Skip to main content
Top
Published in: BMC Infectious Diseases 1/2011

Open Access 01-12-2011 | Research article

Inactivation and sub-lethal injury of salmonella typhi, salmonella typhimurium and vibrio cholerae in copper water storage vessels

Authors: Riti Sharan, Sanjay Chhibber, Robert H Reed

Published in: BMC Infectious Diseases | Issue 1/2011

Login to get access

Abstract

Background

This study provides information on the antibacterial effect of copper against the water-borne pathogens Salmonella Typhi, Salmonella Typhimurium and Vibrio cholerae.

Methods

Suspensions of each pathogen were kept in water within a traditional copper vessel at 30°C for 24 h. Samples were withdrawn, diluted and plated onto suitable growth media. Conventional enumeration of healthy (uninjured) bacteria was carried out using standard aerobic incubation conditions. Additionally, reactive oxygen species-neutralised (ROS-n) conditions were achieved by adding the peroxide scavenger sodium pyruvate to the medium with anaerobic incubation, to enumerate uninjured (ROS-insensitive) and injured (ROS-sensitive) bacteria. Differences between log-transformed means of conventional (aerobic) and ROS-n counts were statistically evaluated using t tests.

Results

Overall, all three pathogens were inactivated by storage in copper vessels for 24 h. However, for shorter-term incubation (4-12 h), higher counts were observed under ROS-n conditions than under aerobic conditions, which demonstrate the presence of substantial numbers of sub-lethally injured cells prior to their complete inactivation.

Conclusions

The present study has for the first time confirmed that these bacterial pathogens are inactivated by storage in a copper vessel within 24 h. However, it has also demonstrated that it is necessary to account for short-term sub-lethal injury, manifest as ROS-sensitivity, in order to more fully understand the process. This has important practical implications in terms of the time required to store water within a copper vessel to completely inactivate these bacteria and thereby remove the risk of water-borne disease transmission by this route.
Appendix
Available only for authorised users
Literature
2.
go back to reference Steinberg EB, Mendoza CE, Glass R, Arana B, Lopez MB, Mejia M, Gold BD, Priest JW, Bibb W, Monroe SS, Bern C, Bell BP, Hoekstra RM, Klein R, Mintz ED, Luby S: Prevalence of infection with waterborne pathogens: A seroepidemiologic study in children 6-36 months old in San Juan Sacatepequez, Guatemala. Am J Trop Med Hyg. 2004, 70: 83-88.PubMed Steinberg EB, Mendoza CE, Glass R, Arana B, Lopez MB, Mejia M, Gold BD, Priest JW, Bibb W, Monroe SS, Bern C, Bell BP, Hoekstra RM, Klein R, Mintz ED, Luby S: Prevalence of infection with waterborne pathogens: A seroepidemiologic study in children 6-36 months old in San Juan Sacatepequez, Guatemala. Am J Trop Med Hyg. 2004, 70: 83-88.PubMed
3.
go back to reference Nwachcuku N, Gerba CP: Emerging water-borne pathogens: can we kill them all?. Curr Opinion Biotech. 2004, 15: 175-180. 10.1016/j.copbio.2004.04.010.CrossRef Nwachcuku N, Gerba CP: Emerging water-borne pathogens: can we kill them all?. Curr Opinion Biotech. 2004, 15: 175-180. 10.1016/j.copbio.2004.04.010.CrossRef
4.
go back to reference Faundez G, Troncoso M, Navarrete P, Figueroa G: Antimicrobial activity of copper surfaces against suspensions of Salmonella enterica and Campylobacter jejuni. BMC Microbiol. 2004, 4: 19-10.1186/1471-2180-4-19.CrossRefPubMedPubMedCentral Faundez G, Troncoso M, Navarrete P, Figueroa G: Antimicrobial activity of copper surfaces against suspensions of Salmonella enterica and Campylobacter jejuni. BMC Microbiol. 2004, 4: 19-10.1186/1471-2180-4-19.CrossRefPubMedPubMedCentral
5.
go back to reference Crump JA, Okoth GO, Slutsker L, Ogaja DO, Keswick BH, Luby SP: Effect of point-of-use disinfection, flocculation and combined flocculation-disinfection on drinking water quality in western Kenya. J Appl Microbiol. 2004, 97: 225-231. 10.1111/j.1365-2672.2004.02309.x.CrossRefPubMed Crump JA, Okoth GO, Slutsker L, Ogaja DO, Keswick BH, Luby SP: Effect of point-of-use disinfection, flocculation and combined flocculation-disinfection on drinking water quality in western Kenya. J Appl Microbiol. 2004, 97: 225-231. 10.1111/j.1365-2672.2004.02309.x.CrossRefPubMed
6.
go back to reference Maskey AP, Day JN, Tuan PQ, Thwaites GE, Campbell JI, Zimmerman M, Farrar JJ, Basnyat B: Salmonella enterica serovar Paratyphi A and S. enterica serovar Typhi cause indistinguishable clinical syndromes in Kathmandu, Nepal. Clin Infect Dis. 2006, 42: 1247-1253. 10.1086/503033.CrossRefPubMed Maskey AP, Day JN, Tuan PQ, Thwaites GE, Campbell JI, Zimmerman M, Farrar JJ, Basnyat B: Salmonella enterica serovar Paratyphi A and S. enterica serovar Typhi cause indistinguishable clinical syndromes in Kathmandu, Nepal. Clin Infect Dis. 2006, 42: 1247-1253. 10.1086/503033.CrossRefPubMed
7.
go back to reference Bhatta DR, Bangtrakulnonth A, Tishyadhigama P, Saroj SD, Bandekar JR, Hendriksen RS: Serotyping, PCR, phage-typing and antibiotic sensitivity testing of Salmonella serovars isolated from urban drinking water supply systems of Nepal. Lett Appl Microbiol. 2007, 44: 588-594. 10.1111/j.1472-765X.2007.02133.x.CrossRefPubMed Bhatta DR, Bangtrakulnonth A, Tishyadhigama P, Saroj SD, Bandekar JR, Hendriksen RS: Serotyping, PCR, phage-typing and antibiotic sensitivity testing of Salmonella serovars isolated from urban drinking water supply systems of Nepal. Lett Appl Microbiol. 2007, 44: 588-594. 10.1111/j.1472-765X.2007.02133.x.CrossRefPubMed
8.
go back to reference Mandal S, Mandal MD, Pal NK: Antimicrobial resistance pattern of Salmonella typhi isolates Kolkata, India during 1991-2001: a retrospective study. Jap J Infect Dis. 2002, 55: 58-59. Mandal S, Mandal MD, Pal NK: Antimicrobial resistance pattern of Salmonella typhi isolates Kolkata, India during 1991-2001: a retrospective study. Jap J Infect Dis. 2002, 55: 58-59.
9.
go back to reference Sur D, Seidlein L, Manna B, Dutta S, Deb AK, Sarkar BL, Kanungo S, Deen JL, Ali M, Kim DR, Gupta VK, Ochiai RL, Tsuzuki A, Acosta CJ, Clemens JD, Bhattacharya SK: The malaria and typhoid fever burden in the slums of Kolkata, India: data for a prospective community-based study. Tran R Soc Trop Med Hyg. 2006, 100: 725-733. 10.1016/j.trstmh.2005.10.019.CrossRef Sur D, Seidlein L, Manna B, Dutta S, Deb AK, Sarkar BL, Kanungo S, Deen JL, Ali M, Kim DR, Gupta VK, Ochiai RL, Tsuzuki A, Acosta CJ, Clemens JD, Bhattacharya SK: The malaria and typhoid fever burden in the slums of Kolkata, India: data for a prospective community-based study. Tran R Soc Trop Med Hyg. 2006, 100: 725-733. 10.1016/j.trstmh.2005.10.019.CrossRef
10.
go back to reference Alam M, Sultana M, Nair GB, Siddique AK, Hasan NA, Sack RB, Sack DA, Ahmed KU, Sadique A, Watanabe H, Grim CJ, Huq A, Colwell RR: Viable but nonculturable Vibrio cholerae O1 in biofilms in the aquatic environment and their role in cholera transmission. PNAS, USA. 2007, 104: 17801-17806. 10.1073/pnas.0705599104.CrossRef Alam M, Sultana M, Nair GB, Siddique AK, Hasan NA, Sack RB, Sack DA, Ahmed KU, Sadique A, Watanabe H, Grim CJ, Huq A, Colwell RR: Viable but nonculturable Vibrio cholerae O1 in biofilms in the aquatic environment and their role in cholera transmission. PNAS, USA. 2007, 104: 17801-17806. 10.1073/pnas.0705599104.CrossRef
11.
go back to reference Tandon P, Chhibber S, Reed RH: Survival and detection of the faecal indicator bacterium Enterococcus faecalis in water stored in traditional vessel. Indian J Med Research. 2007, 125: 557-566. Tandon P, Chhibber S, Reed RH: Survival and detection of the faecal indicator bacterium Enterococcus faecalis in water stored in traditional vessel. Indian J Med Research. 2007, 125: 557-566.
12.
go back to reference Pyle BH, Broadaway SC, McFeters GA: Efficacy of copper and silver ions with iodine in the inactivation of Pseudomonas cepacia. J Appl Bacteriol. 1992, 72: 71-79.PubMed Pyle BH, Broadaway SC, McFeters GA: Efficacy of copper and silver ions with iodine in the inactivation of Pseudomonas cepacia. J Appl Bacteriol. 1992, 72: 71-79.PubMed
13.
go back to reference Tandon P, Chhibber S, Reed RH: Inactivation of Escherichia coli and coliform bacteria in traditional brass and earthernware water storage vessels. Ant van Leeuw. 2005, 88: 35-48. 10.1007/s10482-004-7366-6.CrossRef Tandon P, Chhibber S, Reed RH: Inactivation of Escherichia coli and coliform bacteria in traditional brass and earthernware water storage vessels. Ant van Leeuw. 2005, 88: 35-48. 10.1007/s10482-004-7366-6.CrossRef
14.
go back to reference Brick T, Primrose B, Chandrasekhar R, Roy S, Muliyil J, Kang G: Water contamination in urban south India: household storage practices and their implications for water safety and enteric infections. Int J Hyg Environ Health. 2004, 207: 473-480. 10.1078/1438-4639-00318.CrossRefPubMed Brick T, Primrose B, Chandrasekhar R, Roy S, Muliyil J, Kang G: Water contamination in urban south India: household storage practices and their implications for water safety and enteric infections. Int J Hyg Environ Health. 2004, 207: 473-480. 10.1078/1438-4639-00318.CrossRefPubMed
15.
go back to reference Sudha VBP, Singh KO, Prasad SR, Venkatasubramanian P: Killing of enteric bacteria in drinking water by a copper device for use in home: laboratory evidence. Trans R Soc Trop Med Hyg. 2009, 103: 819-822. 10.1016/j.trstmh.2009.01.019.CrossRefPubMed Sudha VBP, Singh KO, Prasad SR, Venkatasubramanian P: Killing of enteric bacteria in drinking water by a copper device for use in home: laboratory evidence. Trans R Soc Trop Med Hyg. 2009, 103: 819-822. 10.1016/j.trstmh.2009.01.019.CrossRefPubMed
16.
go back to reference Wong H, Wang P, Chen SY, Chiu SW: Resuscitation of viable but non-culturable Vibrio parahaemolyticus in a minimum salt medium. FEMS Microbiol Letters. 2004, 233: 269-275. 10.1111/j.1574-6968.2004.tb09491.x.CrossRef Wong H, Wang P, Chen SY, Chiu SW: Resuscitation of viable but non-culturable Vibrio parahaemolyticus in a minimum salt medium. FEMS Microbiol Letters. 2004, 233: 269-275. 10.1111/j.1574-6968.2004.tb09491.x.CrossRef
17.
go back to reference Oliver JD: Viable but nonculturable bacteria in food environments. Food Borne Pathogens: Microbiology and Molecular Biology. Edited by: Fratamico PM, Bhunia AK. 2005, Horizon Scientific Press, Norfolk, U.K. Oliver JD: Viable but nonculturable bacteria in food environments. Food Borne Pathogens: Microbiology and Molecular Biology. Edited by: Fratamico PM, Bhunia AK. 2005, Horizon Scientific Press, Norfolk, U.K.
18.
go back to reference Wuytack EY, Phuong LDT, Aertsen A, Reyns KMF, Marquenie D, De Ketelaere B, Masschalck B, Van Opstal I, Diels AMJ, Michiels CW: Comparison of sub-lethal injury induced in Salmonella enterica serovar Typhimurium by heat and by different nonthermal treatments. J Food Protection. 2003, 66: 31-37. Wuytack EY, Phuong LDT, Aertsen A, Reyns KMF, Marquenie D, De Ketelaere B, Masschalck B, Van Opstal I, Diels AMJ, Michiels CW: Comparison of sub-lethal injury induced in Salmonella enterica serovar Typhimurium by heat and by different nonthermal treatments. J Food Protection. 2003, 66: 31-37.
19.
go back to reference Khaengraeng R, Reed RH: Oxygen and photoinactivation of Escherichia coli in UVA and sunlight. J Appl Microbiol. 2005, 99: 39-50. 10.1111/j.1365-2672.2005.02606.x.CrossRefPubMed Khaengraeng R, Reed RH: Oxygen and photoinactivation of Escherichia coli in UVA and sunlight. J Appl Microbiol. 2005, 99: 39-50. 10.1111/j.1365-2672.2005.02606.x.CrossRefPubMed
20.
go back to reference Tandon P, Chhibber S, Reed RH: Survival and detection of the faecal indicator bacterium Enterococcus faecalis in water stored in traditional vessel. Indian J Med Res. 2007, 125: 557-566.PubMed Tandon P, Chhibber S, Reed RH: Survival and detection of the faecal indicator bacterium Enterococcus faecalis in water stored in traditional vessel. Indian J Med Res. 2007, 125: 557-566.PubMed
21.
go back to reference Stephens PJ, Druggan P, Caron NV: Stressed Salmonella are exposed to reactive oxygen species from two independent sources during recovery in conventional culture media. Int J Food Microbiol. 2000, 60: 269-285. 10.1016/S0168-1605(00)00345-7.CrossRefPubMed Stephens PJ, Druggan P, Caron NV: Stressed Salmonella are exposed to reactive oxygen species from two independent sources during recovery in conventional culture media. Int J Food Microbiol. 2000, 60: 269-285. 10.1016/S0168-1605(00)00345-7.CrossRefPubMed
22.
go back to reference Ochiai RL, Wang XY, von Seidlein L, Yang J, Bhutta ZA, Bhattacharya SK, Agtini M, Deen JL, Wain J, Kim DR, Ali M, Acosta CJ, Jodar L, Clemens JD: Salmonella Paratyphi A rates, Asia. Emerg Infect Dis. 2005, 11: 1764-1766.CrossRefPubMedPubMedCentral Ochiai RL, Wang XY, von Seidlein L, Yang J, Bhutta ZA, Bhattacharya SK, Agtini M, Deen JL, Wain J, Kim DR, Ali M, Acosta CJ, Jodar L, Clemens JD: Salmonella Paratyphi A rates, Asia. Emerg Infect Dis. 2005, 11: 1764-1766.CrossRefPubMedPubMedCentral
23.
go back to reference Gaffga NH, Tauxe RV, Mintz ED: Cholera: A new homeland in Africa?. Am J Trop Med Hyg. 2007, 77: 705-713.PubMed Gaffga NH, Tauxe RV, Mintz ED: Cholera: A new homeland in Africa?. Am J Trop Med Hyg. 2007, 77: 705-713.PubMed
24.
go back to reference Thompson T, Sobsey M, Bartram J: Providing clean water, keeping water clean: an integrated approach. Int J Env Health Res. 2003, 13: S89-S94.CrossRef Thompson T, Sobsey M, Bartram J: Providing clean water, keeping water clean: an integrated approach. Int J Env Health Res. 2003, 13: S89-S94.CrossRef
25.
go back to reference Trevett AF, Carter RC: Targeting appropriate interventions to minimize deterioration of drinking-water quality in developing countries. J Health Popul Nutr. 2008, 26: 125-138.PubMedPubMedCentral Trevett AF, Carter RC: Targeting appropriate interventions to minimize deterioration of drinking-water quality in developing countries. J Health Popul Nutr. 2008, 26: 125-138.PubMedPubMedCentral
26.
go back to reference Eshcol J, Mahapatra P, Keshapagu S: Is fecal contamination of drinking water after collection associated with household water handling and hygiene practices? A study of urban slum households in Hyderabad, India. J Water Health. 2009, 7: 145-154. 10.2166/wh.2009.094.CrossRefPubMed Eshcol J, Mahapatra P, Keshapagu S: Is fecal contamination of drinking water after collection associated with household water handling and hygiene practices? A study of urban slum households in Hyderabad, India. J Water Health. 2009, 7: 145-154. 10.2166/wh.2009.094.CrossRefPubMed
27.
go back to reference Wu J, Doan H, Cuenca MA: Investigation of gaseous ozone as an anti-fungal fumigant for stored wheat. J Chem Tech & Biotechnol. 2006, 81: 1288-1293. 10.1002/jctb.1550.CrossRef Wu J, Doan H, Cuenca MA: Investigation of gaseous ozone as an anti-fungal fumigant for stored wheat. J Chem Tech & Biotechnol. 2006, 81: 1288-1293. 10.1002/jctb.1550.CrossRef
28.
go back to reference Constantin de Magny G, Long W, Brown CW, Hood RR, Huq A, Murtugudde R, Colwell R: Predicting the distribution of Vibrio spp. In the Chesapeake Bay: A Vibrio cholerae case study. EcoHealth. 2009, 6: 378-89. 10.1007/s10393-009-0273-6.CrossRefPubMed Constantin de Magny G, Long W, Brown CW, Hood RR, Huq A, Murtugudde R, Colwell R: Predicting the distribution of Vibrio spp. In the Chesapeake Bay: A Vibrio cholerae case study. EcoHealth. 2009, 6: 378-89. 10.1007/s10393-009-0273-6.CrossRefPubMed
29.
go back to reference Chaiyanan S, Chaiyanan S, Huq A, Maguel T, Colwell RR: Viability of the nonculturable Vibrio cholerae O1 and O139. Syst App Microbiol. 2001, 24: 331-341. 10.1078/0723-2020-00032.CrossRef Chaiyanan S, Chaiyanan S, Huq A, Maguel T, Colwell RR: Viability of the nonculturable Vibrio cholerae O1 and O139. Syst App Microbiol. 2001, 24: 331-341. 10.1078/0723-2020-00032.CrossRef
30.
go back to reference Bogosian G, Aardema ND, Bourneuf EV, Morris PJL, O'Neil JP: Recovery of hydrogen peroxide-sensitive culturable cells of Vibrio vulnificus gives the appearance of resuscitation from a viable but nonculturable state. J Bacteriol. 2000, 182: 5070-5075. 10.1128/JB.182.18.5070-5075.2000.CrossRefPubMedPubMedCentral Bogosian G, Aardema ND, Bourneuf EV, Morris PJL, O'Neil JP: Recovery of hydrogen peroxide-sensitive culturable cells of Vibrio vulnificus gives the appearance of resuscitation from a viable but nonculturable state. J Bacteriol. 2000, 182: 5070-5075. 10.1128/JB.182.18.5070-5075.2000.CrossRefPubMedPubMedCentral
31.
go back to reference Bang W, Drake MA, Jaykus LA: Recovery and detection of Vibrio vulnificus during cold storage. Food Microbiol. 2007, 24: 664-670. 10.1016/j.fm.2006.12.002.CrossRefPubMed Bang W, Drake MA, Jaykus LA: Recovery and detection of Vibrio vulnificus during cold storage. Food Microbiol. 2007, 24: 664-670. 10.1016/j.fm.2006.12.002.CrossRefPubMed
32.
go back to reference Mizunoe Y, Wai SN, Ishikawa T, Takade A, Yoshida S: Resuscitation of viable but nonculturable cells of Vibrio parahemolyticus induced at low temperature under starvation. FEMS Microbiol Letters. 2000, 186: 115-120. 10.1111/j.1574-6968.2000.tb09091.x.CrossRef Mizunoe Y, Wai SN, Ishikawa T, Takade A, Yoshida S: Resuscitation of viable but nonculturable cells of Vibrio parahemolyticus induced at low temperature under starvation. FEMS Microbiol Letters. 2000, 186: 115-120. 10.1111/j.1574-6968.2000.tb09091.x.CrossRef
33.
go back to reference Sharan R, Chhibber S, Attri S, Reed RH: Inactivation and injury of Escherichia coli in a copper water storage vessel: effects of temperature and pH. Ant van Leeuwen. 2010, 97: 91-97. 10.1007/s10482-009-9395-7.CrossRef Sharan R, Chhibber S, Attri S, Reed RH: Inactivation and injury of Escherichia coli in a copper water storage vessel: effects of temperature and pH. Ant van Leeuwen. 2010, 97: 91-97. 10.1007/s10482-009-9395-7.CrossRef
Metadata
Title
Inactivation and sub-lethal injury of salmonella typhi, salmonella typhimurium and vibrio cholerae in copper water storage vessels
Authors
Riti Sharan
Sanjay Chhibber
Robert H Reed
Publication date
01-12-2011
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2011
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-11-204

Other articles of this Issue 1/2011

BMC Infectious Diseases 1/2011 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.