Abstract
Acute/chronic gastroenteritis is caused by a few serovars of Salmonella enterica. Among different serovars, S. enterica Typhimurium is a potent pathogen that contributes significantly to self-limiting diarrhea related mortality worldwide. With no successful vaccine in hand against this pathogen, antibiotics are used as for gold standard for treatment against Salmonella induced gastroenteritis. Indispensably, rise in multi drug resistance against Salmonella Typhimurium poses challenge to treatment options. South East Asia, with 11 different countries, stands 3rd as super region for global burden of Salmonella induced gastroenteritis. In this review, we made an attempt to discuss on prevalence and multidrug resistance in Salmonella Typhimurium in 11 countries of South East Asia—the issue that has not been seriously addressed so far. By thorough analysis of reported data, we found varying frequencies for prevalence of Salmonella Typhimurium as well as subtle evidences on resistance of this pathogen to multiple antibiotics in different countries. Vietnam ranked top in terms of reports for prevalence and antimicrobial resistance. However, in countries such as Brunei and Timor Leste, no study has been performed so far to track the frequency of incidence and drug resistance of this pathogen. Our review, the first of its kind, emphasizes that, although the pathogen was not found as dominant serovar in South East Asia in last 20 years unlike sub-Saharan Africa, it may be still considered as a major threat in this region due to available evidences for infection in humans as well as contamination in several animal and food sources. More importantly, the importance as a public threat in this subregion of Asia is also due to resistance of this pathogen to multiple antibiotics.
Graphic abstract
South East Asian countries showing incidence and multi drug resistance of Salmonella enterica Typhimurium in human and non-human sources (1969–2020). —Drug resistant S. enterica Typhimurium.
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References
Ao TT, Feasey NA, Gordon MA, Keddy KH, Angulo FJ, Crump JA (2015) Global burden of invasive nontyphoidal Salmonella disease, 2010(1). Emerg Infect Dis. https://doi.org/10.3201/eid2106.140999
Aung KT, Chen HJ, Chau ML, Yap G, Lim XF, Humaidi M et al (2019) Salmonella in retail food and wild birds in Singapore—prevalence, antimicrobial resistance, and sequence types. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph16214235
Benacer D, Thong KL, Watanabe H, Puthucheary SD (2010) Characterization of drug resistant Salmonella enterica serotype Typhimurium by antibiograms, plasmids, integrons, resistance genes and PFGE. J Microbiol Biotechnol 20:1042–1052. https://doi.org/10.4014/jmb.0910.10028
Bukitwetan P, Suryawidjaja JE, Salim O, Hidayat A, Herwana E, Lesmana M (2007) Serovar distribution and antibiotic susceptibility of nontyphoidal Salmonella isolated from pediatric patients in Jakarta, Indonesia. Southeast Asian J Trop Med Public Health 38:1088–1094
Collaborators G B D N-T S I D (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
Dhanoa A, Fatt QK (2009) Non-typhoidal Salmonella bacteraemia: epidemiology, clinical characteristics and its’ association with severe immunosuppression. Ann Clin Microbiol Antimicrob 8:15. https://doi.org/10.1186/1476-0711-8-15
Duong VT, The HC, Nhu TDH, Tuyen HT, Campbell JI, Minh PV et al (2020) Genomic serotyping, clinical manifestations, and antimicrobial resistance of nontyphoidal Salmonella gastroenteritis in hospitalized children in Ho Chi Minh City, Vietnam. J Clin Microbiol. https://doi.org/10.1128/JCM.01465-20
Ellerbroek L, Narapati D, Phu Tai N, Poosaran N, Pinthong R, Sirimalaisuwan A et al (2010) Antibiotic resistance in Salmonella isolates from imported chicken carcasses in Bhutan and from pig carcasses in Vietnam. J Food Prot 73:376–379. https://doi.org/10.4315/0362-028x-73.2.376
Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA (2012) Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 379:2489–2499. https://doi.org/10.1016/S0140-6736(11)61752-2
Ferrari RG, Rosario DKA, Cunha-Neto A, Mano SB, Figueiredo EES, Conte-Junior CA (2019) Worldwide epidemiology of Salmonella serovars in animal-based foods: a meta-analysis. Appl Environ Microbiol. https://doi.org/10.1128/AEM.00591-19
Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, Aarestrup FM (2011) Global monitoring of Salmonella serovar distribution from the World Health Organization Global Foodborne Infections Network Country Data Bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis 8:887–900. https://doi.org/10.1089/fpd.2010.0787
Huoy L, Pornruangwong S, Pulsrikarn C, Chaturongakul S (2014) Molecular characterization of Thai Salmonella enterica serotype typhimurium and serotype 4,5,12:i:- reveals distinct genetic deletion patterns. Foodborne Pathog Dis 11:589–592. https://doi.org/10.1089/fpd.2013.1723
Inthavong P, Srikitjakarn L, Kyule M, Zessin KH, Baumann M, Douangngeun B, Fries R (2006) Microbial contamination of pig carcasses at a slaughterhouse in Vientiane capital, Lao PDR. Southeast Asian J Trop Med Public Health 37:1237–1241
Lan TTQ, Gaucher ML, Nhan NTM, Letellier A, Quessy S (2018) Distribution of virulence genes among Salmonella serotypes isolated from pigs in Southern Vietnam. J Food Prot 81:1459–1466. https://doi.org/10.4315/0362-028X.JFP-17-408
Lay KS, Vuthy Y, Song P, Phol K, Sarthou JL (2011) Prevalence, numbers and antimicrobial susceptibilities of Salmonella serovars and Campylobacter spp. in retail poultry in Phnom Penh, Cambodia. J Vet Med Sci 73:325–329. https://doi.org/10.1292/jvms.10-0373
Le Thi Phuong T, Rattanavong S, Vongsouvath M, Davong V, Phu Huong Lan N, Campbell JI et al (2017) Non-typhoidal Salmonella serovars associated with invasive and non-invasive disease in the Lao People’s Democratic Republic. Trans R Soc Trop Med Hyg 111:418–424. https://doi.org/10.1093/trstmh/trx076
Lee HY, Su LH, Tsai MH, Kim SW, Chang HH, Jung SI et al (2009) High rate of reduced susceptibility to ciprofloxacin and ceftriaxone among nontyphoid Salmonella clinical isolates in Asia. Antimicrob Agents Chemother 53:2696–2699. https://doi.org/10.1128/AAC.01297-08
Lertworapreecha M, Noomee S, Sutthimusik S, Utarapichat B, Tontikapong K (2016) Multidrug resistant and extended spectrum b-lactamase producing Salmonella enterica isolated from food animals in Phatthalung, Thailand. Southeast Asian J Trop Med Public Health 47:1257–1269
Lettini AA, Vo Than T, Marafin E, Longo A, Antonello K, Zavagnin P et al (2016) Distribution of Salmonella serovars and antimicrobial susceptibility from poultry and swine farms in Central Vietnam. Zoonoses Public Health 63:569–576. https://doi.org/10.1111/zph.12265
Ling ML, Goh KT, Wang GC, Neo KS, Chua T (2002) An outbreak of multidrug-resistant Salmonella enterica subsp. enterica serotype Typhimurium, DT104L linked to dried anchovy in Singapore. Epidemiol Infect 128:1–5. https://doi.org/10.1017/s0950268801006367
Luu QH, Fries R, Padungtod P, Tran TH, Kyule MN, Baumann MP, Zessin KH (2006) Prevalence of Salmonella in retail chicken meat in Hanoi, Vietnam. Ann NY Acad Sci 1081:257–261. https://doi.org/10.1196/annals.1373.032
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG et al (2012) Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 18:268–281. https://doi.org/10.1111/j.1469-0691.2011.03570.x
Mahon BE, Fields PI (2016) Invasive infections with nontyphoidal Salmonella in Sub-Saharan Africa. Microbiol Spectr. https://doi.org/10.1128/microbiolspec.EI10-0015-2016
McDermott PF, Zhao S, Wagner DD, Simjee S, Walker RD, White DG (2002) The food safety perspective of antibiotic resistance. Anim Biotechnol 13:71–84. https://doi.org/10.1081/ABIO-120005771
Moe AZ, Paulsen P, Pichpol D, Fries R, Irsigler H, Baumann MP, Oo KN (2017) Prevalence and antimicrobial resistance of Salmonella isolates from chicken carcasses in retail markets in Yangon, Myanmar. J Food Prot 80:947–951. https://doi.org/10.4315/0362-028X.JFP-16-407
Ng KC, Rivera WL (2014) Antimicrobial resistance of Salmonella enterica isolates from tonsil and jejunum with lymph node tissues of slaughtered swine in Metro Manila, Philippines. ISRN Microbiol 2014:364265. https://doi.org/10.1155/2014/364265
Nguyen DT, Kanki M, Nguyen PD, Le HT, Ngo PT, Tran DN et al (2016) Prevalence, antibiotic resistance, and extended-spectrum and AmpC beta-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
Nguyen Thi H, Pham TT, Turchi B, Fratini F, Ebani VV, Cerri D, Bertelloni F (2020) Characterization of Salmonella spp. isolates from swine: virulence and antimicrobial resistance. Animals (Basel). https://doi.org/10.3390/ani10122418
Nhung NT, Van NTB, Cuong NV, Duong TTQ, Nhat TT, Hang TTT et al (2018) Antimicrobial residues and resistance against critically important antimicrobials in non-typhoidal Salmonella from meat sold at wet markets and supermarkets in Vietnam. Int J Food Microbiol 266:301–309. https://doi.org/10.1016/j.ijfoodmicro.2017.12.015
Ogasawara N, Tran TP, Ly TL, Nguyen TT, Iwata T, Okatani AT et al (2008) Antimicrobial susceptibilities of Salmonella from domestic animals, food and human in the Mekong Delta, Vietnam. J Vet Med Sci 70:1159–1164. https://doi.org/10.1292/jvms.70.1159
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 68:1077–1080. https://doi.org/10.4315/0362-028x-68.5.1077
Phongaran D, Khang-Air S, Angkititrakul S (2019) Molecular epidemiology and antimicrobial resistance of Salmonella isolates from broilers and pigs in Thailand. Vet World 12:1311–1318. https://doi.org/10.14202/vetworld.2019.1311-1318
Phu Huong Lan N, Le Thi Phuong T, Nguyen Huu H, Thuy L, Mather AE, Park SE et al (2016) Invasive non-typhoidal Salmonella infections in Asia: clinical observations, disease outcome and dominant serovars from an infectious disease hospital in Vietnam. PLoS Negl Trop Dis 10:e0004857. https://doi.org/10.1371/journal.pntd.0004857
Pornruangwong S, Sriyapai T, Pulsrikarn C, Sawanpanyalert P, Boonmar S, Bangtrakulnonth A (2008) The epidemiological relationship between Salmonella enterica serovar typhimurium and Salmonella enterica serovar 4,[5],12:i:- isolates from humans and swine in Thailand. Southeast Asian J Trop Med Public Health 39:288–296
Reddy EA, Shaw AV, Crump JA (2010) Community-acquired bloodstream infections in Africa: a systematic review and meta-analysis. Lancet Infect Dis 10:417–432. https://doi.org/10.1016/S1473-3099(10)70072-4
Sanguankiat A, Pinthong R, Padungtod P, Baumann MP, Zessin KH, Srikitjakarn L, Fries R (2010) A cross-sectional study of Salmonella in pork products in Chiang Mai, Thailand. Foodborne Pathog Dis 7:873–878. https://doi.org/10.1089/fpd.2009.0436
Santos PDM, Widmer KW, Rivera WL (2020) PCR-based detection and serovar identification of Salmonella in retail meat collected from wet markets in Metro Manila, Philippines. Plos One 15:e0239457. https://doi.org/10.1371/journal.pone.0239457
Saw S, Mak J, Tan M, Teo S, Tan T, Cheow M et al (2020) Detection and quantification of salmonella in fresh vegetables in Perak, Malaysia. Food Res 4:441–448
Sinwat N, Angkittitrakul S, Coulson KF, Pilapil FM, Meunsene D, Chuanchuen R (2016) High prevalence and molecular characteristics of multidrug-resistant Salmonella in pigs, pork and humans in Thailand and Laos provinces. J Med Microbiol 65:1182–1193. https://doi.org/10.1099/jmm.0.000339
Sirichote P, Bangtrakulnonth A, Tianmanee K, Unahalekhaka A, Oulai A, Chittaphithakchai P et al (2010) Serotypes and antimicrobial resistance of Salmonella enterica ssp in central Thailand, 2001–2006. Southeast Asian J Trop Med Public Health 41:1405–1415
Ta YT, Nguyen TT, To PB, da Pham X, Le HT, Thi GN et al (2014) Quantification, serovars, and antibiotic resistance of salmonella isolated from retail raw chicken meat in Vietnam. J Food Prot 77:57–66. https://doi.org/10.4315/0362-028X.JFP-13-221
Thai TH, Hirai T, Lan NT, Yamaguchi R (2012) Antibiotic resistance profiles of Salmonella serovars isolated from retail pork and chicken meat in North Vietnam. Int J Food Microbiol 156:147–151. https://doi.org/10.1016/j.ijfoodmicro.2012.03.016
Thung TY, Mahyudin NA, Basri DF, Wan Mohamed Radzi CW, Nakaguchi Y, Nishibuchi M, Radu S (2016) Prevalence and antibiotic resistance of Salmonella Enteritidis and Salmonella Typhimurium in raw chicken meat at retail markets in Malaysia. Poult Sci 95:1888–1893. https://doi.org/10.3382/ps/pew144
Thung TY, Radu S, Mahyudin NA, Rukayadi Y, Zakaria Z, Mazlan N et al (2017) Prevalence, virulence genes and antimicrobial resistance profiles of Salmonella serovars from retail beef in Selangor, Malaysia. Front Microbiol 8:2697. https://doi.org/10.3389/fmicb.2017.02697
Tran TP, Ly TL, Nguyen TT, Akiba M, Ogasawara N, Shinoda D et al (2004) Prevalence of Salmonella spp. in pigs, chickens and ducks in the Mekong Delta, Vietnam. J Vet Med Sci 66:1011–1014. https://doi.org/10.1292/jvms.66.1011
Tribuddharat C, Pongpech P, Srifuengfung S, Meethai C (2016) Prevalence and drug susceptibility of Salmonella isolated from patients in Bangkok, Thailand. J Glob Antimicrob Resist 6:162–164. https://doi.org/10.1016/j.jgar.2016.05.004
Trongjit S, Angkititrakul S, Tuttle RE, Poungseree J, Padungtod P, Chuanchuen R (2017) Prevalence and antimicrobial resistance in Salmonella enterica isolated from broiler chickens, pigs and meat products in Thailand-Cambodia border provinces. Microbiol Immunol 61:23–33. https://doi.org/10.1111/1348-0421.12462
Trung NV, Carrique-Mas JJ, Nghia NH, Tu LT, Mai HH, Tuyen HT et al (2017) Non-typhoidal Salmonella colonization in chickens and humans in the Mekong Delta of Vietnam. Zoonoses Public Health 64:94–99. https://doi.org/10.1111/zph.12270
Tu LT, Hoang NV, Cuong NV, Campbell J, Bryant JE, Hoa NT et al (2015) High levels of contamination and antimicrobial-resistant non-typhoidal Salmonella serovars on pig and poultry farms in the Mekong Delta of Vietnam. Epidemiol Infect 143:3074–3086. https://doi.org/10.1017/S0950268815000102
Van TT, Moutafis G, Istivan T, Tran LT, Coloe PJ (2007) Detection of Salmonella spp. in retail raw food samples from Vietnam and characterization of their antibiotic resistance. Appl Environ Microbiol 73:6885–6890. https://doi.org/10.1128/AEM.00972-07
Velge P, Wiedemann A, Rosselin M, Abed N, Boumart Z, Chausse AM et al (2012) Multiplicity of Salmonella entry mechanisms, a new paradigm for Salmonella pathogenesis. MicrobiologyOpen 1:243–258. https://doi.org/10.1002/mbo3.28
Vo AT, van Duijkeren E, Fluit AC, Heck ME, Verbruggen A, Maas HM, Gaastra W (2006) Distribution of Salmonella enterica serovars from humans, livestock and meat in Vietnam and the dominance of Salmonella Typhimurium phage type 90. Vet Microbiol 113:153–158. https://doi.org/10.1016/j.vetmic.2005.10.034
Waturangi DE, Wiratama E, Theresia AS (2019) Prevalence and molecular characterization of Salmonella enterica serovar Typhimurium from ice and beverages in Jakarta, Indonesia. BMC Res Notes 12:45. https://doi.org/10.1186/s13104-019-4065-y
Whistler T, Sapchookul P, McCormick DW, Sangwichian O, Jorakate P, Makprasert S et al (2018) Epidemiology and antimicrobial resistance of invasive non-typhoidal Salmonellosis in rural Thailand from 2006–2014. PLoS Negl Trop Dis 12:e0006718. https://doi.org/10.1371/journal.pntd.0006718
World Health Organization & WHO Advisory Group on Integrated Surveillance of Antimicrobial Resistance (AGISAR) (2017) Critically important antimicrobials for human medicine: ranking of antimicrobial agents for risk management of antimicrobial resistance due to non-human use, 5th rev. World Health Organization
Yen NTP, Nhung NT, Van NTB, Cuong NV, Tien Chau LT, Trinh HN et al (2020) Antimicrobial residues, non-typhoidal Salmonella, Vibrio spp. and associated microbiological hazards in retail shrimps purchased in Ho Chi Minh city (Vietnam). Food Control 107:106756. https://doi.org/10.1016/j.foodcont.2019.106756
Yoke-Kqueen C, Learn-Han L, Noorzaleha AS, Son R, Sabrina S, Jiun-Horng S, Chai-Hoon K (2008) Characterization of multiple-antimicrobial-resistant Salmonella enterica Subsp. enterica isolated from indigenous vegetables and poultry in Malaysia. Lett Appl Microbiol 46:318–324. https://doi.org/10.1111/j.1472-765X.2007.02311.x
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The authors acknowledge the support of Department of Biotechnology (Centre of Excellence and Innovation in Biotechnology), Government of India for providing financial assistance. Grant No. BT/MED/30/SP19662/2018.
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The authors acknowledge the support of Department of Biotechnology (Centre of Excellence and Innovation in Biotechnology), Government of India, for providing financial assistance. Grant no. BT/MED/30/SP19662/2018.
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Patra, S.D., Mohakud, N.K., Panda, R.K. et al. Prevalence and multidrug resistance in Salmonella enterica Typhimurium: an overview in South East Asia. World J Microbiol Biotechnol 37, 185 (2021). https://doi.org/10.1007/s11274-021-03146-8
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DOI: https://doi.org/10.1007/s11274-021-03146-8