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- DOI 10.18231/j.ijmmtd.2022.002
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Non Typhoidal Salmonellae and its aetiological spectrum-An overview with Indian perspective
- Author Details:
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Beena Antony *
Introduction
Non Typhoidal Salmonellae (NTS) which excludes S.Typhi & S.Paratyphi- is emerging as a major health problem across the globe. Salmonellae species are widely distributed in the environment and commonly found in farm effluents, human sewage as well as any material that is subjected to faecal contamination. These infections are also acquired through contact with pet animals or from veterinary clinics, zoological gardens, farm environments as a part of occupation. NTS species are mainly responsible for the food borne infections, gastroenteritis acquired through direct or indirect animal contact or by consumption of foods such as meat, sea foods, poultry products, leafy vegetables. Salmonellosis in animals always presents a potential zoonotic threat as these infected animals serve as a source of infections to humans. Subclinical infection in farm animals may lead to the contamination of meat, eggs or milk. It can also cause secondary contamination of fruits and vegetables fertilized or irrigated with water containing faecal wastes. Bovine Salmonellosis manifests clinically resulting in septicemia, acute or chronic enteritis and abortion. Hence, Salmonellosis in farm animals will cause a huge economic burden to the farmers for the management of these infections.
There are many contributory factors in India for the development of NTS infections such as occupation, geographic and climatic conditions. Agriculture being the main occupation in India, contact with farm animals and inadequate sanitary conditions occur very often. Poultry and dairy farming are two important means of livelihood for numerous people in India. Indian peninsula is surrounded by water bodies such as lakes, river, sea, hence fish and seafood are used as a common accompaniment.
Many species of NTS were reported to cause extra intestinal, invasive infections such as meningitis, septicaemia, bacteremia, septic arthritis as reported by various investigators from India. The severity of the NTS infection may vary from self limiting diarrhoeal diseases to fatal invasive infections which are more commonly found in immunocompromised patients or those who are with underlying diseases. In addition, many gastrointestinal outbreaks due to consumption of diverse foods were also documented in the literature.
Genus Salmonella includes more than 2500 serotypes which are potential human and animal pathogen. Taxonomy of Salmonella is complicated and undergoes periodical revisions. The designation of Salmonella serovars got the present Nomenclature status as adopted in WHO International Centre for Salmonella and the Centres for Disease Control and Prevention (CDC) which use shortened serovar nomenclatures. For example, S.enterica serotype typhimurium may be written as Salmonella Typhimurium for convenience. According to this, the name of the genus is written in italics but not the serotype name which starts with a capital letter.
In this overview, an attempt is made to compile the mushrooming, documented reports regarding gastroenteritis, extra intestinal infections and outbreaks due to NTS from Indian subcontinent for the last 5 decades , searching the available databases. The documented reports of NTS from India are shown in [Table 1]. As NTS infections are not notifiable and many of the isolates are not serotyped, this may be an underestimated data. All these reports are arranged in the alphabetical order of the Salmonella Serotypes, each report in the chronological order of occurrence and citing the reference number in the order that appears in the text.
NTS Infections Reported from India
As reported in most of the studies from other countries and also the results of our findings, S.Typhimurium was the most frequenly encountered NTS in India followed by S.Senftenberg and S.Weltevreden. S.Typhimurium mainly causes outbreaks of Gastroenteritis, primarily in children. [1], [2], [3], [4], [5], [6] Few extra intestinal manifestations are also reported which include neonatal septicemia [7] neonatal septic arthritis [8] scalp abscess [9] and meningitis. [10] In our study one isolate of S.Typhimurium was obtained from a suspected case of bacteremia. We have encountered a sporadic outbreak of food poisoning associated with S.Typhimurium due to consumption of squid, during a get together in a reputed restaurant in Mangalore.
S.Senftenberg was the second most common NTS reported from India. It was responsible for Extraintestinal infections such as Septicemia[11], [12] Lung Abscess, [13] Pleuro pulmonary infection [14] Empyema, [15] and ear infection.[16] Many outbreaks were also documented, especially in neonatal or paediatric wards. [17]
S. Weltevreden is another predominant NTS responsible for outbreaks of Gastroenteritis and foodpoisoning.[18], [19], [20] An outbreak investigation of S.Weltevreden foodpoisoning in a tea garden of Assam was reported by Saikia et al [21] Extra intestinal infections include enteric fever like infection, cholecystectomy surgical site infection. [22] Sepsis in two newborns was reported by Patil [23] and ulcerative skin lesions by Desikan [24] An outbreak of food poisoning due to S. Weltevreden involving many nursing students had been occurred in our institute due to a non vegetarian dish, in a get togthrer. [25]
E Enteritidis is usually causing extra intestinal manifestations and reported as aetiological agents of Septic arthritis, [26] complicated Aortic aneurism, meningitis, [27] polyserositis, arthritis following trauma in a child with Thalassemia Major. [28] Gastroenteritis due to S.Enteritidis was reported by Vijaya et.al.[29] We also experienced a small outbreak due to S.Enteritidis, probably associated with consumption of egg.
Rarely encountered NTS
S.Newport & S. Worthington are also reported from India, but not so frequently like other NTS. S Newport was mainly causing Gastrointestinal epidemics[30], [31] and few Extraintestinal infections such as Neonatal septicemia. [32] S. Worthington was more commonly encountered in Extraintestinal manifestations such as septicemia, meningitis[33], [34], [35] An Outbreak of S.Worthington in a neonatal ward in a general hospital was reported by Muley et.al. [36]
S.Oranienberg was responsible for Gastrointestinal outbreaks.[37], [38] S.Dublin was exclusively isolated from invasive infections like meningitis. [39] Dias et.al reported S.Dublin bacteremia mimicking Enteric fever from our institute. [40] S.Bareilly was isolated from pediatric infections, [41] neonatal poly arthritis and septicemia [42] by various investigators. It was reported as the second highest organism isolated from faecal samples in Goa by Verenkar. Two case reports on S.Virchow causing invasive infections such as meningitis, [43] septicemia in an infant [44] were also documented in the literature. Devi from Manipal and Jesudason from Vellore isolated S.Agona from Gastroenteritis cases. [45], [46] In our experience one strain of Agona was isolated from a gastroenteritis case.
Panhotra et.al reported an outbreak of S.Anatum infection from a premature nursery at Chandigarh. [47] We could isolate S.Anatum from a bacteremia case in our institute. The rare isolates of NTS reported from our country include fatal gastroenteritis in an infant with microcephaly due to S.Arizona by Mahajan et.al, [48] S.Bornheim causing UTI in a diabetic patient with aplastic anemia, [49] S.Branderup, [50] S.Cerro causing pyaemia, [51] S.Havana from a case of neonatal meningitis. [52] S.Mbandeka, a rare serotype was isolated in Ambajogai, rural area by Fule and Kaundinya. [53] S.Newbrunswick causing infection in an old man was reported by Shriniwas in a hospital from Delhi. [54] Other unique strains of NTS reported include S.Roan from bacteraemia, [55] S.Tamilnadu from a gastroenteritis in a child. [56] A case of invasive gastroenteritis with acute kidney injury and hemiplegia was reported by Ballal et.al due to S.Wangata.[57] Three rare isolates such as S.Augstenborg, S.Indiana, S.Regent were reported by Basu et.al for the first time in India. In a 16 year study Basu et al described the prevalence of various new Salmonella serotypes in India. [58] A very interesting finding in this study was that out of 99 serotypes obtained from 8027 strains of Salmonella, 13 were isolated only from man and 49 exclusively from animals with S.Weltevreden being the commonest serotype. S.Typhimurium was the commonest species isolated from animals. Jain P et.al reported a blood and urine culture positive bacteremia by S.Choleraesuis for the first time in India. [59] A rare case of Pyogenic meningitis caused by Salmonella choleraesuis var. Kunzendorf had been reported by Prakash and Ray in 1970.[60]
A South Indian Study describing the Seroprofiling of NTS isolated from Gastroenteritis, few rare serovars were reported which included S.Bovismorbificans, S.Schleissheim, S.Wangata and Ciprofloxacin resistant S.Kentucky. More recently, a case of Gastroenteritis in a 10 year old child , complicated by Severe Acute Kidney Injury and neurological dysfunction due to a new NTS species S.Decatur was reported by Krishnamurthy & Mandal from Pondicherry. [61] Occasional reports regarding the changing pattern of Salmonella serovars from various geographical areas also appeared in the literature. Another rare serotype S.Wien, one of the epidemic clones which spread from North Africa through Europe in the 1970s was isolated from 10 cases of gastroenteritis in our hospital. [62]
For the last 10 years duration, 145 NTS were isolated from feces and 8 strains of NTS from suspected cases of bacteremia, including 4 outbreaks occurred in our institute was presented in GISICON, 2021. S.Oslo was not so commonly reported from India. However in the recent past there was a sudden change in the pattern of NTS where we observed the emergence and prevalence of S.Oslo for a certain period of time. Rare serotypes such as S.Bareilly, S.Anatum, S.Infantis, S.Hadar, S.Dunkuwa and S.Kentucky were also obtained from Gastroenteritis cases during this period. Prevalence of S.Oslo was reported by Ballal et.al in Cancer patients, from a neighbouring district of Mangalore, Dakshina Kannada.[63]
Emergence of multi drug resistance in NTS strains is a major concern nowadays. Many investigators reported MDR Salmonellae from various States in India.[64] A detailed Review describing the various mechanisms involved in the resistance in NTS is done by Bhaskar & Harish from Pondicherry.
Conclusions
The documented reports from Indian Subcontinent emphasizes the role of NTS in diverse clinical infections and the possible links of transmission. There are many contributory factors in our country for the occurrence of these infections. As NTS is widely distributed in animals and sea foods, it is very essential to adopt stringent quality measures in the poultry, fish, dairy and meat processing units. A structured questionnaire to the patients and the family, Vaccination of Farm animals and inclusion of NTS in the list of notifiable diseases will definitely be helpful to understand the magnitude of the problem. Many of the NTS species are biochemically similar, hence serotyping of all the isolates are to be made mandatory. In addition, strategies should be formulated by health education and public awareness program to sensitize the population and thereby minimising the incidence of NTS in our country.
|
Serotype |
Clinical Manifestation |
Author |
Ref No. |
|
S.Agona |
Gastroenteritis |
DeviJN et.al(1985)83 |
|
|
Gastroenteritis |
Jesudasan M,(1988) |
||
|
S.Anatum |
Outbreak in Chandigarh |
Panhotra et.al, (1979) |
|
|
S.Arizona |
Fatal Gastroenteritis |
Mahajan et.al, (2003) |
|
|
S.Augstenborg |
First case from India |
Basu S et al., 1972 |
|
|
S.Bareilly |
Paediatric Infections |
Aggarwal et.al, (1983) |
|
|
Septicaemia |
Gupta et.al, (1997) |
||
|
S.Bornheim |
UTI in DM & Aplastic Anaemia |
Snehalatha et.al (1992) |
|
|
S.Bovismorbificans |
Gastroenteritis |
Ballal |
|
|
S.Braenderup |
First case from India |
Devi. JNS et.al, (1988) |
|
|
S.Cerro |
Pyaemia |
Bhore et.al (1980) |
|
|
S.Choleraesuis |
Isolation from blood & urine |
Jain P et.al,2014 |
|
|
S. Decatur |
Gastroenteritis |
Krishnamurthy &, Mandal2020 |
|
|
S.Dublin |
Meningitis |
Diwan et.al (1997) |
|
|
Bacteremia |
Dias et.al (2009) |
||
|
S.Enteritidis2 |
Bilateral septic Arthritis |
John et.al (1993) |
|
|
Meningitis |
Varaiya et.al (2001) |
||
|
Arthritis |
Behera et.al (2010) |
||
|
Gastroenteritis |
Vijaya et.al, (2012) |
||
|
S.Havana |
Meningitis |
Menon et.al, (1994) |
|
|
S.Indiana |
First report from India |
Basu et.al., 1975 |
|
|
S.Infantis |
gastroenteritis |
Taneja |
|
|
S.Kentucky |
gastroenteritis |
Ballal |
|
|
S. Kunzendorf |
Pyogenic Meningitis |
Prakash & Ray, 1970 |
|
|
S.Mbandeka |
Isolation of a rare serotype |
Fule & Kaundinya, (1985) |
|
|
S.New Brunswick |
Infection in an old man |
Shriniwas et.al (!(1983) |
|
|
S.Newport |
Nursery Outbreak |
Kumari S et.al (1980) |
|
|
Epidemic |
Dravid et.al (1989) |
||
|
Neonatal Septicaemia |
Rao MR et al, (1991) |
||
|
S.Oranienburg |
Gastroenteritis |
Aggarwal et.al (1980) |
|
|
Outbreak in NICU |
Mehta et.al (1982) |
||
|
S.Oslo |
Gastroenteritis |
Ballal |
|
|
S.Regent |
First report from India |
Basu et.al , 1973 |
|
|
S.Roan |
Bacteraemia |
Sundaram et.al (1983) |
|
|
S.Schleissheim |
gastroenteritis |
Ballal |
|
|
S.Senftenberg |
Nosocomial outbreak |
Narang et al (1985) |
|
|
Septicemia |
Saigal et.al (1989) |
||
|
Septicaemia |
Gupta P et.al, (1993) |
||
|
Lung Abscess |
Gupta JP, (1994) |
||
|
Pleuropulmonary Infection |
Nair D, (1999) |
||
|
Hospital acquired Empyema |
Ramanathan et.al (2000) |
||
|
Ear Infection |
Bairy I et.al (2000) |
||
|
S.Tamilnadu |
Gastroenteritis in a child |
Nath ML et.al (1970) |
|
|
S.Thompson |
gastroenteritis |
Taneja |
|
|
S.Typhimurium |
Nosocomial epidemic |
Puri et.al, (1980) |
|
|
Outbreak of gastroenteritis |
Bhat & Macaden(1983) |
||
|
Outbreak in Paediatric ward |
Chaturvedi et.al, (1985) |
||
|
Outbreak in Solapur |
Fule et.al (1988) |
||
|
Protracted diarrhoea in infants |
Koshoo et.al (1990) |
||
|
Neonatal septicaemia |
Rao PS (1993) |
||
|
Nosocomial outbreak |
Mahajan R et.al, (1995) |
||
|
Neonatal septic arthritis |
Sarguna &Lakshmi,(2005) |
||
|
Scalp Abscess |
Baliga S et.al(2011) |
||
|
Meningitis in infancy |
Adhikary R,(2013) |
||
|
S.Virchow |
Meningitis in an infant |
Sachdeva et.al(1963) |
|
|
Sepsis in an infant |
Randhawa et.al(2006) |
||
|
S.Wangata |
Invasive Gastroenteritis |
Ballal et.al(2015) |
|
|
|
Outbreak of Gastroenteritis |
Y.K.Chitkara,M K Gill(1976) |
|
|
Outbreak of food poisoning |
Aggarwal,(1985) |
||
|
Post cholecystectomy surg.site inf. |
Ashok R.et.al,(2005) |
||
|
Sepsis in 2 Newborns |
Patil BA et.al,(2006) |
||
|
Sporadic outbreak of food poisoning |
Antony.B.et.al,(2009) |
||
|
Ulcerative skin lesion |
DesikanP et.al,(2009) |
||
|
Outbreak of food poisoning |
Priyanka Jain, (2015) |
||
|
Outbreak in Tea Estate |
Saikia et.al, (2015) |
||
|
S.Wien |
Gastroenteritis -10 cases |
Antony B.et.al, (2009) |
|
|
S.Worthington |
Meningitis & septicaemia |
Ayyagari et.al, (1990) |
|
|
Outbreak of Neonatal septicaemia |
Rodrigues et.al, (1994) |
||
|
Outbreak of Neonatal Meningitis |
Udani et.al, (1999) |
||
|
Neonatal outbreak |
Muley et.al ,(2004) |
Conflicts of Interest
The authors declare no potential conflict of interest with respect to research, authorship, and/or publication of this article.
Source of Funding
None.
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