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  Table of Contents  
Year : 2018  |  Volume : 36  |  Issue : 4  |  Page : 488-493

Multidrug-resistant Enterobacteriaceae colonising the gut of adult rural population in South India

1 Department of Microbiology, Pushpagiri Institute of Medical Sciences and Research Centre, Thiruvalla, Kerala, India
2 Department of Biostatistics, Pondicherry Institute of Medical Sciences, Kalapet, Puducherry, India
3 Department of Microbiology, Pondicherry Institute of Medical Sciences, Kalapet, Puducherry, India

Date of Web Publication18-Mar-2019

Correspondence Address:
Dr. Sherly Antony
Department of Microbiology, Pushpagiri Institute of Medical Sciences and Research Centre, Thiruvalla - 689 101, Kerala
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijmm.IJMM_18_388

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 ~ Abstract 

Background: Multidrug-resistant (MDR) colonisers act as a reservoir for transmission of antibiotic resistance and are a source of infection. Exposure to antibiotics by the commensal flora renders them resistant. Antibiotic consumption and hospitalisation are two major factors influencing this. We studied, antibiotic-resistant bacteria colonising rural adult population who had restricted access to health care and presumably had low consumption of antibiotics. Aim: Detection of multidrug resistance genes of extended spectrum β-lactamase (ESBL-CTX-M), AmpC β-Lactamase (CIT), Klebsiella pneumoniae carbapenemase (KPC) and New Delhi Metallo β-lactamase (NDM) in Enterobacteriaceae colonising the gut of adult population in a South Indian rural community. Methodology: Faecal samples of 154 healthy volunteers were screened for Enterobacteriaceae resistant to commonly used antibiotics by standard methods, followed by phenotypic detection of ESBL by double disk synergy method, AmpC by spot inoculation and carbapenemases by imipenem and ethylenediaminetetraacetic acid + imipenem combined E-test strips and modified Hodge test. Polymerase chain reaction was done to detect blaCTX-M,blaCIT,blaKPC-1 and blaNDM-1 genes coding for ESBL, AmpC, KPC and NDM, respectively. Results: Colonisation rate of enteric bacteria with MDR genes in the community was 30.1%. However, phenotypically, only ESBL (3.2%) and NDM (0.65%) were detected. While the genes coding for ESBL, AmpC and NDM were detected in 35.6%, 17.8% and 4.4% of the MDR isolates, respectively. Conclusions: Carriage of MDR strains with a potential to express multidrug resistance poses a threat of dissemination in the community. Awareness for restricted use of antibiotics and proper sanitation can contain the spread of resistant bacteria.

Keywords: Enterobacteriaceae, faecal carriage, gut colonisers, multidrug-resistant, rural India

How to cite this article:
Antony S, Ravichandran K, Kanungo R. Multidrug-resistant Enterobacteriaceae colonising the gut of adult rural population in South India. Indian J Med Microbiol 2018;36:488-93

How to cite this URL:
Antony S, Ravichandran K, Kanungo R. Multidrug-resistant Enterobacteriaceae colonising the gut of adult rural population in South India. Indian J Med Microbiol [serial online] 2018 [cited 2020 Oct 25];36:488-93. Available from:

 ~ Introduction Top

India contributes to a major proportion of the global burden of antibiotic resistance. A constellation of factors in India includes medical, agricultural, veterinary, social and environmental resulting from unbridled use of antibiotics. The transmission dynamics of antibiotic resistance within a hospital or in persons with easy access to healthcare setup is well documented. It is known that antibiotic pressure is an established cause of propagation of resistance.[1],[2],[3]

Drug-resistant genes initially detected in clinical isolates are now seen in intestinal colonisers.[4] Most of the data on the faecal carriage are from hospitalised patients, who are under antibiotic pressure. There is limited information about the carriage and spread of resistant strains in the community, more importantly in the rural community with little or no access to hospitals or antibiotics.[2],[5] This study was undertaken to determine if a representative group of the rural population harbours antibiotic-resistant bacteria in the gut.

 ~ Methodology Top

This was a prospective cross-sectional study carried out during October 2013 to December 2015 at a tertiary care hospital. The study protocol was reviewed and approved by the Institute's Research and Ethics Committees (Ref No: RC/13/64).

A sample size of 139 (with 95% confidence interval and 5% precision taking 10% prevalence) was calculated with 9% loss to follow-up. A total of 154 healthy adults ranging from 18 to 60 years, of both genders, were recruited from four rural hamlets adjoining Puducherry.

Individuals who gave a history of recent communicable disease were excluded from the study. A pre-tested and validated questionnaire were provided and explained to the participants to elicit information on risk factors and demographic patterns including information on access to healthcare facility, medical practitioners, exposure to antibiotics and pattern of drug purchase.

The participants were provided with a wide mouth leak-proof plastic disposable container and a wooden spatula to collect the stool. These were transported on the same day to the laboratory. The specimen was examined both macroscopically and microscopically for ova and cyst (for the benefit of the participants) and were processed by standard laboratory procedures for isolation of two aerobic enteric bacteria namely  Escherichia More Details coli and Klebsiella pneumoniae due to their propensity to carry resistance genes.[6]

All isolates were tested for susceptibility to ampicillin (10 μg) (except in case of K. pneumoniae isolates which are intrinsically resistant to ampicillin), ciprofloxacin (5 μg), tetracycline (30 μg), gentamicin (10 μg), cotrimoxazole (1.25/23.75 μg), chloramphenicol (30 μg), nitrofurantoin (300 μg), cefoxitin (30 μg), ceftazidime (30 μg) and ceftriaxone (30 μg). Also in isolates showing resistance to cephalosporins, susceptibility to carbapenems were tested with imipenem (10 μg) and meropenem (10 μg) discs. {HiMedia, Chennai, India} Results were interpreted according to the Clinical and Laboratory Standards Institute (CLSI) guidelines.[7]

Phenotypic resistance mechanisms were detected in all isolates that were resistant by the disc diffusion methods to ceftazidime, ceftriaxone and cefoxitin based on the CLSI zone diameter inhibition criteria. Phenotypic detection of extended spectrum β-lactamase (ESBL) was done by double disk synergy test according to CLSI and Amp C detection based on spot inoculation test.[7],[8]

All the isolates which were carbapenem (imipenem and meropenem) intermediately susceptible or resistant were tested for carbapenemase production by Modified Hodge test E. coli ATCC-25922 was used for the test along with K. pneumoniae BAA 1705 and K. pneumoniae BAA 1706 were used as positive and negative controls respectively.[7]

All the carbapenem-resistant isolates were in addition tested for the production of metallo β-lactamase (MBL) by MBL E-test method (HiMEDIA Ezy MIC, Chennai, India) with MBL positive strain having a ratio of MIC of imipenem to MIC of imipenem + ethylenediaminetetraacetic acid (EDTA) >8.[9]

All multidrug-resistant (MDR) isolates were subjected to polymerase chain reaction (PCR) to detect the genes of ESBL (blaCTX-M), AmpC (blaCIT), KPC (blaKPC-1) and NDM (blaNDM-1) (Helini Biomolecules, Chennai, India). Kit inserts were followed throughout the procedures [Table 1].
Table 1: Specific primer sequence for blaCTX-M, blaCIT, blaKPC-1 and blaNDM-1 coding for Extended Spectrum β-Lactamase, AmpC, Klebsiella pneumoniae carbapenemase and New Delhi Metallo β-Lactamase resistance respectively

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Data were entered in Microsoft Excel and analyzed using SPSS software (Version: 20, IBM, Armonk, NY, United States of America). The results were expressed as numbers and percentage. Proportion and 95% confidence interval were used for calculating the prevalence of MDR genes in the community. Chi-square test was used to determine the association of various risk factors and multidrug resistance.

 ~ Results Top

E. coli and K. pneumoniae were isolated from 98.1% of the samples cultured. E. coli was isolated from 120 individuals, K. pneumoniae from 26 and a combination of both E. coli and K. pneumoniae from five participants. Three participants did not yield either of these organisms. Resistance profile of the isolates is shown in [Figure 1]. Multidrug resistance was observed in 32% (40 of 125) isolates of E. coli and in 22.6% (7 of 31) isolates of K. pneumoniae, totalling 47 (30.1%) MDR isolates from 156 isolates.
Figure 1: Antibiotic resistance profile of the isolates from study participants

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ESBL and NDM were detected in 3.2% (five E. coli isolates) and 0.6% (one K. pneumoniae isolate) respectively with a confidence interval of 1.1%–7.4% and 0.02%–3.5%. AmpC and K. pneumoniae carbapenemase (KPC) production were not observed in any of the isolates tested phenotypically for the respective enzyme.

Genes of ESBL, AmpC and NDM were detected by PCR in 45 MDR isolates (two isolates could not be tested). Sixteen isolates, i.e., 35.6% showed the presence of blaCTX-M, eight isolates (17.8%) had blaCIT and two isolates (4.4%) showed the presence of blaNDM-1 with a confidence interval of in each of them at 21.9%–51.2%, 8.0%–32.1% and 0.5%–15.2%. None of the isolates demonstrated blaKPC gene.

Among the isolates subjected to PCR for blaCTX-M, five E. coli isolates which had phenotypically demonstrated the production of ESBL were positive for blaCTX-M. Remaining eleven E. coli isolates (36.7%) did not show the production of ESBL phenotypically but harboured the gene blaCTX-M.

All isolates tested phenotypically for the presence of AmpC were negative by spot inoculation test. However, the AmpC gene (blaCIT) was detected in six K. pneumoniae and two E. coli isolates. One E. coli isolate showed the presence of both ESBL and AmpC though neither of the antibiotic resistance mechanisms was expressed phenotypically.

Among the isolates tested for NDM gene by PCR, one isolate of K. pneumoniae which was phenotypically detected by E-test was positive for blaNDM-1. In addition, one isolate of E. coli which was sensitive to imipenem and meropenem showed the presence of blaNDM-1.

Participants were grouped, and various risk factors were analysed, and the findings are summarised in [Table 2].
Table 2: Prevalence and bivariate analysis of potential risk factors for multi-drug resistance in rural population (n=154)

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 ~ Discussion Top

Antimicrobial resistance is a looming threat with serious implications on successful treatment of bacterial infections, transmission of these drug-resistant strains in the community and the massive costs involved in prevention and treatment.[1],[10] Research by targeting these organisms in the clinical scenario has now shifted its focus to the faecal carriage of multi-drug-resistant organisms (MDROs) in the community.[11] Studies both in clinical and community settings have shown that increasing number of commensal strains have acquired drug-resistant genes, especially in the urban population.[1],[4],[12] The results of the present study revealed that 30.1% of isolates were MDR, i.e., with resistance to one or more agent in three or more categories of antibiotics, i.e., penicillins, cephalosporins, aminoglycosides, fluoroquinolones, folate pathway inhibitors, phenicols, carbapenems and polymixins (in Enterobacteriaceae).[13] A study in healthy pregnant women attending urban community centre and rural primary health centres of Vellore (2004) showed the prevalence of MDR was 8.4%, whereas the study done in Ujjain (2011) in children aged 3–16 years in the community of Palwa, showed a prevalence rate of 33%.[14],[15] The study from Vellore had low MDR carriage as the study population was pregnant women who were young and exposure to antibiotics would be presumed to be low. While the study from Ujjain reported similar carriage rates. These studies show an increasing trend in the colonisation by MDROs in the community over the years though a previous study from this centre reported a similar carriage rate of 32% among primary school children belonging to Mathur and Kozhivari rural communities in Pondicherry.[16] A study in France, in patients hospitalised for acute diarrhoea reported MDR carriage rate as high as 31.7%.[17] While a study from nursing homes in U. K and long-term care facility in U. S reported MDR carriage rate as 40.5% and 61%.[18],[19] Higher percentage of carriage rates were due to the nosocomial settings of the participants.

Both E. coli and K. pneumoniae share similarities in resistance though exceptions are present which may be due to the lower isolation rate of K. pneumoniae from the gut. The changing trends in resistance of commensal E. coli in the gut to commonly used antibiotics noted from various studies on colonisation in Indian population may be a reflection of the changing trends in the prescription of antibiotics over the years.[14],[15],[16]

The prevalence of ESBL and NDM were 3.2% and 0.65%, respectively, with a confidence interval of 1.1%–7.4% and 0.02%–3.5%, detected phenotypically. No KPC and AmpC producers were detected phenotypically in our study. A study from Pondicherry comparing simultaneous gut colonisation and infection by ESBL E. coli in hospitalised patients showed a faecal carriage rate of 21%. This was due to existing infection in these patients with ESBL producing E. coli.[20] A study from CMC Vellore (2004) in healthy pregnant women attending urban community centre and rural primary health centre reported in 1095 E. coli, 18 isolates as ESBL producers (1.6%) though only 4 ESBLs in 510 isolates were isolated from participants from the rural health centre.[14] In a study from Uttar Pradesh (2011), the prevalence rates of ESBL (double disc synergy test) and AmpC (AmpC disk test using TrisEDTA) in 396 healthy adults from the community were 4.2% and 0.51%, respectively.[21] The prevalence of ESBL correlates with the present study. While there were no AmpC producers detected in comparison. This could be due to a different phenotypic test method being used in the present study. AmpC testing shows high variability across methods and in CLSI there is no specific recommendation for the same. Data regarding colonisation of NDM-1 in the community is not available though recent studies point towards high carriage rate in hospitalised patients in our country.[22],[23] A study done in 2010 from New Delhi showed a high level of NDM-1 carriage in seepage and tap water with two of 50 drinking-water samples and 51 of 171 seepage samples positive for it.[24] The present study did not look into environmental factors.

Another finding during the study was the co-expression of AmpC and ESBL in one isolate. These could not be detected by the phenotypic method by their respective tests because when ESBL and AmpC are coproduced their expression is masked.

Among the probable risk factors which were analysed for association with multidrug resistance in E. coli and K. pneumoniae. Factor influencing the development of resistant flora was the literacy status i.e., participants, who were literate had a higher rate of MDROs colonisation (34.6%) in their normal flora (P = 0.04). On the other hand, participants who did not know what antibiotics were (32.3%) and had a tendency to repeat similar medication while ill also had a higher risk for carriage of resistant organisms (52.7%) (P = 0.341 and P = 0.042 respectively). However, other factors such as age, employment, socio-economic status of the participants, choice of health-care facility, factors determining the choice of health-care practices and usage of antibiotics and duration of consumption were not statistically significant (P > 0.05). A study among 417 rural Thai volunteers where there was statistically significant association, i.e., (P ≤ 0.05) between age (94 participants), no formal education (72 participants), unemployed (95 participants) and prescription of antibiotics in the last year (285 participants), 3 months (236 participants) and hospitalisation in the past 3 months (160 participants).[3]

The present study targeted the supposedly antibiotic naïve rural population with limited access to health-care facilities and has found colonisation of 30.1% MDROs in the volunteers, thereby indicating that Antimicrobial Resistance (AMR) has percolated the diminishing boundaries of urban and rural habitation. Although a small percentage, detection of resistant isolates among the gut flora of the rural population is a cause for concern. It also points to lack of proper practices, guidelines, monitoring agencies and control over prescription and sale of antibiotics in the area which need to be addressed to curb wrong practices. The study provides proof that organisms possessing resistance mechanisms, such as ESBL and NDM, are on the rise in the community. One should expect these resistance mechanisms when starting a patient on empiric therapy for serious bacterial infection.

One limitation of the study was that only a few of the common genes were checked for and not the entire range of genes which codes for MDR. Furthermore, as this study was participant questionnaire based hence the details of hospital visits and antibiotic usage needed to have been verified with the nearby hospitals. Another lacuna was that environmental sampling was not done. This would have indicated whether similar drug-resistant clones are found in nearby water source which could lead to widespread dissemination of these strains in the community. Furthermore, details regarding usage of antibiotics in livestock were not collected. Hence, further studies need to be done to incorporate environmental association with MDRO isolation from the community. Awareness and antibiotic guidelines need to be disseminated among health care personnel as well as among lay persons in these areas. Routine screening of patients especially those admitted to intensive care units (I. C. Us) for common resistance mechanisms like ESBLs and carbapenemases may help in understanding the dynamics of antibiotic resistance and help containing its emergence.

 ~ Conclusions Top

This study revealed a high faecal carriage rate of MDR organisms in rural population which is presumed not to be under apparent antibiotic pressure. Detection of commensal organisms carrying resistance genes is worrisome. This has a potential of dissemination and also the possibility of getting expressed in the presence of antibiotic pressure. The outcome of the dissemination of genes will adversely affect the treatment strategy in community-acquired infections. Further studies need to be undertaken with environmental sampling and correlation of prescription pattern in the area to see the true expanse of MDR in the community. Efforts for continuous surveillance should be undertaken for monitoring the alarming situation. Stringent enforcement of laws regarding procurement of antibiotics, prescriptions, patient compliance should be ensured. Safe drinking water and proper sanitation could contain the spread of resistant bacteria. Also creating awareness on the use and misuse of antibiotics in the community must be done to stem the tide of antibiotic resistance among human microbiota.


The molecular tests were validated by Dr. Vivian Joseph Ratnam P., Associate Professor and In-charge Molecular Biology Laboratory, Pondicherry Institute of Medical Sciences, Kalapet - 605 014, Puducherry, India.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

 ~ References Top

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Kohler P, Fulchini R, Albrich WC, Egli A, Balmelli C, Harbarth S, et al. Antibiotic resistance in Swiss nursing homes: Analysis of national surveillance data over an 11-year period between 2007 and 2017. Antimicrob Resist Infect Control 2018;7:88.  Back to cited text no. 5
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