Prevalence of ESBL-Producing Escherichia coli Isolated from elderly living at home setting in Mae Chai district, Phayao, Thailand

Kanittapon Supadej; Narong Nuanmuang; Pareeya Baiubon; Aksarakorn Kummasook

doi:10.14456/nujst.2023.2

Authors

Kanittapon Supadej Unit of Excellent in Infectious Disease, Department of Medical Technology, School of Allied Health Sciences, University of Phayao, Phayao Province, Thailand 56000
Narong Nuanmuang Unit of Excellent in Infectious Disease, Department of Medical Technology, School of Allied Health Sciences, University of Phayao, Phayao Province, Thailand 56000
Pareeya Baiubon Unit of Excellent in Infectious Disease, Department of Medical Technology, School of Allied Health Sciences, University of Phayao, Phayao Province, Thailand 56000
Aksarakorn Kummasook Unit of Excellent in Infectious Disease, Department of Medical Technology, School of Allied Health Sciences, University of Phayao, Phayao Province, Thailand 56000

DOI:

https://doi.org/10.14456/nujst.2023.2

Keywords:

ESBL-producing E. coli, elderly people, multidrug resistance, blaCTX-M, Thailand

Abstract

The prevalence of ESBL-producing bacteria has become a problem worldwide. This study aimed to investigate the existence of ESBL-producing E. coli isolates and their drug resistant genes that have become normal flora of the elderly population living in Phayao province. The fecal specimens from 252 elderly people were collected and drug resistant phenotypic screening was done by plating the samples on MacConkey agar supplemented with (1 µg/mL) cefotaxime or ceftazidime. The suspected E. coli isolates were identified with biochemical tests. Then, the phenotype of ESBL was confirmed by combination disk method and analyzed for bla_TEM, bla_SHV, and bla_CTX-M-1 by PCR. In this study, 75 isolates (29.8%) were confirmed as suspected ESBL-producing E. coli. All confirmed isolates were multidrug resistant (MDR), and resistant to AMP, CTX, CRO, and CPD. However, all of them were susceptible to IMP, ETP, and MEM. There were 5 phenotypic β-lactam resistant patterns detected. The most predominant pattern was AMP CTX CAZ CRO FEP CPD ATM (55.4%). The genotypic characterization showed predominance of bla_CTX-M-1 (35.7%) while there was no bla_SHV detected. Moreover, the combination of bla_TEM and bla_CTX-M-1 together was detected at about 43%. This study showed there was high prevalence of ESBL-producing E. coli in elderly people residing in one regional community. These results suggest that ESBL may be transmitted via feces in communities of close-living quarters without good cleaning and hygiene practices.

References

Ahmed, S. F., Ali, M. M., Mohamed, Z. K., Moussa, T. A., & Klena, J. D. (2014). Fecal carriage of extended-spectrum β-lactamases and AmpC-producing Escherichia coli in a Libyan community. Annals of clinical microbiology and antimicrobials, 13, 22. http://dx.doi.org/10.1186/1476-0711-13-22

Apisarnthanarak, A., Danchaivijitr, S., Khawcharoenporn, T., Limsrivilai, J., Warachan, B., Bailey, T. C.,

. . . Thammasart University Antibiotic Management, T. (2006). Effectiveness of education and an antibiotic-control program in a tertiary care hospital in Thailand. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America, 42(6), 768-775. http://dx.doi.org/10.1086/500325

Ben Sallem, R., Ben Slama, K., Estepa, V., Jouini, A., Gharsa, H., Klibi, N., . . . Torres, C. (2012). Prevalence and characterisation of extended-spectrum β-lactamase (ESBL)-producing Escherichia coli isolates in healthy volunteers in Tunisia. European journal of clinical microbiology & infectious diseases: official publication of the European Society of Clinical Microbiology, 31(7), 1511-1516. http://dx.doi.org/10.1007/s10096-011-1471-z

Blom, A., Ahl, J., Mansson, F., Resman, F., & Tham, J. (2016). The prevalence of ESBL-producing Enterobacteriaceae in a nursing home setting compared with elderly living at home: a cross-sectional comparison. BMC infectious diseases, 16, 111. http://dx.doi.org/10.1186/s12879-016-1430-5

Boonyasiri, A., Tangkoskul, T., Seenama, C., Saiyarin, J., Tiengrim, S., & Thamlikitkul, V. (2014). Prevalence of antibiotic resistant bacteria in healthy adults, foods, food animals, and the environment in selected areas in Thailand. Pathogens and global health, 108(5), 235-245. http://dx.doi.org/10.1179/2047773214Y.0000000148

Bubpamala, J., Khuntayaporn, P., Thirapanmethee, K., Montakantikul, P., Santanirand, P., & Chomnawang, M. T. (2018). Phenotypic and genotypic characterizations of extended-spectrum beta-lactamase-producing Escherichia coli in Thailand. Infection and drug resistance, 11, 2151–2157. https://doi.org/10.2147/IDR.S174506

Chanawong, A., Lulitanond, A., Kaewkes, W., Lulitanond, V., Srigulbutr, S., & Homchampa, P. (2007). CTX-M extended-spectrum β-lactamases among clinical isolates of Enterobacteriaceae in a Thai university hospital. The Southeast Asian journal of tropical medicine and public health, 38(3), 493-500.

Chang, K., Rattanavong, S., Mayxay, M., Keoluangkhot, V., Davong, V., Vongsouvath, M., . . . Dance, D. (2020). Bacteremia caused by extended-spectrum β-lactamase-producing Enterobacteriaceae in Vientiane, Lao PDR: A 5-Year Study. The American journal of tropical medicine and hygiene, 102(5), 1137-1143. http://dx.doi.org/10.4269/ajtmh.19-0304

CLSI, (2016). Performance standards for antimicrobial disk susceptibility tests, CLSI supplement M100 (26th ed.). Wayne: Clinical and Laboratory Standards Institute.

Dallenne, C., Da Costa, A., Decré, D., Favier, C., & Arlet, G. (2010). Development of a set of multiplex PCR assays for the detection of genes encoding important β-lactamases in Enterobacteriaceae. The Journal of antimicrobial chemotherapy, 65(3), 490–495. https://doi.org/10.1093/jac/dkp498

Hafza, N., Challita, C., Dandachi, I., Bousaab, M., Dahdouh, E., & Daoud, Z. (2018). Competition assays between ESBL-producing E. coli and K. pneumoniae isolates collected from Lebanese elderly: An additional cost on fitness. Journal of infection and public health., 11(3), 393-397. http://dx.doi.org/10.1016/j.jiph.2017.09.010

Jorgensen, J. H., McElmeel, M. L., Fulcher, L. C., & Zimmer, B. L. (2010). Detection of CTX-M-type extended-spectrum β -lactamase (ESBLs) by Testing with microscan overnight and ESBL confirmation panels. Journal of Clinical Microbiology, 48(1), 120-123. http://dx.doi.org/10.1128/jcm.01507-09

Kader, A. A., Kumar, A., & Kamath, K. A. (2007). Fecal carriage of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in patients and asymptomatic healthy individuals. Infection control and hospital epidemiology, 28(9), 1114–1116. https://doi.org/10.1086/519865

Kanoksil, M., Jatapai, A., Peacock, S. J., & Limmathurotsakul, D. (2013). Epidemiology, microbiology and mortality associated with community-acquired bacteremia in northeast Thailand: a multicenter surveillance study. PLoS One, 8(1), e54714. http://dx.doi.org/10.1371/journal.pone.0054714

Kawamura, K., Nagano, N., Suzuki, M., Wachino, J. I., Kimura, K., & Arakawa, Y. (2017). ESBL-producing Escherichia coli and its rapid rise among healthy people. Food safety, 5(4), 122-150. http://dx.doi.org/10.14252/foodsafetyfscj.2017011

Khamsarn, S., Nampoonsak, Y., Busamaro, S., Tangkoskul, T., Seenama, C., Rattanaumpawan, P., . . . Thamlikitkul, V. (2016). Epidemiology of antibiotic use and antimicrobial resistance in selected communities in Thailand. Journal of the Medical Association of Thailand, 99(3), 270-275.

Kiratisin, P., Apisarnthanarak, A., Laesripa, C., & Saifon, P. (2008). Molecular characterization and epidemiology of extended-spectrum-β-lactamase-producing Escherichia coli and Klebsiella pneumoniae isolates causing health care-associated infection in Thailand, where the CTX-M family is endemic. Antimicrobial agents and chemotherapy, 52(8), 2818-2824. http://dx.doi.org/10.1128/aac.00171-08

Kola, A., Kohler, C., Pfeifer, Y., Schwab, F., Kühn, K., Schulz, K., . . . Steinmetz, I. (2012). High prevalence of extended-spectrum-β-lactamase-producing Enterobacteriaceae in organic and conventional retail chicken meat, Germany. Journal of Antimicrobial Chemotherapy, 67(11), 2631-2634. http://dx.doi.org/10.1093/jac/dks295

Ku, N. S., Kim, Y. C., Kim, M. H., Song, J. E., Oh, D. H., Ahn, J. Y., . . . Choi, J. Y. (2014). Risk factors for 28-day mortality in elderly patients with extended-spectrum β-lactamase (ESBL)-producing Escherichia coli and Klebsiella pneumoniae bacteremia. Archives of gerontology and geriatrics, 58(1), 105-109. http://dx.doi.org/10.1016/j.archger.2013.07.002

Luvsansharav, U. O., Hirai, I., Niki, M., Sasaki, T., Makimoto, K., Komalamisra, C., . . . Yamamoto, Y. (2011). Analysis of risk factors for a high prevalence of extended-spectrum {β}-lactamase-producing Enterobacteriaceae in asymptomatic individuals in rural Thailand. Journal of medical microbiology, 60(Pt 5), 619-624. http://dx.doi.org/10.1099/jmm.0.026955-0

Mitchell, J., Purohit, M., Jewell, C. P., Read, J. M., Marrone, G., Diwan, V., & Stålsby Lundborg, C. (2021). Trends, relationships and case attribution of antibiotic resistance between children and environmental sources in rural India. Scientific reports, 11(1), 22599. https://doi.org/10.1038/s41598-021-01174-w

Nakayama, T., Ueda, S., Huong, B. T., Tuyen, l., Komalamisra, C., Kusolsuk, T., Hirai, I., & Yamamoto, Y. (2015). Wide dissemination of extended-spectrum β-lactamase-producing Escherichia coli in community residents in the Indochinese peninsula. Infection and drug resistance, 8, 1–5. https://doi.org/10.2147/IDR.S74934

Nguyen, V. T., Jamrozy, D., Matamoros, S., Carrique-Mas, J. J., Ho, H. M., Thai, Q. H., . . . Ngo, T. H. (2019). Limited contribution of non-intensive chicken farming to ESBL-producing Escherichia coli colonization in humans in Vietnam: an epidemiological and genomic analysis. The Journal of antimicrobial chemotherapy, 74(3), 561-570. http://dx.doi.org/10.1093/jac/dky506

Pehlivanlar Önen, S., Aslantaş, Ö., Şebnem Yılmaz, E., & Kürekci, C. (2015). Prevalence of β-lactamase producing Escherichia coli from retail meat in Turkey. Journal of Food Science, 80(9), M2023-M2029. http://dx.doi.org/10.1111/1750-3841.12984

Pishtiwan, A. H., & Khadija, K. M. (2019). Prevalence of blaTEM, blaSHV, and blaCTX-M genes among ESBL-producing Klebsiella pneumoniae and Escherichia coli isolated from thalassemia patients in Erbil, Iraq. Mediterranean journal of hematology and infectious diseases, 11(1), e2019041. http://dx.doi.org/10.4084/mjhid.2019.041

Reuland, E. A., Al Naiemi, N., Kaiser, A. M., Heck, M., Kluytmans, J. A. J. W., Savelkoul, P. H. M., . . . Vandenbroucke-Grauls, C. M. J. E. (2016). Prevalence and risk factors for carriage of ESBL-producing Enterobacteriaceae in Amsterdam. The Journal of antimicrobial chemotherapy, 71(4), 1076-1082. http://dx.doi.org/10.1093/jac/dkv441

Saekhow, P., & Sriphannam, C. (2021). Prevalence of extended-spectrum beta-lactamase-producing Escherichia coli strains in dairy farm wastewater in Chiang Mai: Veterinary Integrative Sciences, 19(3), 349–362. https://doi.org/10.12982/VIS.2021.030

Sawatwong, P., Sapchookul, P., Whistler, T., Gregory, C. J., Sangwichian, O., Makprasert, S., . . . Rhodes, J. (2019). High burden of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae bacteremia in older adults: a seven-year study in two rural Thai provinces. The American journal of tropical medicine and hygiene, 100(4), 943-951. http://dx.doi.org/10.4269/ajtmh.18-0394

Seenama, C., Thamlikitkul, V., & Ratthawongjirakul, P. (2019). Multilocus sequence typing and blaESBL characterization of extended-spectrum β-lactamase-producing Escherichia coli isolated from healthy humans and swine in northern Thailand. Infection and drug resistance, 12, 2201-2214. http://dx.doi.org/10.2147/IDR.S209545

Thamlikitkul, V., & Apisitwittaya, W. (2004). Implementation of clinical practice guidelines for upper respiratory infection in Thailand. International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases, 8(1), 47–51. http://dx.doi.org/10.1016/j.ijid.2003.09.001

Thamlikitkul, V., Tangkoskul, T., & Seenama, C. (2019). Fecal carriage rate of extended-spectrum β-lactamase-producing Enterobacteriaceae as a proxy composite indicator of antimicrobial resistance in a community in Thailand. Open forum infectious diseases, 6(10), ofz425. http://dx.doi.org/10.1093/ofid/ofz425

Wyres, K. L., Nguyen, T. N. T., Lam, M. M. C., Judd, L. M., van Vinh Chau, N., Dance, D. A. B., . . . Holt, K. E. (2020). Genomic surveillance for hypervirulence and multi-drug resistance in invasive Klebsiella pneumoniae from South and Southeast Asia. Genome medicine, 12(1), 11-11. http://dx.doi.org/10.1186/s13073-019-0706-y

Xu, G., An, W., Wang, H., & Zhang, X. (2015). Prevalence and characteristics of extended-spectrum β-lactamase genes in Escherichia coli isolated from piglets with post-weaning diarrhea in Heilongjiang province, China. Frontiers in microbiology, 6, 1103. https://doi.org/10.3389/fmicb.2015.01103