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Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study

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Summary

Background

Not all patients infected with NDM-1-positive bacteria have a history of hospital admission in India, and extended-spectrum β-lactamases are known to be circulating in the Indian community. We therefore measured the prevalence of the NDM-1 gene in drinking water and seepage samples in New Delhi.

Methods

Swabs absorbing about 100 μL of seepage water (ie, water pools in streets or rivulets) and 15 mL samples of public tap water were collected from sites within a 12 km radius of central New Delhi, with each site photographed and documented. Samples were transported to the UK and tested for the presence of the NDM-1 gene, blaNDM-1, by PCR and DNA probing. As a control group, 100 μL sewage effluent samples were taken from the Cardiff Wastewater Treatment Works, Tremorfa, Wales. Bacteria from all samples were recovered and examined for blaNDM-1 by PCR and sequencing. We identified NDM-1-positive isolates, undertook susceptibility testing, and, where appropriate, typed the isolates. We undertook Inc typing on blaNDM-1-positive plasmids. Transconjugants were created to assess plasmid transfer frequency and its relation to temperature.

Findings

From Sept 26 to Oct 10, 2010, 171 seepage samples and 50 tap water samples from New Delhi and 70 sewage effluent samples from Cardiff Wastewater Treatment Works were collected. We detected blaNDM-1 in two of 50 drinking-water samples and 51 of 171 seepage samples from New Delhi; the gene was not found in any sample from Cardiff. Bacteria with blaNDM-1 were grown from 12 of 171 seepage samples and two of 50 water samples, and included 11 species in which NDM-1 has not previously been reported, including Shigella boydii and Vibrio cholerae. Carriage by enterobacteria, aeromonads, and V cholera was stable, generally transmissible, and associated with resistance patterns typical for NDM-1; carriage by non-fermenters was unstable in many cases and not associated with typical resistance. 20 strains of bacteria were found in the samples, 12 of which carried blaNDM-1 on plasmids, which ranged in size from 140 to 400 kb. Isolates of Aeromonas caviae and V cholerae carried blaNDM-1 on chromosomes. Conjugative transfer was more common at 30°C than at 25°C or 37°C.

Interpretation

The presence of NDM-1 β-lactamase-producing bacteria in environmental samples in New Delhi has important implications for people living in the city who are reliant on public water and sanitation facilities. International surveillance of resistance, incorporating environmental sampling as well as examination of clinical isolates, needs to be established as a priority.

Funding

European Union.

Introduction

The spread of mobile carbapenemases among bacterial pathogens is of great concern, not only because these enzymes confer resistance to carbapenems and other β-lactam antibiotics, but also because such pathogens typically are resistant to multiple other antibiotic classes, leaving very few treatment options available.1, 2 This concern is certainly warranted for Enterobacteriaceae that produce NDM-1 β-lactamase.3 Plasmids carrying the gene for this carbapenemase, blaNDM-1, can have up to 14 other antibiotic resistance determinants (M A Toleman, unpublished data) and can transfer this resistance to other bacteria, resulting in multidrug-resistant or extreme drug-resistant phenotypes.4 Resistance of this scale could have serious public health implications because so much of modern medicine is dependent on the ability to treat infection.2, 5, 6

So far, the NDM-1 enzyme has been found clinically in Enterobacteriaceae and Acinetobacter baumannii,7 and both our previous study4 and findings by Deshpande and colleagues8 showed that NDM-1 is widely disseminated in the Indian subcontinent. The first NDM-1-positive isolate described was from a Swedish resident of Indian origin who contracted a Klebsiella pneumoniae infection while in India in late 2007. The patient also had an NDM-1-positive Escherichia coli strain in his gut flora.3 A recent surveillance study9 showed that isolates containing NDM-1 were circulating in New Delhi as early as 2006, 2 years before the first European case was identified. Since 2008, there has been repeated import of NDM-1-positive bacteria from the Indian subcontinent to Europe, the USA, Canada, Asia, and Australasia, which was often mediated via transfers of patients, as well as some direct transmission in Europe and some unaccounted clusters linked to the Balkans.10

Many of the patients from Europe, North America, Asia, and Australasia had been admitted to hospital in India, Pakistan, or Bangladesh, but a few had a history of travel to the subcontinent without hospital admission. For example, some individuals had gut colonisation with producer strains found coincidentally while being assessed for traveller's diarrhoea.11 Also, the known problem of poor sanitation in some parts of India12 and the fact that many travellers to the Indian subcontinent experience gut colonisation with other multiresistant bacteria13 led us to investigate the extent to which blaNDM-1 is circulating in community waste seepage and tap water in urban New Delhi and to assess the transmissibility of blaNDM-1-encoding elements.

Section snippets

Sample collection

An employee of Channel 4 News who holds a UK biology degree oversaw the sample collection and was given strict verbal and written instructions on collection of samples. The corresponding author spoke to the team several times to ensure that proper procedures were followed. Swabs of seepage water and tap water samples from individual sites, picked by team members, within a 12 km radius of central New Delhi were collected. Swabs were taken from waste seepage sites (ie, water pools in streets or

Results

From Sept 26 to Oct 10, 2010, 171 swabs of seepage water and 50 tap water samples from New Delhi and 70 sewage effluent samples from Cardiff Wastewater Treatment Works were collected. Analyses of samples was done from Oct 12, 2010, to Jan 10, 2011. Two of 50 water samples and 51 of 171 seepage samples from throughout the centre and surrounding areas of New Delhi were blaNDM-1 positive (figure 1); however, eight seepage samples did not give a positive result with PCR alone (figure 2). All 70

Discussion

NDM-1 β-lactamase is widely disseminated in New Delhi and has spread into key enteric pathogens. These data present an account of the environmental distribution of bacteria carrying the NDM-1 gene in New Delhi (panel). The two water sources that were blaNDM-1-positive are used for drinking and food preparation as well as personal washing and cleaning of clothes. Whether these data can be extrapolated to other Indian cities is unknown, but clearly there is an urgent need for broad

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