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 Table of Contents  
ORIGINAL ARTICLE
Year : 2017  |  Volume : 20  |  Issue : 2  |  Page : 132-138

Changing epidemiology and antimicrobial resistance pattern of Vibrio cholerae isolates at a tertiary care health laboratory in North India (2011–2015)


Department of Microbiology, Maulana Azad Medical College and Lok Nayak Hospital, New Delhi, India

Date of Web Publication14-Nov-2017

Correspondence Address:
Bhanu Mehra
Department of Microbiology, Maulana Azad Medical College and Lok Nayak Hospital, New Delhi - 110 002
India
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DOI: 10.4103/tjmr.tjmr_17_17

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  Abstract 

Background: Vibrio cholerae is a common bacterial enteropathogen causing acute diarrheal disease in the developing world. Marked variations in epidemiology and in in vitro susceptibility of isolates are commonly observed, and emerging and progressive resistance to various classes of antibiotics is frequent. The present research was undertaken to document the epidemiological profile of cholera cases in Delhi and surrounding areas and to monitor the antibiotic resistance patterns of this enteropathogen across the study years. Materials and Methods: The present retrospective analysis was conducted over a 5-year period (2011–2015) at a tertiary care medical center in New Delhi, India. A cumulative 11,570 diarrheic/dysentric fecal samples received in the laboratory were processed for common enteropathogens by standard bacteriological methods. Any suspected V. cholerae colonies were identified by standard biochemical reactions, and serological confirmation was obtained by agglutination using specific antisera. Antimicrobial susceptibility profile of the isolated strains was assessed by Kirby–Bauer's disc diffusion technique and in accordance with the Clinical and Laboratory Standards Institute guidelines. Results: V. cholerae was isolated in 2.4% of the stool samples, with V. cholerae O1 serotype Ogawa being the most prevalent serotype, and a rise in the number of cholera cases was evident during monsoon season each year. While resistance to nalidixic acid and ampicillin was consistently high during the study period, aminoglycoside resistance showed variance and fluctuations across the study years. Further, a significant rise was seen in resistance to ciprofloxacin and cefotaxime. Conclusions: Our findings suggest high levels of antibiotic resistance among the circulating V. cholerae strains in this part of the country, with fluctuations in antibiograms being commonly noted. Therefore, active and continuous community surveillance of changing epidemiology and antimicrobial resistance profile of this enteropathogen is of utmost importance.

Keywords: Antibiogram, antimicrobial resistance, cholera, diarrhea, epidemiology, India, Vibrio cholerae


How to cite this article:
Uppal B, Mehra B, Panda PS, Kumar SK. Changing epidemiology and antimicrobial resistance pattern of Vibrio cholerae isolates at a tertiary care health laboratory in North India (2011–2015). Trop J Med Res 2017;20:132-8

How to cite this URL:
Uppal B, Mehra B, Panda PS, Kumar SK. Changing epidemiology and antimicrobial resistance pattern of Vibrio cholerae isolates at a tertiary care health laboratory in North India (2011–2015). Trop J Med Res [serial online] 2017 [cited 2017 Nov 18];20:132-8. Available from: http://www.tjmrjournal.org/text.asp?2017/20/2/132/218207


  Introduction Top


Cholera is an acute infectious severe diarrheal illness caused by the enteric bacterial pathogen Vibrio cholerae. It is a major public health concern globally and a leading cause of bacterial diarrhea in developing nations of Asia and Africa.[1],[2],[3] The causative organism is essentially a food and waterborne Gram-negative bacillus, the peak transmission rates of which coincide with monsoon season and outbreaks are frequently noted in areas of inadequate sanitation services and poor access to clean water supply.[4],[5],[6]

The profuse and painless watery diarrhea associated with cholera often leads to severe and life-threatening dehydration and electrolyte disturbances.[7] Oral and intravenous rehydration and electrolyte repletion is, therefore, the mainstay of management of this disease. The role of antimicrobials in the treatment of cholera is essentially adjunctive but often warranted particularly in severe cases. A rationale use of efficacious antibiotics not only shortens the duration of diarrhea, but also reduces the volume of diarrheal stools, the duration of fecal excretion of Vibrio, and the fatality associated with the diarrheal disease.[7],[8] In addition, antimicrobials shorten the length of hospital stay and curb hospital-related costs as was evident in the cholera epidemic in Peruvia in 1991.[9]

Vibrio cholerae was initially sensitive to several antimicrobials for a long period with a very low resistance rate documented in a global survey in 1976.[10] However, the extensive injudicious and prophylactic utilization of antimicrobials, as well as their use in animal husbandry, has changed the scenario.[11],[12] Changing antibiogram of V. cholerae strains as well as emergence of multidrug-resistant isolates is being frequently reported from India and other parts of the world.[13],[14],[15],[16],[17],[18],[19],[20] Furthermore, a diversity and variation in the prevalence of causative serovars as well as their susceptibility profiles is observed in different geographical regions and over varying time periods. Therefore, therapeutic choices must be guided by local antibiograms generated by a continuous vigilance of resistance patterns of this pathogen.

Keeping this in view and the limited availability of contemporary data in this regard over the last few years, the present study was undertaken as an attempt to document the epidemiological and antimicrobial susceptibility profile of V. cholerae strains isolated at an Indian tertiary care hospital over a 5-year period (2011–2015) and to analyze the changing trends in resistance patterns across these years.


  Materials and Methods Top


Study design and site

The present retrospective analysis was conducted over a 5-year period, from January 2011 to December 2015, at the Department of Microbiology of a tertiary care health institute in New Delhi, India. The study protocol was approved by the Ethics Committee of the Institution.

Collection of samples

A total of 11,570 consecutive stool samples, collected from diarrheic/dysentric patients presenting to the outpatient departments, as well as those admitted in various inpatient units of the hospital, were processed during this period. Fresh fecal samples were collected from patients of all age groups and transported immediately to the laboratory where they were processed as per the recommended standard microbiological methods to detect the common diarrheagenic enteropathogens.[21],[22]

Isolation and identification of Vibrio cholerae

Stool samples were observed for macroscopic findings, and a hanging drop preparation was made and examined for darting motility. In addition, a stool wet mount examination for red blood cells, pus cells, cysts, and trophozoites of parasites was performed. The stool samples were streaked onto MacConkey agar, thiosulfate-citrate-bile salts-sucrose agar (TCBS), and deoxycholate citrate agar (DCA), and incubated at 37°C for 18–24 h. A part of the stool samples was enriched in alkaline peptone water and selenite F broth at 37°C for 6 h, and subsequently subcultured onto TCBS and DCA, respectively. Any typical V. cholerae-like colonies were further characterized by conventional biochemical tests, and organisms with biochemical reactions resembling those of Vibrio were identified serologically by slide agglutination test employing specific antisera (polyvalent O1, O139, and monospecific Ogawa and Inaba antisera) obtained from Denka Seiken Company Limited, Tokyo, Japan.

Antimicrobial susceptibility testing

All the isolated strains of V. cholerae were tested for in vitro susceptibility to different antimicrobials employing the agar disc diffusion technique as described by Bauer et al. and in accordance with guidelines defined by the Clinical and Laboratory Standards Institute (CLSI).[23],[24] A panel of six antimicrobial agents was used for susceptibility testing. These included ampicillin (10 μg), nalidixic acid (30 μg), ciprofloxacin (5 μg), gentamicin (10 μg), amikacin (10 μg), and cefotaxime (30 μg). The strains were characterized as susceptible, intermediate susceptible, or resistant based on the diameter of zone of inhibition around each antibiotic-impregnated disc and its comparison with the interpretive criteria as recommended by the CLSI guidelines.[24] American Type Culture Collection Escherichia coli 25922 was used as the control strain for disc diffusion. Isolates showing intermediate susceptibility to a particular antimicrobial agent were considered as resistant for the purpose of analysis.

Statistical analysis

Data analysis was performed using the Epi info statistical software, version 3.5.3, Centers for Disease Control and Prevention, Atlanta, GA, USA. Descriptive statistics were expressed in terms of proportions and figures. Any differences in resistance patterns across the years were determined using Fisher's exact test and Chi-square test, and a two-tailed P < 0.05 was considered to denote a statistically significant difference.


  Results Top


Isolation rate of Vibrio cholerae

Of the cumulative 11,570 diarrheal stool samples processed during the 5-year period, V. cholerae was isolated in 283, giving an overall positive yield of 2.4%. The annual detection rates of V. cholerae were 2.1% (47/2233), 1.3% (28/2150), 3.7% (86/2298), 2% (52/2549), and 2.9% (70/2340) for the years 2011, 2012, 2013, 2014, and 2015, respectively. The number of V. cholerae strains isolated each year during the study duration is depicted in [Figure 1].
Figure 1: Year-wise distribution of cholera cases and annual serogroup distribution profile of Vibrio cholerae strains isolated from stool samples (2011–2015)

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Seasonal trends

Seasonal variations were noted in the isolation frequency of V. cholerae as is evident from [Figure 2].
Figure 2: Month-wise distribution of cholera cases (2011–2015)

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Demographic profile of cholera cases

Two hundred and forty (84.8%) cholera patients in our study were below 15 years of age, with a large proportion of cases (114, 40.3%) being <5 years. Furthermore, among cholera-affected children <5 years of age, 36 (31.6%) were infants and two of the cases were reported in neonates aged 2 days and 7 days, respectively.

Serogroup and serotype distribution

Two hundred and seventy-seven (97.9%) V. cholerae isolates were confirmed as belonging to serogroup O1 while a small proportion of strains (6; 2.1%) failed to agglutinate with O1 and O139 antisera and were identified as non-O1/non-O139. Serotyping revealed all V. cholerae serogroup O1 strains isolated during this period to be serotype Ogawa. The annual serogroup distribution of these isolates between 2011 and 2015 is depicted in [Figure 1].

Antimicrobial resistance profile

A comparison of the antimicrobial resistance profile of V. cholerae strains across these years is summarized in [Table 1]. Analysis of antibiogram over this 5-year period revealed that the proportion of isolates resistant to nalidixic acid (94.3%–100%) and ampicillin (89.4%–100%) remained consistently high and stable during the study duration with no significant variance noted in resistance rates to these antibiotics during the years [Figure 3]. On the contrary, while strains were usually susceptible to ciprofloxacin during the initial period, subsequent years witnessed a significant rise in the rates of resistance to this antimicrobial (21.3%, i.e., 16/75 in 2011–2012 vs. 54.3%, i.e., 113/208 in 2013–2015; P < 0.0001). A similar trend was observed with cefotaxime with the proportion of resistant strains increasing dramatically from 16% (12/75) in 2011–2012 to 42.3% (88/208) in 2013–2015 (P < 0.0001). Furthermore, an interesting phenomenon was observed with regard to the patterns of aminoglycoside resistance among V. cholerae strains across the years. Amikacin resistance among V. cholerae isolates increased significantly from 19.1% (9/47) in 2011 to 40.4% (46/114) in 2012–2013 (P = 0.01), with peak resistance rates documented in 2013 [Figure 3]. Resistance to amikacin then fell in subsequent years such that the proportion of resistant V. cholerae strains in 2014–2015 was significantly lower (40.4%, i.e., 46/114 in 2012–2013 vs. 13.1%, i.e., 16/122 in 2014–2015; P < 0.0001). Gentamicin resistance showed a similar trend with resistance rates increasing from 21.3% (10/47) in 2011 to a peak of 38.6% (44/114) in 2012–2013 (P = 0.05) and then showing a significant decline to 23.8% (29/122) in the recent years (P = 0.02).
Table 1: Year-wise comparison of drug resistance pattern of Vibrio cholerae isolates (2011-2015)

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Figure 3: Trends in antimicrobial resistance pattern of Vibrio cholerae strains (2011–2015)

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  Discussion Top


Cholera has shown a constant endemicity in Delhi region since the last several years.[25],[26] In our study population, the incidence of V. cholerae-associated diarrhea was noted to vary from 1.3%–3.7%. High incidence in endemic areas has been reported by other studies and drastically higher detection rates are documented in outbreak situations.[17],[26],[27],[28]

As with previous studies, the number of cholera cases in our population started increasing from May–June onward, coinciding with the rise in environmental temperatures and a monsoon peak, and clustering of cases was documented each year as is evident by the month-wise distribution of cholera cases.[16],[29] In addition, few winter cases of cholera were also seen as has been previously reported by other researchers.[30]

Although cholera can affect people of all age groups and genders, high infection rates are notably reported among children. A group of researchers from Puducherry, India, observed that 40%–70% of V. cholerae isolates in their study were obtained from children aged 0–5 years.[29] Similarly, Sharma et al. found nearly 32.7% of cholera cases in Delhi and adjoining regions to occur in children aged <5 years.[31] They also observed that 16.2% of cholera cases that belonged to under 5 years' age group were in fact infants.[31] Our data concord these findings with infants contributing significantly to the burden of cholera cases among under-five children in our study. However, the proportion of infantile cases was much higher than what has been previously reported.[31] Moreover, while the recorded minimum age by Sharma et al. was 1 month, two cases in our study were reported in neonates aged 2 days and 7 days, respectively.[31] Neonatal cholera has also been previously reported and a possible causative role of contaminated holy water has been suggested.[32],[33] Unfortunately, the retrospective nature of our study did not allow us to explore and introspect the possible sources of infection in these cases.

Throughout the study duration, V. cholerae O1 remained the predominant circulating serogroup and not even a single strain of O139 was isolated from the stool samples. The predominance of V. cholerae serogroup O1, particularly the serotype Ogawa, has been reported in previous outbreaks from Kolkata and Chandigarh, and is well documented in Delhi region as well where it has been the main serotype responsible for cholera infections.[16],[13],[26],[27],[34] In addition, while the isolation of serotype Inaba has been described from various parts of the country, and the evidence of Ogawa to Inaba serotype interconversion and switching has been firmly established in Delhi in 2004–2006 by Das et al., none of the isolates in our study belonged to serotype Inaba.[15],[18],[35] Furthermore, non-O1 and non-O139 V. cholerae constituted only 2.1% of the total V. cholerae strains isolated from diarrheal stool samples and their isolation rates remained at a low level throughout the study period. Review of previous Indian literature has also revealed variable isolation rates of these serogroups with isolation frequencies ranging from 5% in Delhi during 1992–2000 to as high as 25.8% in Hubli, Karnataka, during the years 2000–2004.[34],[36] Though these serogroups are essentially associated with sporadic cases of diarrhea, keeping in view the fact that localized outbreaks due to non-O1 and non-O139 serogroups of V. cholerae have previously occurred and that these serogroups may play an important role in transferring resistance determinants to other serogroups, the significance of a careful laboratory surveillance of these pathogens cannot be underscored.[37],[38]

Rampant and indiscriminate use of antibiotics is the principal factor responsible for the emergence and increase in the prevalence of antimicrobial resistance among pathogenic bacteria. With reference to V. cholerae, various resistance patterns have been reported among strains isolated from different parts of the country and across the globe. The present study has demonstrated high levels of resistance to ampicillin and nalidixic acid, suggesting that these drugs are nearly impractical for therapeutic management of cholera. A study conducted at the Infectious Disease Hospital, Kolkata, from 1992 to 1997, noted a rising resistance to ampicillin and nalidixic acid among clinical isolates of V. cholerae from the year 1994 onward.[39] Another study of V. cholerae O1 isolates from acute diarrheal patients at a surveillance site and from different outbreak regions of Odisha showed that, while both Ogawa and Inaba strains were sensitive to ampicillin, nalidixic acid resistance was 100% among both the serotypes.[14] Circulation of ampicillin and nalidixic acid-resistant V. cholerae isolates has also been documented by several other researchers.[18],[15],[31],[40]

While the V. cholerae strains analyzed in our study showed nearly universal and consistently high resistance to ampicillin and nalidixic acid, the susceptibility patterns of V. cholerae isolates against the other tested antimicrobials have varied significantly across these years. We report a significant rise in ciprofloxacin resistance among V. cholerae isolates at our center. In variance to our findings, Chander et al. found only three V. cholerae isolates obtained between 1999 and 2007 (2/34, i.e., 5.9% in 2004 and 1/12, i.e., 8.3% in 2007) to be ciprofloxacin resistant.[16] Pal et al. observed V. cholerae O1 isolates in their study to show uniform sensitivity to ciprofloxacin.[14] In contrast, a similar study conducted in Kolkata during the same time frame reported ciprofloxacin resistance rates of 12.5% and 5.3%–36.7% for Inaba and Ogawa strains, respectively.[40] Das et al. from Delhi have also revealed a significant increase in ciprofloxacin resistance between 2001 and 2006 with sustained high resistance rates recorded in subsequent years at their center.[18],[41]

We have documented a rise and fall of aminoglycoside resistance among V. cholerae strains isolated at our center. A 9-year antibiogram of V. cholerae strains isolated at a tertiary care center in Chandigarh has shown the isolates to exhibit consistent sensitivity to gentamicin.[16] High gentamicin susceptibility has also been documented among outbreak strains from Odisha and West Bengal.[14],[15] While Das et al. revealed all the V. cholerae strains isolated during 2001–2006 to be gentamicin sensitive, a more recent published literature by the aforementioned authors has reported a sudden rise in gentamicin resistance in 2007 followed by a reversion to previous universal susceptibility to gentamicin in 2008–2009.[18],[41] The baseline aminoglycoside resistance among the isolated V. cholerae strains was high in our study, and though resistance rates to amikacin and gentamicin peaked in 2013 and subsequently declined, the proportion of isolates resistant to aminoglycosides is definitely higher than what is reported in previously published peer-reviewed medical literature, exception being a gentamicin resistance rate of 41.3% reported by Das et al.[41]

While the circulation of V. cholerae strains resistant to the commonly used enteric antimicrobials is well established across the globe, resistance to cephalosporins has rarely been encountered till date. High cefotaxime susceptibility among V. cholerae strains has been demonstrated by several researchers.[16],[41] A recent analysis of antimicrobial susceptibility patterns of V. cholerae isolated in 2008 and 2010 by Mandal et al. also found that the strains have largely retained their susceptibility to ceftriaxone.[29] Resistance to third-generation cephalosporins among V. cholerae strains was first reported in Argentina and more recently from Delhi, India.[31],[42] A more contemporary report has discussed about the isolation of V. cholerae strains resistant to ceftriaxone from three pediatric cholera cases from Puducherry.[43] Our study has also documented a dramatic increase in cefotaxime resistance over the recent years among V. cholerae isolates in this part of the country. Though cephalosporins are not yet recommended for therapeutic management of cholera, resistance to this class of antimicrobials among V. cholerae strains could have serious implications, keeping in view the epidemic potential of this organism.

Thus, we observed that a significant proportion of V. cholerae strains at our center are no longer sensitive to the commonly used antibiotics for the treatment of enteric infections. Furthermore, the current data have shown that fluctuations in antibiograms of clinical isolates of V. cholerae are common, and on comparing our findings with the published reports from Delhi and other parts of the country, we found that wide temporal and spatial variations are noted in the antibiotic treatment protocols and thus resistance patterns often differ by geographical region. This implies that antibiotic sensitivity pattern of V. cholerae cannot be predicted easily and it is imperative that each and every clinical isolate should be subjected to antimicrobial susceptibility testing. Furthermore, resistance patterns fluctuate with variations in the serogroups and this thus mandates not only a continuous vigilance of the changing resistance profiles of the isolates but also monitoring of cyclical changes in the circulating serovars and serotypes in the population.

Our analysis has provided the most recent insight into the epidemiology and resistance profile of V. cholerae strains isolated at one of the largest tertiary care institutes in North India. The study, however, is not without limitations. A major shortcoming was that it does not report the antibiotic minimum inhibitory concentration values for the V. cholerae isolates. In addition, genetic analysis of isolates to determine the genomic basis of resistance to various classes of antimicrobials and molecular studies to determine their clonal type was not performed. Moreover, the study was retrospective in nature and thus clinical information of the cholera-affected patients could not be retrieved.


  Conclusions Top


Our study has provided a more contemporary epidemiological profile of cholera in this region and has emphasized on the rapid gain and increase in the spectrum of antimicrobial resistance among clinical isolates of V. cholerae in this belt that has complicated the selection of antimicrobial therapy and rendered the treatment of cholera enormously difficult. The ever-evolving epidemiology of V. cholerae either in terms of predominant serogroups and serotypes or changing antimicrobial resistance patterns calls for close monitoring and perhaps establishment of a nationwide surveillance network. This will provide a baseline information to devise locally effective empirical antibiotic treatment regimens, and further antibiogram updates would be useful to revise these protocols from time to time.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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