/JALSI/2017/36952
European Food Safety Authority and European Centre for Disease Prevention and Control (EFSA and ECDC) (2018) The European Union summary report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks in 2017. EFSA J.16. https://doi.org/10.2903/j.efsa.2018.5500
Food and Agriculture Organization (FAO) (2003) Assessment and Management of Seafood Safety and Quality: 5.1.1 Pathogenic bacteria (Hans Henrik Huss/Lone Gram). Food and Agriculture Organization of the United Nations, Rome. Available at https://www.fao.org/3/Y4743E/y4743e09.htm. Accessed 18 Dec 2023
Food and Agriculture Organization (FAO) (2010) Expert Workshop on the application of biosecurity Measures to control Salmonella Contamınatıon in Sustainable aquaculture FAO Fisheries and Aquaculture Report No. 937 ISSN 2070- 6987, Mangalore, India, 19–21 January 2010
Fierer J, Guiney DG (2001) Diverse virulence traits underlying different clinical outcomes of Salmonella infection. J Clin Investig 107:775–780. https://doi.org/10.1172/JCI12561
Figueiredo R, Henriques A, Sereno R, Mendonça N, Silva GJ (2013) Resistência a antibióticos em isolados de Salmonella enterica em alimentos de origem animal [Antimicrobial resistance of Salmonella enterica isolated from food of animal origin]. RPCV 108:39–43
Fikre D, Abdulahi SM, Hamid M, Abdula JA (2022) Prevalence and antimicrobial resistance profile of salmonella from fish harvested from Haramaya Lake, Eastern Ethiopia. Acta Sci Vet Sci 4:11
Food and Agriculture Organization (FAO), 2012. Fishery and aquaculture statistics 2012. Food and Agriculture Organization of the United Nations, Rome available at https://www.fao.org/documents/card/en/c/e533a964-a1a1-4d84-9de0. Accessed 2 Nov 2023
Food and Agriculture Organization (FAO) 2022. The State of World Fisheries and Aquaculture 2022. Towards Blue Transformation. Rome, FAO. https://doi.org/10.4060/cc0461en
Furushita M, Shiba T, Maeda T, Yahata M, Kaneoka A, Takahashi Y, Torii K, Hasegawa T, Ohta M (2003) Similarity of tetracycline resistance genes isolated from fish farm bacteria to those from clinical isolates. Appl Environ Microbiol 69:5336–5342. https://doi.org/10.1128/AEM.69.9.5336-5342.2003
Gawish MF, Ahmed AM, Torky HA, Shimamoto T (2021) Prevalence of extended-spectrum β-lactamase (ESBL)-producing Salmonella enterica from retail fishes in Egypt: a major threat to public health. Int J Food Microbiol 351:109268. https://doi.org/10.1016/j.ijfoodmicro.2021.109268
Germini A, Masola A, Carnevali P, Marchelli R (2009) Simultaneous detection of Escherichia coli O175: H7, Salmonella spp., and Listeria monocytogenes by multiplex PCR. J Food Control 20:733–738. https://doi.org/10.1016/j.foodcont.2008.09.010
Gorman R, Bloomfield S, Adley CC (2002) A study of cross-contamination of food-borne pathogens in the domestic kitchen in the Republic of Ireland. Int J Food Microbiol 76:143–150. https://doi.org/10.1016/S0168-1605(02)00028-4
Gorvel JP, Méresse S (2001) Maturation steps of the Salmonella-containing vacuole. Microbes Infect 3:1299–1303
Guerin PJ, De Jong B, Heir E, Hasseltvedt V, Kapperud G, Styrmo K, Gondrosen B, Lassen J, Andersson Y, Aavitsland P (2004) Outbreak of Salmonella Livingstone infection in Norway and Sweden due to contaminated processed fish products. Epidemiol Infect 132:889–895. https://doi.org/10.1017/S0950268804002523
Hansen-Wester I, Hensel M (2001) Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect 3:549–559. https://doi.org/10.1016/S1286-4579(01)01411-3
Hitchcock PJ, Leive L, Mäkelä PH, Rietschel ET, Strittmatter W, Morrison DC (1986) Lipopolysaccharide nomenclature–past, present, and future. J Bacteriol 184:2857–2862
Hounmanou YMG, Baniga Z, García V, Dalsgaard A (2022) Salmonella Salamae and S. Waycross isolated from Nile perch in Lake Victoria show limited human pathogenic potential. Sci Rep 12:1–11. https://doi.org/10.1038/s41598-022-08200-5
Hur J, Jawale C, Lee JH (2012) Antimicrobial resistance of Salmonella isolated from food animals: a review. Food Res Int 45:819–830. https://doi.org/10.1016/j.foodres.2011.05.014
Huss HH, Gram L (2004) Characterization of hazards in seafood assurance of seafood quality FAO Fisheries Technical Paper
Iwamoto M, Ayers T, Mahon BE, Swerdlow DL (2010) Epidemiology of seafood-associated infections in the United States. J Clin Microbiol 23:399–411. https://doi.org/10.1128/cmr.00059-09
Jacoby GA, Strahilevitz J, Hooper DC (2015) Plasmid-mediated quinolone resistance. Plasmids 30:475–503. https://doi.org/10.1128/9781555818982.ch25
Jeamsripong S, Kuldee M, Thaotumpitak V, Chuanchuen R (2023) Antimicrobial resistance, Extended-Spectrum β-Lactamase production and virulence genes in Salmonella enterica and Escherichia coli isolates from estuarine environment. PLoS ONE 18:1–16. https://doi.org/10.1371/journal.pone.0283359
Johari FB, Zapri NF, Mohamed S (2022) Prevalence of escherichia coli and salmonella in fish and blood clam (anadara granosa) from wet markets and hypermarkets in Kuala Pilah. J Acad 10:97–107
Joseph B, Otta SK, Karunasagar I, Karunasagar I (2001) Biofilm formation by Salmonella spp. On food contact surfaces and their sensitivity to sanitizers. Int J Food Microbiol 64:367–372. https://doi.org/10.1016/S0168-1605(00)00466-9
Kakatkar AS, Pansare LS, Gautam RK, Shashidhar R, Karani M, Bandekar JR (2011) Molecular characterization of antibiotic resistant Salmonella isolates from Indian foods. Food Res Int 44:3272–3275. https://doi.org/10.1016/j.foodres.2011.09.014
Khalefa HS, Ahmed ZS, Abdel-Kader F, Ismail EM, Elshafiee EA (2021) Sequencing and phylogenetic analysis of the stn gene of Salmonella species isolated from different environmental sources at Lake Qarun protectorate: The role of migratory birds and public health importance. Vet World 14(10):2764–2772. https://doi.org/10.14202/vetworld.2021.2764-2772
Koonse B, Burkhardt W III, Chirtel S, Hoskin GP (2005) Salmonella and the sanitary quality of aquacultured shrimp. J Food Prot 68:2527–2532. https://doi.org/10.4315/0362-028X-68.12.2527
Kotian A, Aditya V, Jazeela K, Karunasagar I, Karunasagar I, Deekshit VK (2020) Effect of bile on growth and biofilm formation of non-typhoidal Salmonella serovars isolated from seafood and poultry. Res Microbiol 171:165–173. https://doi.org/10.1016/j.resmic.2020.06.002
Kumar R, Surendran PK, Thampuran N (2009a) Analysis of antimicrobial resistance and plasmid profiles in salmonella serovars associated with tropical seafood of india. Foodborne Pathog Dis 6:621–625
Kumar Y, Sharma A, Sehgal R, Kumar S (2009b) Distribution trends of Salmonella serovars in India (2001–2005). Trans R Soc Trop Med Hyg 103:390–394. https://doi.org/10.1016/j.trstmh.2008.09.009
Kusumaningrum HD, Van Asselt ED, Beumer RR, Zwietering MH (2004) A quantitative analysis of cross-contamination of Salmonella and Campylobacter spp. via domestic kitchen surfaces. J Food Prot 67:1892–1903. https://doi.org/10.4315/0362-028X-67.9.1892
Lindstedt BA, Heir E, Nygård I, Kapperud G (2003) Characterization of class I integrons in clinical strains of Salmonella enterica subsp. enterica serovars Typhimurium and Enteritidis from Norwegian hospitals. Journal of Medical Microbiology. J Med Microbiol 52:141–149. https://doi.org/10.1099/jmm.0.04958-0
Liu X, Jiang Z, Liu Z, Li D, Liu Z, Dong X, Yan S (2023) Research Progress of Salmonella Pathogenicity Island. Int J Biol Life Sci 2:7–11. https://doi.org/10.5409/ijbls.v2i3.8643
Lorente-Cebrián S, Costa AG, Navas-Carretero S, Zabala M, Martínez JA, Moreno-Aliaga MJ (2013) Role of omega-3 fatty acids in obesity, metabolic syndrome, and cardiovascular diseases: a review of the evidence. J Physiol Biochem 69:633–651. https://doi.org/10.1007/s13105-013-0265-4
Lozano-Leon A, Garcia-Omil C, Dalama J, Rodriguez-Souto R, Martinez-Urtaza J, Gonzalez-Escalona N (2019) Detection of colistin resistance mcr-1 gene in Salmonella enterica serovar Rissen isolated from mussels, Spain, 2012 to 2016. Eurosurveillance 24:1–5. https://doi.org/10.2807/1560-7917.ES.2019.24.16.1900200
Lozano-León A, García-Omil C, Rodríguez-Souto RR, Lamas A, Garrido-Maestu A (2022) An Evaluation of the Pathogenic Potential, and the Antimicrobial Resistance, of Salmonella Strains Isolated from Mussels. Microorganisms. https://doi.org/10.3390/microorganisms10010126
Lunestad BT, Nesse L, Lassen J, Svihus B, Nesbakken T, Fossum K, Rosnes JT, Kruse H, Yazdankhah S (2007) Salmonella in fish feed; occurrence and implications for fish and human health in Norway. Aquaculture 265:1–8. https://doi.org/10.1016/j.aquaculture.2007.02.011
Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O’Brien SJ, Jones TF, Fazil A, Hoekstra RM (2010) The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50:882–889. https://doi.org/10.1086/650733
Marcus SL, Brumell JH, Pfeifer CG, Finlay BB (2000) Salmonella pathogenicity islands: big virulence in small packages. Microbes Infect 2:145–156. https://doi.org/10.1016/S1286-4579(00)00273-2
Marijani E (2022) Prevalence and Antimicrobial Resistance of Bacteria Isolated from Marine and Freshwater Fish in Tanzania. Int J Microbiol. https://doi.org/10.1155/2022/4652326
Mastroeni P, Vazquez-Torres A, Fang FC, Xu Y, Khan S, Hormaeche CE, Dougan G (2000) Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. The Journal of experimental medicine. J Exp Med 192:237–248. https://doi.org/10.1084/jem.192.2.237
Mdegela RH, Mhongole OJ, Kamundia PW, Byarugaba D, Mbuthia PG (2015) Identification of Salmonella and Vibrio in water and Oreochromis niloticus in Mwanza gulf, Lake Victoria, Tanzania. Int J Curr Res 7:18087–18092
Mumbo MT, Nyaboga EN, Kinyua JK, Muge EK, Mathenge SG, Rotich H, Muriira G, Njiraini B, Njiru JM (2023) Antimicrobial resistance profiles of Salmonella spp. and Escherichia coli isolated from fresh nile tilapia (Oreochromis niloticus) fish marketed for human consumption. BMC Microbiol 23:306. https://doi.org/10.1186/s12866-023-03049-8
Musto J, Kirk M, Lightfoot D, Combs BG, Mwanri L (2006) Multidrug resistant Salmonella Java infections acquired from tropical fish aquariums, Australia, 2003–04. Commun Dis Intell 30:222–227
Nair S, Wain J, Connell S, de Pinna E, Peters T (2014) Salmonella enterica subspecies II infections in England and Wales–the use of multilocus sequence ty** to assist serovar identification. J Med Microbiol 63:831–834. https://doi.org/10.1099/jmm.0.072702-0
Nakayama T, Yamamoto S, Ohata N, Yamaguchi T, **nai M, Minh DT, Hoang ON, Le Thi HI, Thanh PN, Hoai PH, Do PN (2023) Common presence of plasmid encoding blaCTX-M-55 in extended-spectrum β-lactamase-producing Salmonella enterica and Escherichia coli isolates from the same edible river fish. J Microorg Control. 28:49–56. https://doi.org/10.4265/jmc.28.2_49
Newaj-Fyzul A, Adesiyun AA, Mutani A (2006) Prevalence and antimicrobial resistance of Salmonella spp. isolated from apparently healthy ornamental fish and pond water in Trinidad. J Food, Agric Environ 4:27–29
Nguyen DT, Kanki M, Do Nguyen P, Le HT, Ngo PT, Tran DN, Le NH, Van Dang C, Kawai T, Kawahara R, Yonogi S (2016) Prevalence, antibiotic resistance, and extended-spectrum and AmpC β-lactamase productivity of Salmonella isolates from raw meat and seafood samples in Ho Chi Minh City, Vietnam. Int J Food Microbiol 236:115–122. https://doi.org/10.1016/j.ijfoodmicro.2016.07.017
Nimnoi P, Pongsilp N (2020) Distribution and expression of virulence genes in potentially pathogenic bacteria isolated from seafood in Thailand. CYTA J Food 8:753–763. https://doi.org/10.1080/19476337.2020.1842502
Nógrády N, Gadó I, Tóth Á, Pászti J (2005) Antibiotic resistance and class 1 integron patterns of non-typhoidal human Salmonella serotypes isolated in Hungary in 2002 and 2003. Int J Antimicrob Agents 26:126–132. https://doi.org/10.1016/j.ijantimicag.2005.04.015
Nys S, Okeke IN, Kariuki S, Dinant GJ, Driessen C, Stobberingh EE (2004) Antibiotic resistance of faecal Escherichia coli from healthy volunteers from eight develo** countries. J Anti Microb Chemother 54:952–955. https://doi.org/10.1093/jac/dkh448
Ogbonna D, Inana M (2018) Characterization and Multiple Antibiotic Resistance of Bacterial Isolates Associated with Fish Aquaculture in Ponds and Rivers in Port Harcourt. Nigeria J Adv Microbiol 10:1–14. https://doi.org/10.9734/JAMB/2018/41073
Ortega RM (2006) Importance of functional foods in the Mediterranean diet. Public Health Nutr 9:1136–1140. https://doi.org/10.1017/S1368980007668530
Över U, Gür D, Ünal S, Miller GH (2001) Aminoglycoside Resistance Study Group. The changing nature of aminoglycoside resistance mechanisms and prevalence of newly recognized resistance mechanisms in Turkey. Clin Microbiol Infect 7:470–478. https://doi.org/10.1046/j.1198-743x.2001.00284.x
Pandey PK, Kass PH, Soupir ML, Biswas S, Singh VP (2014) Contamination of water resources by pathogenic bacteria. AMB Express 4:1–6. https://doi.org/10.1186/s13568-014-0051-x
Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, Churcher C, Mungall KL, Bentley SD, Holden MT, Sebaihia M, Baker S, Basham D, Brooks K, Chillingworth T, Connerton P, Cronin A, Davis P, Davies RM, Dowd L, White N, Farrar J, Feltwell T, Hamlin N, Haque A, Hien TT, Holroyd S, Jagels K, Krogh A, Larsen TS, Leather S, Moule S, O’Gaora P, Parry C, Quail M, Rutherford K, Simmonds M, Skelton J, Stevens K, Whitehead S, Barrell BG (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413:848–852. https://doi.org/10.1038/35101607
Phan TT, Khai LT, Ogasawara N, Tam NT, Okatani AT, Akiba M, Hayashidani H (2005) Contamination of Salmonella in retail meats and shrimps in the Mekong Delta. Vietnam J Food Prot 65:1077–1080
Pickard D, Wain J, Baker S, Line A, Chohan S, Fookes M, Barron A, Gaora PO, Chabalgoity JA, Thanky N, Scholes C, Thomson N, Quail M, Parkhill J, Dougan G (2003) Composition, acquisition, and distribution of the Vi exopolysaccharide-encoding Salmonella enterica Pathogenicity Island SPI-7. J Bacteriol 185:5055–5065. https://doi.org/10.1128/jb.185.17.5055-5065.2003
Ponce E, Khan AA, Cheng CM, Summage-West C, Cerniglia CE (2008) Prevalence and characterization of Salmonella enterica serovar Weltevreden from imported seafood. Food Microbiol 25:29–35. https://doi.org/10.1016/j.fm.2007.09.001
Prabhakar P, Lekshmi M, Ammini P, Nayak BB, Kumar S (2020) Salmonella contamination of seafood in landing centers and retail markets of Mumbai, India. J AOAC Int 103:1361–1365. https://doi.org/10.1093/jaoacint/qsaa042
Rahimi E, Shakerian A, Falavarjani AG (2013) Prevalence and antimicrobial resistance of Salmonella isolated from fish, shrimp, lobster, and crab in Iran. Comp Clin Path 22:59–62. https://doi.org/10.1007/s00580-011-1368-3
Rakthong P (2023) Prevalence and Antimicrobial Resistance of Salmonella Isolated from Blood Cockles in Surat Thani Province, Thailand. Health Sci J Thailand 5:48–56. https://doi.org/10.55164/hsjt.v5i2.258935
Raufu IA, Lawan FA, Bello HS, Musa AS, Ameh JA, Ambali AG (2014) Occurrence and antimicrobial susceptibility profiles of Salmonella serovars from fish in Maiduguri, sub-Saharah, Nigeria, Egypt. J Aquat Res 40:59–63. https://doi.org/10.1016/j.ejar.2014.01.003
Riehle MM, Bennett AF, Long AD (2001) Genetic architecture of thermal adaptation in Escherichia coli. Proc Natl Acad Sci USA 98:525–530. https://doi.org/10.1073/pnas.98.2.525
Saharan VV, Verma P, Singh AP (2020) High prevalence of antimicrobial resistance in Escherichia coli, Salmonella spp. and Staphylococcus aureus isolated from fish samples in India. Aquac Res 51:1200–1210. https://doi.org/10.1111/are.14471
Salam F, Lekshmi M, Prabhakar P, Kumar SH, Nayak BB (2023) Physiological characteristics and virulence gene composition of selected serovars of seafood-borne Salmonella enterica. Vet World 16:431–438. https://doi.org/10.14202/vetworld.2023.431-438
Saroj SD, Shashidhar R, Karani M, Bandekar JR (2008) Distribution of Salmonella pathogenicity island (SPI)-8 and SPI-10 among different serotypes of Salmonella. J Med Microbiol 57:424–427. https://doi.org/10.1099/jmm.0.47630-0
Shabarinath S, Sanath Kumar H, Khushiramani R, Karunasagar I, Karunasagar I (2007) Detection and characterization of Salmonella associated with tropical seafood. Int J Food Microbiol 114:227–233. https://doi.org/10.1016/j.ijfoodmicro.2006.09.012
Sing CK, Khan MZ, Daud HH, Aziz AR (2016) Prevalence of Salmonella sp in African Catfish (Clarias gariepinus) obtained from farms and wet markets in Kelantan, Malaysia and their antibiotic resistance. Sains Malaysiana 45:1597–1602. https://doi.org/10.1128/iai.01275-08
Singh AS, Lekshmi M, Prakasan S, Nayak BB, Kumar S (2017) Multiple antibiotic-resistant, extended spectrum-β-lactamase (ESBL)-producing enterobacteria in fresh seafood. Microorganisms. https://doi.org/10.3390/microorganisms5030053
Stanaway JD, Parisi A, Sarkar K, Blacker BF, Reiner RC, Hay SI, Nixon MR, Dolecek C, James SL, Mokdad AH, Abebe G (2019) The global burden of non-typhoidal Salmonella invasive disease: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Infect Dis 19:1312–1324. https://doi.org/10.1016/S1473-3099(19)30418-9
Stephen J, Lekshmi M, Nayak BB, Kumar SH (2022) First report of a multidrug-resistant Salmonella enterica Serovar Infantis carrying pESI megaplasmid isolated from marine shrimp in India. J Glob Antimicrob Resist 31:248–251. https://doi.org/10.1016/j.jgar.2022.09.014
Surya T, Jeyasekaran G, Shakila RJ, Sivaraman B, Shalini R, Sundhar S, Arisekar U (2000) Prevalence of biofilm forming Salmonella in different seafood contact surfaces of fishing boats, fish landing centres, fish markets and seafood processing plants. Mar Pollut Bull 1:114285. https://doi.org/10.1016/j.marpolbul.2022.114285
Szeto J, Namolovan A, Osborne SE, Coombes BK, Brumell JH (2009) Salmonella-containing vacuoles display centrifugal movement associated with cell-to-cell transfer in epithelial cells. Infect Immun Infect Immun 77:996–1007. https://doi.org/10.1128/iai.01275-08
Tekale AA, Savalia CV, Kshirsagar DP, Brahmbhatt MN, Chatur YA (2015) Detection and virulence gene characterization of Salmonella isolates from fish by conventional and molecular methods. J Vet Pub Hlth 13:43–46
Tessari EN, Kanashiro AM, Stoppa GF, Luciano RL, De Castro AG, Cardoso AL (2012) Important aspects of Salmonella in the poultry industry and in public health. Salmonella-A Dangerous Foodborne Pathogen 20:182–206
Thaotumpitak V, Sripradite J, Atwill ER, Jeamsripong S (2023) Emergence of colistin resistance and characterization of antimicrobial resistance and virulence factors of Aeromonas hydrophila, Salmonella spp. and Vibrio cholerae isolated from hybrid red tilapia cage culture. PeerJ 11:e148966. https://doi.org/10.7717/peerj.14896
Thomas CM, Nielsen KM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711–721. https://doi.org/10.1038/nrmicro1234
Tomastikova Z, Romero SB, Knotek Z, Karpiskova R (2017) Prevalence and characteristics of Salmonella species isolated from captive reptiles in the Czech Republic. Vet Med 62:456–469. https://doi.org/10.17221/44/2017-VETMED
Van TTH, Moutafis G, Tran LT, Coloe PJ (2007) Antibiotic resistance in foodborne bacterial contaminants in Vietnam. Appl Environ Microbiol 73:7906–7911. https://doi.org/10.1128/AEM.00973-07
van Asten AJ, van Dijk JE (2005) Distribution of “classic” virulence factors among Salmonella spp. FEMS Immunol Med Microbiol 44:251–259. https://doi.org/10.1016/j.femsim.2005.02.002
White W (1998) Medical consequences of antibiotic use in agriculture. Science 279:996–997. https://doi.org/10.1126/science.279.5353.996
Yan H, Li L, Alam MJ, Shinoda S, Miyoshi S-i, Shi L (2010) Prevalence and antimicrobial resistance of Salmonella in retail foods in northern China. Int J Food Microbiol 143:230–234. https://doi.org/10.1016/j.ijfoodmicro.2010.07.034
Yanestria SM, Rahmaniar RP, Wibisono FJ, Effendi MH (2019) Detection of invA gene of Salmonella from milkfish (Chanos chanos) at Sidoarjo wet fish market, Indonesia, using polymerase chain reaction technique. Vet World 12:170–175. https://doi.org/10.14202/vetworld.2019.170-175
Yang X, Wu Q, Zhang J, Huang J, Chen L, Liu S, Yu S, Cai S (2015) Prevalence, enumeration, and characterization of Salmonella isolated from aquatic food products from retail markets in China. Food Control 57:308–313. https://doi.org/10.1016/j.foodcont.2015.03.046
Yang X, Wu Q, Zhang J, Huang J, Chen L, Wu S, Zeng H, Wang J, Chen M, Wu H, Gu Q (2019) Prevalence, bacterial load, and antimicrobial resistance of Salmonella serovars isolated from retail meat and meat products in China. Front Microbiol 10:2121. https://doi.org/10.3389/fmicb.2019.02121
Yang X, Huang J, Zhang Y, Liu S, Chen L, **ao C, Zeng H, Wei X, Gu Q, Li Y, Wang J (2020) Prevalence, abundance, serovars and antimicrobial resistance of Salmonella isolated from retail raw poultry meat in China. Sci Total Environ 713:136385. https://doi.org/10.1016/j.scitotenv.2019.136385
Yang X, Huang J, Su Y, Cai S, Zhang J, Guo W, Wang J, Chen M, Wu S, Yang S, Wu Q (2022) Incidence and antimicrobial resistance of Salmonella serovars in fresh retail aquatic products from China. Lwt 171:114123. https://doi.org/10.1016/j.lwt.2022.114123
Zhang J, Yang X, Kuang D, Shi X, **ao W, Zhang J, Gu Z, Xu X, Meng J (2015) Prevalence of antimicrobial resistance of non-typhoidal Salmonella serovars in retail aquaculture products. Int J Food Microbiol 210:47–52. https://doi.org/10.1016/j.ijfoodmicro.2015.04.019
Zhang S, den Bakker HC, Li S, Chen J, Dinsmore BA, Lane C, Lauer AC, Fields PI, Deng X (2019) SeqSero2: Rapid and improved Salmonella serotype determination using whole-genome sequencing data. Appl Environ Microbiol 85:e01746-e1819. https://doi.org/10.1128/AEM.01746-19
Zhao S, McDermott PF, Friedman S, Qaiyumi S, Abbott J, Kiessling C, Ayers S, Singh R, Hubert S, Sofos J, White DG (2006) Characterization of antimicrobial-resistant Salmonella isolated from imported foods. J Food Prot 69:500–507. https://doi.org/10.4315/0362-028X-69.3.500
Acknowledgements
This research received no specific grant from public, commercial, or not-for-profit funding agencies.
Author information
Authors and Affiliations
Contributions
SM and G-JH contributed to the conception and design of the study. SM, PMK, and G-JH performed the literature search. SM wrote the first draft of the manuscript, and all authors contributed to reviewing and editing the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Majeed, S., Kumarage, P.M. & Heo, GJ. Virulence and antimicrobial resistance genes occurring in Salmonella spp. isolated from aquatic food. J Consum Prot Food Saf 19, 15–32 (2024). https://doi.org/10.1007/s00003-023-01474-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00003-023-01474-5