Rupnik M , Wilcox MH , Gerding DN , 2009. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat Rev Microbiol 7: 526–536.
Vonberg RP et al.2008. Infection control measures to limit the spread of Clostridium difficile. Clin Microbiol Infect 14: 2–20.
Knight DR , Thean S , Putsathit P , Fenwick S , Riley TV , 2013. Cross-sectional study reveals high prevalence of Clostridium difficile non-PCR ribotype 078 strains in Australian veal calves at slaughter. Appl Environ Microbiol 79: 2630–2635.
Knight DR , Squire MM , Riley TV , 2015. Nationwide surveillance study of Clostridium difficile in Australian neonatal pigs shows high prevalence and heterogeneity of PCR ribotypes. Appl Environ Microbiol 81: 119–123.
Jawa RS , Mercer DW , 2012. Clostridium difficile-associated infection: a disease of varying severity. Am J Surg 204: 836–842.
Zellweger RM , Carrique-Mas J , Limmathurotsakul D , Day NPJ , Thwaites GE , Baker S , 2017. A current perspective on antimicrobial resistance in Southeast Asia. J Antimicrob Chemother 72: 2963–2972.
Om C , Daily F , Vlieghe E , McLaughlin JC , McLaws ML , 2017. Pervasive antibiotic misuse in the Cambodian community: antibiotic-seeking behaviour with unrestricted access. Antimicrob Resist Infect Control 6: 30.
Quet F et al.2015. Antibiotic prescription behaviours in Lao People’s Democratic Republic: a knowledge, attitude and practice survey. Bull World Health Organ 93: 219–227.
Om C , McLaws ML , 2016. Antibiotics: practice and opinions of Cambodian commercial farmers, animal feed retailers and veterinarians. Antimicrob Resist Infect Control 5: 42.
Thu TA , Rahman M , Coffin S , Harun-Or-Rashid M , Sakamoto J , Hung NV , 2012. Antibiotic use in Vietnamese hospitals: a multicenter point-prevalence study. Am J Infect Control 40: 840–844.
Mavros MN , Alexiou VG , Vardakas KZ , Tsokali K , Sardi TA , Falagas ME , 2012. Underestimation of Clostridium difficile infection among clinicians: an international survey. Eur J Clin Microbiol Infect Dis 31: 2439–2444.
Duong DTT , 2017. Determination of Infection Rates and Some Molecular Epidemiological Characteristics of Toxin Gene Carried Clostridium difficile Strains Isolated from Patients with Diarrhea after Antibiotic Treatment in Four Hospitals in Hanoi from 2013 to 2015. Hanoi, Vietnam: Department of Microbiology, Vietnam University of Science.
Duong VT et al.2016. Evaluation of Luminex xTAG gastrointestinal pathogen panel assay for detection of multiple diarrheal pathogens in fecal samples in Vietnam. J Clin Microbiol 54: 1094–1100.
Chhin S , Harwell JI , Bell JD , Rozycki G , Ellman T , Barnett JM , Ward H , Reinert SE , Pugatch D , 2006. Etiology of chronic diarrhea in antiretroviral-naive patients with HIV infection admitted to Norodom Sihanouk Hospital, Phnom Penh, Cambodia. Clin Infect Dis 43: 925–932.
Cheong E , Roberts T , Rattanavong S , Riley TV , Newton PN , Dance DAB , 2017. Clostridium difficile infection in the Lao People’s Democratic Republic: first isolation and review of the literature. BMC Infect Dis 17: 635.
Finney JMT , 1893. Gastroenterostomy for cicatrizing ulcer of the pylorus. Bull Johns Hopkins Hosp 4: 53–55.
Hall IC , O’Toole E , 1935. Intestinal flora in new-born infants: with a description of a new pathogenic anaerobe, Bacillus difficilis. AMA Am J Dis Child 49: 390–402.
Prévot AR , 1938. Études de systématique bactérienne. IV. Critique de la conception actuelle du genre Clostridium. Ann Inst Pasteur (Paris) 61: 72–91.
Snyder ML , 1940. The normal fecal flora of infants between two weeks and one year of age. J Infect Dis 66: 1–16.
Hafiz S , 1974. Clostridium difficile and Its Toxins. Leeds, United Kingdom: Department of Microbiology, Biological Sciences, University of Leeds.
Green RH , 1974. The association of viral activation with penicillin toxicity in guinea pigs and hamsters. Yale J Biol Med 47: 166–181.
Larson HE , Price AB , 1977. Pseudomembranous colitis: presence of clostridial toxin. Lancet 310: 1312–1314.
Bartlett JG , Onderdonk AB , Cisneros RL , Kasper DL , 1977. Clindamycin-associated colitis due to a toxin-producing species of Clostridium in hamsters. J Infect Dis 136: 701–705.
Bartlett JG , Chang TW , Gurwith M , Gorbach SL , Onderdonk AB , 1978. Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med 298: 531–534.
George WL , Goldstein EJC , Sutter VL , Ludwig SL , Finegold SM , 1978. Etiology of antimicrobial agent associated colitis. Lancet 311: 802–803.
Aronsson B , Mollby R , Nord CE , 1985. Antimicrobial agents and Clostridium difficile in acute enteric disease: epidemiological data from Sweden, 1980–1982. J Infect Dis 151: 476–481.
Hughes JM , Jarvis WR , 1987. Nosocomial gastrointestinal infections. In: Wenzel RP (ed.), Prevention and Control of Nosocomial Infections. Baltimore, MD: Williams & Wilkins, 405–439.
Riley TV , O’Neill GL , Bowman RA , Golledge CL , 1994. Clostridium difficile-associated diarrhoea: epidemiological data from Western Australia. Epidemiol Infect 113: 13–20.
Thomas C , Stevenson M , Williamson DJ , Riley TV , 2002. Clostridium difficile-associated diarrhea: epidemiological data from Western Australia associated with a modified antibiotic policy. Clin Infect Dis 35: 1457–1462.
Hirschhorn LR , Trnka Y , Onderdonk A , Lee MLT , Platt R , 1994. Epidemiology of community-acquired Clostridium difficile-associated diarrhea. J Infect Dis 169: 127–133.
McFarland LV , Mulligan ME , Kwok RY , Stamm WE , 1989. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 320: 204–210.
McDonald LC , Owings M , Jernigan DB , 2006. Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996–2003. Emerg Infect Dis 12: 409–415.
Dial S , Delaney JA , Barkun AN , Suissa S , 2005. Use of gastric acid-suppressive agents and the risk of community-acquired Clostridium difficile-associated disease. JAMA 294: 2989–2995.
Wren B , Clayton C , Tabaqchali S , 1990. Rapid identification of toxigenic Clostridium difficile by polymerase chain reaction. Lancet 335: 1.
Kato N , Ou CY , Kato H , Bartley SL , Brown VK , Dowell VR , Ueno K , 1991. Identification of toxigenic Clostridium difficile by the polymerase chain reaction. J Clin Microbiol 29: 33–37.
Clements ACA , Magalhaes RJS , Tatem AJ , Paterson DL , Riley TV , 2010. Clostridium difficile PCR ribotype 027: assessing the risks of further worldwide spread. Lancet Infect Dis 10: 395–404.
Pepin J , Valiquette L , Alary ME , Villemure P , Pelletier A , Forget K , Pepin K , Chouinard D , 2004. Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. CMAJ 171: 466–472.
Muto CA et al.2005. A large outbreak of Clostridium difficile-associated disease with an unexpected proportion of deaths and colectomies at a teaching hospital following increased fluoroquinolone use. Infect Control Hosp Epidemiol 26: 273–280.
He M et al.2013. Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nat Genet 45: 109–113.
Brazier JS , Raybould R , Patel B , Duckworth G , Pearson A , Charlett A , Duerden BI , Network HPARM , 2008. Distribution and antimicrobial susceptibility patterns of Clostridium difficile PCR ribotypes in English hospitals, 2007–08. Euro Surveill 13: 13.
Bauer MP , Notermans DW , van Benthem BHB , Brazier JS , Wilcox MH , Rupnik M , Monnet DL , van Dissel JT , Kuijper EJ , 2011. Clostridium difficile infection in Europe: a hospital-based survey. Lancet 377: 63–73.
Kuijper EJ et al.2008. Update of Clostridium difficile infection due to PCR ribotype 027 in Europe, 2008. Euro Surveill 13: 1–7.
Adler A , Schwartzberg Y , Samra Z , Schwartz O , Carmeli Y , Schwaber MJ , 2014. Trends and changes in Clostridium difficile diagnostic policies and their impact on the proportion of positive samples: a national survey. Clin Microbiol Infect 20: O904–O910.
Riley TV , Huovinen P , 2008. Infection control measures to limit the spread of Clostridium difficile. Introduction. Clin Microbiol Infect 14: 1.
Katz KC et al.2018. The evolving epidemiology of Clostridium difficile infection in Canadian hospitals during a postepidemic period (2009–2015). CMAJ 190: E758–E765.
Gessel HV , 2008. Measuring the incidence of Clostridium difficile-associated diarrhoea in a group of Western Australian hospitals. Healthc Infect 13: 56–62.
Goorhuis A , Bakker D , Corver J , Debast SB , Harmanus C , Notermans DW , Bergwerff AA , Dekker FW , Kuijper EJ , 2008. Emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078. Clin Infect Dis 47: 1162–1170.
Riley TV , Thean S , Hool G , Golledge CL , 2009. First Australian isolation of epidemic Clostridium difficile PCR ribotype 027. Med J Aust 190: 706–708.
Lim PL et al.2011. Isolation of the first three cases of Clostridium difficile polymerase chain reaction ribotype 027 in Singapore. Singapore Med J 52: 361–364.
Collins DA , Riley TV , 2018. Clostridium difficile guidelines. Clin Infect Dis 67: 1639.
Collins DA , Sohn KM , Wu Y , Ouchi K , Ishii Y , Elliott B , Riley TV , Tateda K , 2020. Clostridioides difficile infection in the Asia-Pacific region. Emerg Microbes Infect 9: 42–52.
Collins DA , Hawkey PM , Riley TV , 2013. Epidemiology of Clostridium difficile infection in Asia. Antimicrob Resist Infect Control 2: 21.
Warren CA , Labio E , Destura R , Sevilleja JE , Jamias JD , Daez ML , 2012. Clostridium difficile and Entamoeba histolytica infections in patients with colitis in the Philippines. Trans R Soc Trop Med Hyg 106: 424–428.
Oyofo BA et al.2002. Enteropathogens associated with acute diarrhea in community and hospital patients in Jakarta, Indonesia. FEMS Immunol Med Microbiol 34: 139–146.
Kurniawan A , Lugito NPH , Yanto TA , Tjiang MM , Setiadinata R , Wijaya I , Soemantri S , 2014. Clostridium difficile infection in elderly hepatocellular carcinoma patients in general hospital, Karawaci, Tangerang, Banten, Indonesia. J Geriatr Oncol 5: S17.
Seugendo M et al.2018. Prevalence and strain characterization of Clostridioides (Clostridium) difficile in representative regions of Germany, Ghana, Tanzania and Indonesia - a comparative multi-center cross-sectional study. Front Microbiol 9: 1843.
Collins DA , Gasem MH , Habibie TH , Arinton IG , Hendriyanto P , Hartana AP , Riley TV , 2017. Prevalence and molecular epidemiology of Clostridium difficile infection in Indonesia. New Microbes New Infect 18: 34–37.
Chrisnanda RH , Wardhani P , 2019. The incidence of Clostridium difficile infection in diarrhea patients after receiving antibiotics at Dr. Soetomo Hospital Surabaya. Bali Med J 8: 342–346.
Parasakthi N , Puthucheary SD , Goh KL , Sivanesaratnam V , 1988. Clostridium difficile associated diarrhoea: a report of seven cases. Singapore Med J 29: 504–507.
Hassan SA , Othman N , Idris FM , Abdul Rahman Z , Maning N , Abdul Rahman R , Tiong CG , 2012. Prevalence of Clostridium difficile toxin in diarhoeal stool samples of patients from a tertiary hospital in North Eastern Penisular Malaysia. Med J Malaysia 67: 402–405.
Zainul NH , Ma ZF , Besari A , Siti Asma H , Rahman RA , Collins DA , Hamid N , Riley TV , Lee YY , 2017. Prevalence of Clostridium difficile infection and colonization in a tertiary hospital and elderly community of north-eastern Peninsular Malaysia. Epidemiol Infect 145: 3012–3019.
Riley TV et al.2018. High prevalence of toxigenic and nontoxigenic Clostridium difficile strains in Malaysia. J Clin Microbiol 56: e00170–e00118.
Theseira L , 2021. Singapore-Country Commercial Guide. Available at: https://www.trade.gov/country-commercial-guides/singapore-healthcare. Accessed February 3, 2022.
Kumarasinghe G , Lim YS , Chow C , Bassett DC , 1992. Prevalence of bacterial agents of diarrhoeal disease in the National University Hospital, Singapore and their resistance to antimicrobial a gents. Trop Geogr Med 44: 229–232.
Lim PL , Barkham TM , Ling LM , Dimatatac F , Alfred T , Ang B , 2008. Increasing incidence of Clostridium difficile-associated disease, Singapore. Emerg Infect Dis 14: 1487–1489.
Koh TH , Tan AL , Tan ML , Wang G , Song KP , 2007. Epidemiology of Clostridium difficile infection in a large teaching hospital in Singapore. Pathology 39: 438–442.
Hsu LY , Tan TY , Koh TH , Kwa AL , Krishnan P , Tee NW , Jureen R , 2011. Decline in Clostridium difficile-associated disease rates in Singapore public hospitals, 2006 to 2008. BMC Res Notes 4: 77.
Chan M , Lim PL , Chow A , Win MK , Barkham TM , 2011. Surveillance for Clostridium difficile infection: ICD-9 coding has poor sensitivity compared to laboratory diagnosis in hospital patients, Singapore. PLOS One 6: e15603.
Tan XQ , Verrall AJ , Jureen R , Riley TV , Collins DA , Lin RT , Balm MN , Chan D , Tambyah PA , 2014. The emergence of community-onset Clostridium difficile infection in a tertiary hospital in Singapore: a cause for concern. Int J Antimicrob Agents 43: 47–51.
Chau ML , Hartantyo SH , Yap M , Kang JS , Aung KT , Gutierrez RA , Ng LC , Tam CC , Barkham T , 2016. Diarrheagenic pathogens in adults attending a hospital in Singapore. BMC Infect Dis 16: 32.
Wongwanich S , Ramsiri S , Vanasin B , Khowsaphit P , Tantipatayangkul P , Phan-urai R , 1990. Clostridium difficile-associated disease in Thailand. Southeast Asian J Trop Med Public Health 21: 367–372.
Thamlikitkul V , Danpakdi K , Chokloikaew S , 1996. Incidence of diarrhea and Clostridium difficile toxin in stools from hospitalized patients receiving clindamycin, beta-lactams, or nonantibiotic medications. J Clin Gastroenterol 22: 161–163.
Wongwanich S , Rugdeekha S , Pongpech P , Dhiraputra C , 2003. Detection of Clostridium difficile toxin A and B genes from stool samples of Thai diarrheal patients by polymerase chain reaction technique. J Med Assoc Thai 86: 970–975.
Chotiprasitsakul D , Janvilisri T , Kiertiburanakul S , Watcharananun S , Chankhamhaengdecha S , Hadpanus P , Malathum K , 2012. A superior test for diagnosis of Clostridium difficile-associated diarrhea in resource-limited settings. Jpn J Infect Dis 65: 326–329.
Putsathit P , Maneerattanaporn M , Piewngam P , Kiratisin P , Riley TV , 2017. Prevalence and molecular epidemiology of Clostridium difficile infection in Thailand. New Microbes New Infect 15: 27–32.
Imwattana K , Wangroongsarb P , Riley TV , 2019. High prevalence and diversity of tcdA-negative and tcdB-positive, and non-toxigenic, Clostridium difficile in Thailand. Anaerobe 57: 4–10.
Aanpreung P , Veerakul G , Chaichanwatanakul K , 1998. Clostridium difficile infection in febrile neutropenic malignancy children. Siriraj Hosp Gaz 50: 588–593.
Pupaibool J , Khantipong M , Suankratay C , 2008. A study of Clostridium difficile-associated disease in King Chulalongkorn Memorial Hospital, Thailand. J Med Assoc Thai 91: 37–43.
World Health Organization , 2005. The Treatment of Diarrhoea: A Manual for Physicians and Other Senior Health Workers, 4th Revision. Geneva, Switzerland: WHO.
Huong VTT , Hang PTT , Nga TT , Trang LT , Duong DTT , Canh TQ , 2018. Molecular characterization of Clostridium difficile isolates from patients with antibiotics-associated diarrhea in Hanoi, Vietnam. VJPM 28: 70.
Giang NTH , Thuy PTH , Huong VTT , Duong TN , 2019. Epidemiology and clinical manifestations of Clostridium difficile-associated diarrhea in adults in Bach Mai Hospital from 2013 to 2017. VJPM 29: 9.
Giang NTH , 2020. Characteristics of Epidemiology, Clinical Manifestations, and Risk Factors of Clostridium difficile Infection Among Adult Patients with Diarrhoea in Bach Mai Hospital from 2013 to 2017. Hanoi, Vietnam: Department of Epidemiology, National Institute of Hygiene & Epidemiology.
Giang NTH , Huong VTT , Thuy PTTT , Duong TN , 2019. Genotypic distribution characteristics of Clostridium difficile associated diarrhea in adult patients in Bach Mai Hospital from 2013 to 2017. VJPM 29: 18.
Liao F , Li W , Gu W , Zhang W , Liu X , Fu X , Xu W , Wu Y , Lu J , 2018. A retrospective study of community-acquired Clostridium difficile infection in southwest China. Sci Rep 8: 3992.
Warny M , Pepin J , Fang A , Killgore G , Thompson A , Brazier J , Frost E , McDonald LC , 2005. Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 366: 1079–1084.
Collins DA , Riley TV , 2018. Clostridium difficile in Asia: opportunities for One Health management. Trop Med Infect Dis 4: 7.
Cairns MD et al.2017. Comparative genome analysis and global phylogeny of the toxin variant Clostridium difficile PCR ribotype 017 reveals the evolution of two independent sublineages. J Clin Microbiol 55: 865–876.
Imwattana K , Knight DR , Kullin B , Collins DA , Putsathit P , Kiratisin P , Riley TV , 2019. Clostridium difficile ribotype 017 - characterization, evolution and epidemiology of the dominant strain in Asia. Emerg Microbes Infect 8: 796–807.
Imwattana K , Putsathit P , Collins DA , Leepattarakit T , Kiratisin P , Riley TV , Knight DR , 2022. Global evolutionary dynamics and resistome analysis of Clostridioides difficile ribotype 017. Microb Genom 8. https://doi.org/10.1099/mgen.0.000792.
Putsathit P , Neela VK , Joseph NMS , Ooi PT , Ngamwongsatit B , Knight DR , Riley TV , 2019. Molecular epidemiology of Clostridium difficile isolated from piglets. Vet Microbiol 237: 108408.
Zhang WZ , Li WG , Liu YQ , Gu WP , Zhang Q , Li H , Liu ZJ , Zhang X , Wu Y , Lu JX , 2020. The molecular characters and antibiotic resistance of Clostridioides difficile from economic animals in China. BMC Microbiol 20: 20.
Usui M , Nanbu Y , Oka K , Takahashi M , Inamatsu T , Asai T , Kamiya S , Tamura Y , 2014. Genetic relatedness between Japanese and European isolates of Clostridium difficile originating from piglets and their risk associated with human health. Front Microbiol 5: 513.
Ngamskulrungroj P , Sanmee S , Putsathit P , Piewngam P , Elliott B , Riley TV , Kiratisin P , 2015. Molecular epidemiology of Clostridium difficile infection in a large teaching hospital in Thailand. PLOS One 10: e0127026.
Lew T , Putsathit P , Sohn KM , Wu Y , Ouchi K , Ishii Y , Tateda K , Riley TV , Collins DA , 2020. Antimicrobial susceptibilities of Clostridium difficile isolates from 12 Asia-Pacific countries in 2014 and 2015. Antimicrob Agents Chemother 64: 1–11.
World Health Organization , 2017. One Health. Available at: https://www.who.int/features/qa/one-health/en/. Accessed December 10, 2020.
Squire MM , Riley TV , 2013. Clostridium difficile infection in humans and piglets: a ‘One Health’ opportunity. Curr Top Microbiol Immunol 365: 299–314.
Niwa H et al.2013. Postoperative Clostridium difficile infection with PCR ribotype 078 strain identified at necropsy in five thoroughbred racehorses. Vet Rec 173: 607.
Eyre DW et al.2013. Diverse sources of C. difficile infection identified on whole-genome sequencing. N Engl J Med 369: 1195–1205.
Lim SC , Knight DR , Riley TV , 2020. Clostridium difficile and One Health. Clin Microbiol Infect 26: 857–863.
Knight DR , Squire MM , Collins DA , Riley TV , 2016. Genome analysis of Clostridium difficile PCR ribotype 014 lineage in Australian pigs and humans reveals a diverse genetic repertoire and signatures of long-range interspecies transmission. Front Microbiol 7: 2138.
Rupnik M , 2007. Is Clostridium difficile-associated infection a potentially zoonotic and foodborne disease? Clin Microbiol Infect 13: 457–459.
Songer JG , Trinh HT , Killgore GE , Thompson AD , McDonald LC , Limbago BM , 2009. Clostridium difficile in retail meat products, USA, 2007. Emerg Infect Dis 15: 819–821.
Bakri MM , Brown DJ , Butcher JP , Sutherland AD , 2009. Clostridium difficile in ready-to-eat salads, Scotland. Emerg Infect Dis 15: 817–818.
Tsai BY , Ko WC , Chen TH , Wu YC , Lan PH , Chen YH , Hung YP , Tsai PJ , 2016. Zoonotic potential of the Clostridium difficile RT078 family in Taiwan. Anaerobe 41: 125–130.
|Past two years||Past Year||Past 30 Days|
|Full Text Views||103||103||5|
This review describes the current understanding of Clostridium (Clostridioides) difficile infection (CDI) in southeast Asia regarding the prevalence of CDI, C. difficile detection methods, antimicrobial susceptibility profiles, and the potential significance of a One Health approach to prevention and control. Our initial focus had been the Indochina region, however, due to limited studies/surveillance of CDI in Indochina, other studies in southeast Asian countries and neighboring Chinese provinces are presented here for comparison. Clostridium (Clostridioides) difficile infection is one of the most common causes of hospital-acquired gastroenteritis worldwide. Since its discovery as a cause of pseudomembranous colitis in 1978, C. difficile-related disease has been more prevalent in high-income rather than low-income countries. This may be because of a lack of knowledge and awareness about the significance of C. difficile and CDI, resulting in underreporting of true rates. Moreover, the abuse of antimicrobials and paucity of education regarding appropriate usage remain important driving factors in the evolution of CDI worldwide. The combination of underreporting of true CDI rates, along with continued misuse of antimicrobial agents, poses an alarming threat for regions like Indochina. C. difficile ribotype (RT) 027 has caused outbreaks in North America and European countries, however, C. difficile RT 017 commonly occurs in Asia. Toxin A-negative/toxin B-positive (A−B+) strains of RT 017 have circulated widely and caused outbreaks throughout the world and, in southeast Asia, this strain is endemic.
Authors’ addresses: Peng An Khun, School of Biomedical Sciences, The University of Western Australia, Western Australia, Australia, E-mail: firstname.lastname@example.org. Thomas V. Riley, School of Biomedical Sciences, The University of Western Australia, Western Australia, Australia, School of Medical and Health Sciences, Edith Cowan University, Joondalup, Western Australia, Australia, Medical, Molecular and Forensic Sciences, Murdoch University, Murdoch, Western Australia, Australia, and Department of Microbiology, PathWest Laboratory Medicine, Nedlands, Western Australia, Australia, E-mail: email@example.com.