{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,26]],"date-time":"2026-03-26T12:50:23Z","timestamp":1774529423157,"version":"3.50.1"},"reference-count":38,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2018,1,19]],"date-time":"2018-01-19T00:00:00Z","timestamp":1516320000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>Surveillance data on the level of resistant bacteria is needed to inform strategies to reduce the development and spread of antibiotic resistance. The aim of this study was to determine the non-susceptibility trends to extended-spectrum cephalosporins and carbapenems among Escherichia coli and Klebsiella spp. isolates from the district of Nashik in Western India during the period 2004\u20132014. Antibacterial susceptibility testing of clinical isolates was performed using Kirby-Bauer disc diffusion method to determine inhibitory zone diameters. The change in proportions of non-susceptible bacteria over calendar time was investigated with spline transformations in a logistic regression model. For the extended-spectrum cephalosporins, the proportions of non-susceptible E. coli and Klebsiella spp. isolates were above 78.4% and 84.9% throughout the study period, respectively. E. coli and Klebsiella spp. isolates exhibited carbapenem non-susceptibility levels as high as 76.9% and 84.1% respectively. The proportions of extended-spectrum betalactamase (ESBL)-producing isolates ranged from 38.3\u201385.9% in E. coli and from 45.1\u201393.1% in Klebsiella spp. Significantly higher proportions of non-susceptible and ESBL-producing isolates were found among isolates from inpatients compared to isolates from outpatients for both E. coli and Klebsiella spp. (p &lt; 0.050). The high proportions of non-susceptible isolates observed show that there is great need to focus on optimal use of antibiotics to reduce the development of antibiotic resistance.<\/jats:p>","DOI":"10.3390\/ijerph15010155","type":"journal-article","created":{"date-parts":[[2018,1,22]],"date-time":"2018-01-22T04:51:13Z","timestamp":1516596673000},"page":"155","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Trends in Resistance to Extended-Spectrum Cephalosporins and Carbapenems among Escherichia coli and Klebsiella spp. Isolates in a District in Western India during 2004\u20132014"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5337-8619","authenticated-orcid":false,"given":"Ingvild","family":"Odsbu","sequence":"first","affiliation":[{"name":"Department of Public Health Sciences, Karolinska Institutet, 17177 Stockholm, Sweden"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Smita","family":"Khedkar","sequence":"additional","affiliation":[{"name":"Bac-Test Laboratory, College Road, Nashik 422005, Maharashtra, India"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Frida","family":"Lind","sequence":"additional","affiliation":[{"name":"Department of Public Health Sciences, Karolinska Institutet, 17177 Stockholm, Sweden"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Uday","family":"Khedkar","sequence":"additional","affiliation":[{"name":"Bac-Test Laboratory, College Road, Nashik 422005, Maharashtra, India"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sandeep","family":"Nerkar","sequence":"additional","affiliation":[{"name":"Department of Public Health Sciences, Karolinska Institutet, 17177 Stockholm, Sweden"},{"name":"Indian Initiative for Management of Antibiotic Resistance, Department of Environmental Medicine, R.D. Gardi Medical College, Ujjain 456006, India"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nicola","family":"Orsini","sequence":"additional","affiliation":[{"name":"Department of Public Health Sciences, Karolinska Institutet, 17177 Stockholm, Sweden"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0731-1680","authenticated-orcid":false,"given":"Ashok","family":"Tamhankar","sequence":"additional","affiliation":[{"name":"Department of Public Health Sciences, Karolinska Institutet, 17177 Stockholm, Sweden"},{"name":"Indian Initiative for Management of Antibiotic Resistance, Department of Environmental Medicine, R.D. Gardi Medical College, Ujjain 456006, India"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6525-1861","authenticated-orcid":false,"given":"Cecilia","family":"St\u00e5lsby Lundborg","sequence":"additional","affiliation":[{"name":"Department of Public Health Sciences, Karolinska Institutet, 17177 Stockholm, Sweden"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2018,1,19]]},"reference":[{"key":"ref_1","unstructured":"World Economic Forum (2013). Global Risks 2013, World Economic Forum."},{"key":"ref_2","unstructured":"The World Health Organization (WHO) (2014). Antimicrobial Resistance: Global Report on Surveillance, The World Health Organization (WHO)."},{"key":"ref_3","unstructured":"The World Health Organization (WHO) (2015). Global Action Plan on Antimicrobial Resistance, The World Health Organization (WHO)."},{"key":"ref_4","unstructured":"The World Health Organization (WHO) (2015, January 22\u201323). Meeting report: Global antimicrobial resistance surveillance system (GLASS). Proceedings of the Technical Meeting on the Early Implementation Phase, Copenhagen, Denmark."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"65","DOI":"10.11599\/germs.2015.1073","article-title":"A decade of change in susceptibility patterns of Gram-negative blood culture isolates: A single center study","volume":"5","author":"Alagesan","year":"2015","journal-title":"Germs"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"407","DOI":"10.4103\/0377-4929.138733","article-title":"Prevalence of extended spectrum beta-lactamase producing uropathogens and their antibiotic resistance profile in patients visiting a tertiary care hospital in central India: Implications on empiric therapy","volume":"57","author":"Bajpai","year":"2014","journal-title":"Indian J. Pathol. Microbiol."},{"key":"ref_7","first-page":"25","article-title":"Changing trends in antimicrobial susceptibility and hospital acquired infections over an 8-year period in a tertiary care hospital in relation to introduction of an infection control programme","volume":"58","author":"Gopalakrishnan","year":"2010","journal-title":"J. Assoc. Physicians India"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"485","DOI":"10.4103\/0019-5359.102118","article-title":"Changing trends of in vitro antimicrobial resistance patterns in blood isolates in a tertiary care hospital over a period of 4 years","volume":"64","author":"Gupta","year":"2010","journal-title":"Indian J. Med. Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"56","DOI":"10.4103\/0976-0105.118797","article-title":"Antimicrobial resistance pattern in a tertiary care hospital: An observational study","volume":"4","author":"Saravanan","year":"2013","journal-title":"J. Basic Clin. Pharm."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"39","DOI":"10.4103\/0976-9668.175060","article-title":"A retrospective study of the changing trends of antimicrobial resistance of Klebsiella pneumoniae isolated from urine samples over last 3 years (2012\u20132014)","volume":"7","author":"Sharma","year":"2016","journal-title":"J. Nat. Sci. Biol. Med."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"105","DOI":"10.4103\/0976-0105.141948","article-title":"Retrospective analysis of antibiotic resistance pattern to urinary pathogens in a Tertiary Care Hospital in South India","volume":"5","author":"Somashekara","year":"2014","journal-title":"J. Basic Clin. Pharm."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.ijid.2016.08.002","article-title":"Trends in antibiotic resistance among major bacterial pathogens isolated from blood cultures tested at a large private laboratory network in India, 2008\u20132014","volume":"50","author":"Gandra","year":"2016","journal-title":"Int. J. Infect. Dis."},{"key":"ref_13","unstructured":"(2017, March 27). Bac-Test Laboratory Web Page. Available online: http:\/\/www.indiamart.com\/bac-test-laboratory\/."},{"key":"ref_14","unstructured":"(2017, March 27). Indian Census 2011. Available online: http:\/\/www.census2011.co.in\/census\/district\/354-nashik.html."},{"key":"ref_15","unstructured":"The World Health Organization (WHO) (2017, March 27). WHONET Software. Available online: http:\/\/www.whonet.org\/software.html."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Blomberg, B., Mwakagile, D.S., Urassa, W.K., Maselle, S.Y., Mashurano, M., Digranes, A., Harthug, S., and Langeland, N. (2004). Surveillance of antimicrobial resistance at a tertiary hospital in Tanzania. BMC Public Health, 4.","DOI":"10.1186\/1471-2458-4-45"},{"key":"ref_17","unstructured":"National Committee for Clinical Laboratory Standards (2015). Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically, National Committee for Clinical Laboratory Standards (NCCLS). [10th ed.]. Approved Standard M07-A6."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1093\/ajcp\/45.4_ts.493","article-title":"Antibiotic susceptibility testing by a standardized single disk method","volume":"45","author":"Bauer","year":"1966","journal-title":"Am. J. Clin. Pathol."},{"key":"ref_19","unstructured":"Clinical and Laboratory Standards Institute (2004\u20132014). Performance Standards for Antimicrobial Susceptibility Testing, CLSI Documents M100-S14-M100-S24, Clinical and Laboratory Standards Institute (CLSI)."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1177\/1536867X0700700103","article-title":"Multivariable modeling with cubic regression splines: A principled approach","volume":"7","author":"Royston","year":"2007","journal-title":"Stata J."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1086\/669523","article-title":"Trends in resistance to carbapenems and third-generation cephalosporins among clinical isolates of Klebsiella pneumoniae in the United States, 1999\u20132010","volume":"34","author":"Braykov","year":"2013","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1016\/j.ijantimicag.2016.01.008","article-title":"Epidemiology and antimicrobial susceptibility profiles of pathogens causing urinary tract infections in the Asia-Pacific region: Results from the Study for Monitoring Antimicrobial Resistance Trends (SMART), 2010\u20132013","volume":"47","author":"Jean","year":"2016","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"129","DOI":"10.4111\/icu.2016.57.2.129","article-title":"Vancomycin resistant enterococci in urine cultures: Antibiotic susceptibility trends over a decade at a tertiary hospital in the United Kingdom","volume":"57","author":"Toner","year":"2016","journal-title":"Investig. Clin. Urol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/j.ijid.2004.01.001","article-title":"Antimicrobial resistance of Gram-negative bacilli isolates from inpatients and outpatients at Yaounde Central Hospital, Cameroon","volume":"8","author":"Pieboji","year":"2004","journal-title":"Int. J. Infect. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1608","DOI":"10.1016\/j.juro.2013.10.064","article-title":"A comparison of inpatient versus outpatient resistance patterns of pediatric urinary tract infection","volume":"191","author":"Saperston","year":"2014","journal-title":"J. Urol."},{"key":"ref_27","unstructured":"National Centre for Disease Control (2016). National Treatment Guidelines for Antimicrobial Use in Infectious Diseases."},{"key":"ref_28","unstructured":"The World Health Organization (WHO) (2017, March 27). World Health Day 2011. Available online: http:\/\/www.who.int\/world-health-day\/2011\/en\/."},{"key":"ref_29","unstructured":"(2017, March 27). Indian Initiative of Management of Antibiotic Resistance Web Page. Available online: http:\/\/save-antibiotics.blogspot.se\/2011\/04\/activities-of-iimar-members-on-world.html."},{"key":"ref_30","unstructured":"(2017, March 27). Antibiotic Stewardship Network in India Web Page. Available online: http:\/\/www.absn.in\/."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Gjelstad, S., Hoye, S., Straand, J., Brekke, M., Dalen, I., and Lindbaek, M. (2013). Improving antibiotic prescribing in acute respiratory tract infections: Cluster randomised trial from Norwegian general practice (prescription peer academic detailing (Rx-PAD) study). Br. Med. J., 347.","DOI":"10.1136\/bmj.f4403"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"125","DOI":"10.3109\/03009734.2014.905664","article-title":"Understanding and changing human behavior\u2014Antibiotic mainstreaming as an approach to facilitate modification of provider and consumer behaviour","volume":"119","author":"Tamhankar","year":"2014","journal-title":"Upsala J. Med. Sci."},{"key":"ref_33","unstructured":"Directorate General of Health Services (2011). National Policy for Containment of Antimicrobial Resistance in India."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/j.bjid.2013.07.010","article-title":"Ecology of blood stream infection and antibiotic resistance in intensive care unit at a tertiary care hospital in North India","volume":"18","author":"Wattal","year":"2014","journal-title":"Braz. J. Infect. Dis."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Lohiya, A., Kant, S., Kapil, A., Gupta, S.K., Misra, P., and Rai, S.K. (2015). Pattern of Antibiotic Resistance Among Community Derived Isolates of Enterobacteriaceae Using Urine Sample: A Study from Northern India. J. Clin. Diagn. Res., 9.","DOI":"10.7860\/JCDR\/2015\/14230.6254"},{"key":"ref_36","unstructured":"European Centre for Disease Prevention and Control (2015). Antimicrobial Resistance Surveillance in Europe 2014. Annual Report of the European Antimicrobial Resistance Surveillance Network (EARS-Net), European Centre for Disease Prevention and Control (ECDC)."},{"key":"ref_37","first-page":"628","article-title":"Ertapenem susceptibility of extended spectrum beta-lactamase-producing Enterobacteriaceae at a tertiary care centre in India","volume":"50","author":"Behera","year":"2009","journal-title":"Singap. Med. J."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"153","DOI":"10.4103\/2279-042X.162363","article-title":"Antimicrobial susceptibility pattern of extended-spectrum beta-lactamase producing Klebsiella pneumoniae clinical isolates in an Indian tertiary hospital","volume":"4","author":"Singh","year":"2015","journal-title":"J. Res. Pharm. Pract."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/15\/1\/155\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T14:51:53Z","timestamp":1760194313000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/15\/1\/155"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,1,19]]},"references-count":38,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2018,1]]}},"alternative-id":["ijerph15010155"],"URL":"https:\/\/doi.org\/10.3390\/ijerph15010155","relation":{},"ISSN":["1660-4601"],"issn-type":[{"value":"1660-4601","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,1,19]]}}}