Salmonella enterica serovars Takoradi, Tananarive and Uganda from foods in Tripura, their virulence & antimicrobial resistance

Goutam Chowdhury; Hritusree Guha; Asish K. Mukhopadhyay; Madhuchanda Das; Venencia Albert; Samaresh Das; Nilanjan Chakraborty; Shanta Dutta; Tapan Majumdar; Thandavarayan Ramamurthy

doi:10.25259/ijmr_179_24

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10.25259/ijmr_179_24

Salmonella enterica serovars Takoradi, Tananarive and Uganda from foods in Tripura, their virulence & antimicrobial resistance

Goutam Chowdhury^1,#, Hritusree Guha^3,#, Asish K. Mukhopadhyay¹, Madhuchanda Das⁴, Venencia Albert⁴, Samaresh Das², Nilanjan Chakraborty¹, Shanta Dutta¹, Tapan Majumdar³, Thandavarayan Ramamurthy¹

1ICMR-National Institute of Cholera and Enteric Diseases, Kolkata, India

2Centre for Development of Advanced Computing (CDAC), Kolkata, India

3Department of Microbiology, Agartala Government Medical College, Tripura, India

4Indian Council of Medical Research, New Delhi, India

#Equal Contribution

*For correspondence: drtapan1960@gmail.com

Received: 2024-01-27, Epub ahead of print: 2024-09-27, Published: 2024-09-30

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This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, transform, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.

Sir,

The presence of Salmonella in foods has been considered a public health issue, as the pathogen might be transmitted from the contaminated foods into the human food chain. The zoonotic pathogen Salmonella enterica is a leading cause of foodborne infection in humans^1,2. Currently, the number of outbreaks due to S. enterica infections is increasing mostly due to contaminated foods of animal origin³.

The species S. enterica is highly diverse with about 2,600 serovars⁴. Based on the infectivity, they are classified as typhoidal (TS) and non-typhoidal Salmonella (NTS) serovars. Control of NTS is challenging as they have multiple sources and virulence factors. Gastroenteritis caused by the NTS is self-limiting, but it also instigates significant health risks due to its invasive nature⁵. The incidence of invasive non-typhoidal Salmonella (iNTS) has been increasing in several countries, especially Malawi^6-8. Globally, the infections and deaths caused by NTS have been projected to be about 78 million and >59,000, respectively⁹.

NTS control requires a ‘One Health Approach’, as involving multiple sectors such as public health, animal welfare, and food and environment protection remains essential. The NTS infections in India are on the rise¹⁰. Several virulence factors in TS and NTS encoded on the Salmonella pathogenicity islands (SPIs) play an important role in invasion into the host cell, multiplication and spread¹¹.

Since 2020, the Indian Council of Medical Research (ICMR) has conducted an ongoing project on systematic laboratory-based surveillance of foodborne enteric disease and related outbreaks in four North-east Indian States. Between January and April 2023, we screened 1004 food samples collected from 36 places covering 4 different regions of Tripura. During the surveillance period, there was no flux of foreign travellers. In this ongoing study, we identified three S. enterica serovars that were not reported from India. These Salmonella strains were first identified by biochemical tests¹², followed by serotyping using Salmonella somatic (O) and flagellar (H) antisera (SSI Diagnostica, Denmark) according to the Kauffmann–White scheme⁴. Antimicrobial susceptibility was determined by disk diffusion testing¹³. To determine the important virulence encoding genes, these strains were subjected to PCR analysis following previously published methods^14,15.

S. enterica serovars Takoradi, Tananarive and Uganda were identified from market samples of mutton, sweet and fish, respectively, collected between January and April 2023 in Tripura. The serotype scheme, antimicrobial resistance profile and virulence-encoding genes detected by the PCR assay are shown in Table. S. Takoradi and S. Tananarive were resistant to tetracycline. All these serovars showed reduced susceptibility to azithromycin but were susceptible to fluoroquinolones (ciprofloxacin, norfloxacin, ofloxacin), meropenem, ceftriaxone, sulfamethoxazole/trimethoprim, chloramphenicol and cefotaxime. The emergence of reduced susceptibility to azithromycin is a cause of concern. This drug has been used to treat enteric infections in India. Many of the TS and NTS clinical strains have shown resistance to azithromycin^16,17.

Table. Detection of antimicrobial resistance and virulence encoding genes in S. Takorandi, S. Tananarive and S. Uganda

Sample ID	Source	Salmonella enterica serovar (O:H antigen formula)	Antimicrobial susceptibility test			Virulence encoding gene^*
Sample ID	Source	Salmonella enterica serovar (O:H antigen formula)	Resistance	Intermediate	Susceptible	Virulence encoding gene^*
TRP/NTH/RAWMEAT/1829	Mutton	Takoradi (8:i;1,5)	TET	AM, S, AZM, D, CAZ	NA, CIP, NOR, OFX, MEM, CR, SXT, C, CTX	invE/A, orgA, ttrC, ssaQ, mgtC, misL, spi4R, spi4D, sopB, pipA, hilA, stn
TRP/STH/SWEET/1966	Sweet	Tananarive (6,8:y;1,5)	TET	AM, S, AZM, D	NA, CIP, NOR, OFX, MEM, CR, SXT, C, CAZ, CTX	invE/A, orgA, ttrC, ssaQ, mgtC, misL, spi4R, spi4D, sopB, pipA, hilA, stn
TRP/DHL/RAWFISH/1104	Fish	Uganda (3,10:l,z₁₃;1,5)		AM, S, AZM, D, NA, TET	CIP, NOR, OFX, MEM, CRO, SXT, C, CAZ, CTX	invE/A, orgA, ttrC, ssaQ, mgtC, misL, spi4R, spi4D, soupB, pipA, pefA, hilA, stn

* All the serovars were negative for spvC. AM, ampicillin; AZM, azithromycin; C, chloramphenicol; CAZ, ceftazidime; CIP, ciprofloxacin; CRO, ceftriaxone; CTX, cefotaxime; D, doxycycline; MEM, meropenem; NA, nalidixic acid; NOR, norfloxacin; OFX, ofloxacin; S, streptomycin; SXT, sulfamethoxazole/trimethoprim; TET, tetracycline

All the three serovars harboured orgA, (oxygen-regulated gene for host recognition and invasion), invE/A (SPI-1, for host cell invasion), ttrC (tetrathionate reductase, fitness advantage), ssaQ (SPI-2 T3SS; secretion system apparatus protein), mgtC (SPI-3 intracellular proliferation inside macrophages, Mg²⁺ transporter), misL (SPI-3, T5SS-secreted (autotransported) adhesins, involved in intramacrophage survival), spi4R and spi4D (encodes a T1SS), sopB (SPI-1, SPI-5-T3SS secreted effector Salmonella outer protein B for bacterial internalization), pip (SPI-5, pathogenicity island protein for intestinal mucosal fluid secretion and inflammation), hilA (SPI-1-T3SS, hyperinvasive locus the expression of invasion) and stn (Salmonella enterotoxin). In addition to these potential virulence genes, the S. Uganda serovar had pefA that encodes fimbria-associated virulence. The possession of these virulence encoding genes would suggest that the NTS serovars investigated in the current study have the ability to cause enteric salmonellosis in humans. Many of these genes have been reported to be present in S. Typhi. In this study, all the serovars were negative for the plasmid virulence factor encoding gene spvC. Some of the studies indicate importance of this gene for the survival and proliferation of NTS inside the reticuloendothelial cells and associated with bacteraemia in humans^18,19.

To our knowledge, S. enterica serovars Takoradi, Tananarive and Uganda have not yet been reported from India. S. Takoradi has been reported from poultry slaughterhouses in Korea²⁰, and birds in Scotland²¹. S. Tananarive has been isolated from humans²² and food animals ( https://www.fao.org/4/i1547e/i1547e00.pdf , https://www.bvmj.bu.edu.eg/issues/25-2/8.pdf). S. Uganda caused a foodborne outbreak in China²³ and was also identified from turkeys in Canada²⁴, cattle and mink in USA^25,26, camels in Nigeria²⁷, and ducks in Trinidad²⁸.

Our findings highlight the risks associated with new Salmonella serovars with virulence potential and antimicrobial resistance in foods. Considering the public health risks associated with food contamination, constant surveillance and stringent control measures are needed at the production level and also along the food chain.

Financial support & sponsorship

The study was supported by the fund received from ICMR-task force project “Surveillance of Food Borne Pathogen from Northeast India” [Grant No. 5/8-I(3)/2019-20-ECD-II(Part-G)].

Conflicts of Interest

None.

Use of Artificial Intelligence (AI)-Assisted Technology for manuscript preparation

The authors confirm that there was no use of AI-assisted technology for assisting in the writing of the manuscript and no images were manipulated using AI.

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Salmonella enterica serovars Takoradi, Tananarive and Uganda from foods in Tripura, their virulence & antimicrobial resistance

Financial support & sponsorship

Conflicts of Interest

Use of Artificial Intelligence (AI)-Assisted Technology for manuscript preparation

References

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