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  Table of Contents  
Year : 2016  |  Volume : 34  |  Issue : 3  |  Page : 387-389

Outbreak of enteric fever due to Salmonella Paratyphi A variety durazzo (2,12:a:-) in a hilly region of North India: A report of 43 cases

1 Department of Microbiology, Indira Gandhi Medical College, Shimla, Himachal Pradesh, India
2 Department of Microbiology, All India Institute of Medical Sciences, New Delhi, India

Date of Submission21-May-2015
Date of Acceptance10-Jan-2016
Date of Web Publication12-Aug-2016

Correspondence Address:
V Sharma
Department of Microbiology, Indira Gandhi Medical College, Shimla, Himachal Pradesh
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0255-0857.188366

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 ~ Abstract 

Enteric fever due to Salmonella Paratyphi A (SPA) is a global problem occurring as outbreaks at times. An unusual SPA (2,12:a:-) variety durazzo has been reported rarely. We report an outbreak of enteric fever due to this variety affecting 43 individuals. The blood samples grew unusual mucoid, lactose non-fermenting colonies with atypical biochemical reactions in sugar fermentation and amino acid decarboxylation. Isolates had sensitivity to ceftriaxone, chloramphenical, cotrimoxazole, intermediate susceptibility to ciprofloxacin and resistance to ampicillin and nalidixic acid. Identification was confirmed as SPA (2,12:a:-) at the National Salmonella Centre.

Keywords: Ampicillin, ciprofloxacin, durazzo, Salmonella Paratyphi A

How to cite this article:
Verma S, Sharma V, Mokta K, Thakur C, Angrup A, Singh D, Kanga A. Outbreak of enteric fever due to Salmonella Paratyphi A variety durazzo (2,12:a:-) in a hilly region of North India: A report of 43 cases. Indian J Med Microbiol 2016;34:387-9

How to cite this URL:
Verma S, Sharma V, Mokta K, Thakur C, Angrup A, Singh D, Kanga A. Outbreak of enteric fever due to Salmonella Paratyphi A variety durazzo (2,12:a:-) in a hilly region of North India: A report of 43 cases. Indian J Med Microbiol [serial online] 2016 [cited 2021 Mar 5];34:387-9. Available from:

 ~ Introduction Top

Enteric fever is a systemic illness caused by Salmonella enterica serotypes Typhi and Paratyphi. The Indian subcontinent and South East Asian regions hold the greatest disease burden. Every year, 22 million cases and 6,00,000 deaths are reported the world over. [1]

Recent reports on enteric fever have described outbreaks from the USA, India, Nepal. [1],[2],[3],[4] Outbreaks have been linked to consumption of fresh fruits and vegetables or eggs and poultry. Incidence of Salmonella Paratyphi A (SPA) is on the increase in the last two decades and antimicrobial susceptibility patterns demonstrate greater resistance to fluoroquinolones and sensitivity to ampicillin and cotrimoxazole. [5],[6] During the summer of 2014, the sub-Himalayan region witnessed an outbreak of enteric fever due to SPA variety durazzo (2,12:a:-) as per Kauffman-White scheme. There was unusual biochemical profile and antibiotic susceptibility pattern of the outbreak isolates. Since these were atypical observations, it needs documentation as any unexpected changes in the disease pattern may hint at genetic mutations in existing strain and need for constant vigil on emergence of new strains with erratic antibiotic sensitivities.

 ~ Case Report Top

A 39-year-old male adult presented with fever, malaise and loss of appetite of 1 week duration. Fever was continuous and documented up to 103°F on several occasions. There were no chills or rigors or accompanying sweating. General physical examination was normal except fever spiking to 101°F and respiratory rate of 26/min. Vital parameters were normal and biochemical parameters were within limits. Total leucocyte count was 16,500/cmm, neutrophils 49% and lymphocytes 46%. In the laboratory investigations for fever, urine culture was sterile. Blood culture obtained in brain heart infusion broth was incubated at 37°C; subculture at 24 h was sterile and that after 72 h grew mucoid lactose non-fermenting colonies on Mac Conkey agar [Figure 1]. Non-sporing, Gram-negative bacilli were seen on smear and were motile in hanging drop preparation. Colonies were catalase positive, oxidase negative, glucose was fermented with production of acid and gas. Indole, Voges-Proskauer test (VP), citrate utilization, urease, phenyl pyruvic acid tests were negative, methyl red test was positive and triple sugar iron gave alkaline slant and acidic butt with gas and without hydrogen sulphide production. The isolate was provisionally placed in family Enterobacteriaceae, Tribe Salmonelleae. For further confirmation sugar fermentation was done. Sucrose, maltose and mannose were fermented with acid and gas production whereas lactose, dulcitol and arabinose were not fermented. The isolate decarboxylated only ornithine but lysine and arginine were not attacked. There was failure to agglutinate the saline suspension using polyvalent A-G antisera (obtained from National Salmonella Centre, Central Research Institute (CRI), Kasauli) for Salmonella. Antimicrobial susceptibility testing was done by Kirby Baeur's disc diffusion test incorporating ampicillin (10 μg), cotrimoxazole (1.25/23.75 μg), chloramphenicol (30 μg), nalidixic acid (30 μg), ciprofloxacin (5 μg) and ceftriaxone (30 μg) discs and results interpreted as per CLSI guidelines 2014. [7] The isolate was sensitive to cotrimoxazole, chloramphenicol and ceftriaxone, showed intermediate susceptibility to ciprofloxacin and resistance to ampicilln and nalidixic acid.
Figure 1: Culture plate of Mac Conkey agar showing growth of lactose non-fermenting mucoid colonies after 24 h of incubation at 37°C

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During the following 7 months from March to September 2014, a total of 81 Salmonellae were isolated from blood samples of clinical suspects of enteric fever or pyrexia of unknown origin. These included 17 Salmonella Typhi and 64 SPA. Of the SPA, 43 were similar in morphology, biochemical profile and serotype and had same antimicrobial sensitivity pattern as the index case indicating same strain. These 43 subjects included 24 males and 19 females. Age ranged between 1 and 74 years; <11 years (10), 11-30 years (20), 31-50 years (10) and three patients more than 50 years of age. The month wise distribution included March (3), April (2), May (2), June (19), July (13), August (1) and September (3). Every sixth isolate was dispatched to the Indian National Salmonella Centre, CRI, Kasauli, for antigenic serotyping. Isolates were confirmed as SPA (2,12:a:-) which as per the Kauffman-White scheme is the SPA variety durazzo.

The patients were instituted antimicrobial therapy in accordance with the sensitivity profile and patients recovered completely.

 ~ Discussion Top

Enteric fever is a disease prevalent worldwide and of major health concern. In the west, it is reported in travellers returning from endemic countries and in the developing countries it is the leading cause of pyrexia of unknown origin. Salmonella Typhi remained the predominant serotype till the 1990s but since then serotype Paratyphi A has shown rising trends. [5],[6] Institution of vaccine against Salmonella Typhi does not provide protection against the Paratyphi A serotype and thus accounts for increase in its disease association. [8] A recent study from Delhi documented an outbreak due to SPA. [4] Lately, uncommon serotypes of Salmonella like S. Cerro, S. Mbandaka, S. Stanlep, S. Welterverden, S. Litchinfield, S. Javiana, S. Poona and SPA var durazzo, etc., have been documented. [2],[9]

An unusual outbreak of food poisoning due to SPA var. durazzo (2,12:a:-) is previously reported only from Yavatmal, Maharashtra, India, in 1995. [10] The source tracing implicated consumption of contaminated vegetarian food infecting 33 patients. SPA var. durazzo was recovered from faecal samples of 12 subjects. [10] In the present study, the primary presentation was fever and majority patients were treated on outdoor basis. Available data was insufficient to trace the cases to any common source, neither were the cases confined to a localized area.

On the basis of morphology and biochemical reactions, the isolates were identified in Family Enterobacteriaceae, Tribe Salmonelleae. There was failure to agglutinate the isolates with antisera in the laboratory and sugar fermentation and amino acid decarboxylation reactions were atypical thus confirmation of identity of representative samples as SPA (2,12:a:-) was done at CRI, Kasauli. Presence of certain fimbriae account for untypeable Salmonella isolates since their autoaggregation could mask the serotype profile while performing standard agglutination tests to identify flagellar or lipopolysaccharide O antigens. These thin aggregative fimbriae, collectively named GVVPQ fimbriae are encoded by the agfA gene and have been demonstrated in many Enterobacteriaceae and SPA var. durazzo. [11] The SPA var. durazzo differs from SPA only in being deficient in O-antigen 1. [8],[12]

The current antimicrobial susceptibility pattern of SPA reported from this region reveals sensitivity to ampicillin, cotrimoxazole, chloramphenicol and ceftriaxone and resistance to ciprofloxacin and nalidixic acid. [13],[14] The isolates obtained during the present outbreak differed as all 43 isolates were resistant to ampicillin and had intermediate resistance to ciprofloxacin. Single point mutations are associated with decreased susceptibility to ciprofloxacin and multiple mutations relate to complete resistance to fluroquinolones. Such mutations are induced under antibiotic selective pressure and may be unaccounted [15],[16] The inability to elucidate such mechanisms was a limitation of this study. But the observations made herein cautions to observe changing biochemical profile and sensitivity of Salmonella spp. as antibiotic susceptibility patterns keep varying under antibiotic selective pressure and documentation of epidemiological profile guides therapeutic strategies.


We sincerely thank The Director and Dr. Yashwant Kumar, technical supervisor, CRI, Kasauli, Himachal Pradesh, for very kindly confirming the identity of the isolates.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

 ~ References Top

Dahiya S, Kapil A, Kumar R, Das BK, Sood S, Chaudhry R, et al. Multiple locus sequence typing of Salmonella typhi, isolated in north India - A preliminary study. Indian J Med Res 2013;137:957-62.  Back to cited text no. 1
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Jackson BR, Griffin PM, Cole D, Walsh KA, Chai SJ. Outbreak-associated Salmonella enterica serotypes and food commodities, United States, 1998-2008. Emerg Infect Dis 2013;19:1239-44.  Back to cited text no. 2
Gal-Mor O, Suez J, Elhadad D, Porwollik S, Leshem E, Valinsky L, et al. Molecular and cellular characterization of a Salmonella enterica serovar Paratyphi A outbreak strain and the human immune response to infection. Clin Vaccine Immunol 2012;19:146-56.  Back to cited text no. 3
Thong KL, Nair S, Chaudhry R, Seth P, Kapil A, Kumar D, et al. Molecular analysis of Salmonella Paratyphi A from an outbreak in New Delhi, India. Emerg Infect Dis 1998;4:507-8.  Back to cited text no. 4
Micoli F, Rondini S, Gavini M, Lanzilao L, Medaglini D, Saul A, et al. O:2-CRM (197) conjugates against Salmonella Paratyphi A. PLoS One 2012;7:e47039.  Back to cited text no. 5
Singhal L, Gupta PK, Kale P, Gautam V, Ray P. Trends in antimicrobial susceptibility of Salmonella typhi from North India (2001-2012). Indian J Med Microbiol 2014;32:149-52.  Back to cited text no. 6
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CLSI. Performance Standards for Antimicrobial Susceptibility Testing, 24 th Informational Supplement. M100-S24. Wayne, PA: Clinical and Laboratory Standards Institute; 2014.  Back to cited text no. 7
Teh CS, Chua KH, Thong KL. Paratyphoid fever: Splicing the global analyses. Int J Med Sci 2014;11:732-41.  Back to cited text no. 8
Fule RP. Changing trend of Salmonella infection. Indian J Med Sci 1997;51:221-5.  Back to cited text no. 9
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Fule RP, Ingole KV, Jalgaonkar SV, Moon BU. Outbreak of food poisoning due to Salmonella Paratyphi A var durazzo (2,12:a:-) in Yavatmal (Maharashtra) in May 1995. Indian J Med Res 1996;103:74-6.  Back to cited text no. 10
Doran JL, Collinson SK, Burian J, Sarlós G, Todd EC, Munro CK, et al. DNA-based diagnostic tests for Salmonella species targeting agfA, the structural gene for thin, aggregative fimbriae. J Clin Microbiol 1993;31:2263-73.  Back to cited text no. 11
Johnson EM. Somatic antigen 2 inheritance in Salmonella groups B and D. J Bacteriol 1967;94:2018-21.  Back to cited text no. 12
Verma S, Thakur S, Kanga A, Singh G, Gupta P. Emerging Salmonella paratyphi A enteric fever and changing trends in antimicrobial resistance pattern of Salmonella in Shimla. Indian J Med Microbiol 2010;28:51-3.  Back to cited text no. 13
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Garg A, Verma S, Kanga A, Singh D, Singh B. Antimicrobial resistance pattern and in vitro activity of azithromycin in Salmonella isolates [corrected]. Indian J Med Microbiol 2013;31:287-9.  Back to cited text no. 14
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Dutta S, Das S, Mitra U, Jain P, Roy I, Ganguly SS, et al. Antimicrobial resistance, virulence profiles and molecular subtypes of Salmonella enterica serovars Typhi and Paratyphi A blood isolates from Kolkata, India during 2009-2013. PLoS One 2014;9:e101347.  Back to cited text no. 15
Dahiya S, Kapil A, Lodha R, Kumar R, Das BK, Sood S, et al. Induction of resistant mutants of Salmonella enterica serotype Typhi under ciprofloxacin selective pressure. Indian J Med Res 2014;139:746-53.  Back to cited text no. 16
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