786 infection control & hospital epidemiology july 2018, vol. 39, no. 7
hospitalization was a risk factor for C. difficile colonization. We identified 8 episodes (5 isolates were ribotype 002) and 16 episodes (5 isolates were ribotype 002) of possible C. difficile acquisition in hospitals and nursing homes, respectively. Other significant factors associated with C. difficile coloni-
zation included bedbound state, presence of hepatic diseases, and prior exposure to penicillin-group antibiotics. Because of the relatively small sample size, the use of a proton pump inhibitor did not reach statistical significance (P=.051). Notably, the presence of a nasogastric tube was an independent risk factor for C. difficile colonization, which was also asso- ciated with CDI and the colonization or infection caused by other multidrug-resistant organisms.18–20 Some have postu- lated that disruption in normal gut flora and dependence on nursing home staff for enteral feeding led to an increased risk
of acquiring colonization through the fecal–oral route.19 Our findings are only partially in agreement with those of a recently published meta-analysis which demonstrated that a history of CDI, prior hospitalization, and antimicrobial use were sig- nificant factors linked to C. difficile carriage.14 The different study settings might account for the discrepancy. In contrast to our study, which included multiple facilities in a nonepidemic setting, most of the studies included in the meta-analysis were performed in single facilities, and half of these were preceded by CDI outbreaks.14 Our data, therefore, are useful for formulating infection control policies targeted at asymp- tomatic C. difficile carriers in a nonoutbreak, long-term care setting. In the prospective part of the study, we showed that a
moderately high rate of toxigenic C. difficile acquisition (7.3%) occurred over a median period of 29 weeks in a nonepidemic setting. The C. difficile isolates acquired in nursing home H (N=4), nursing home F (N=3), and nursing home E (N=2 each) belonged to ribotypes 029, 014, 053 and 002, respec- tively. Considering the high degree of genetic relatedness with the same ribotype,21 intrafacility transmissions were indicated. This finding contrasts with that of another study performed more than 20 years ago in which a similar rate of C. difficile acquisition was reported but with little evidence of cross infection.22 This difference could be due to the changing characteristics of residents and the epidemiology of C. difficile in LTCFs over time. Our study provides additional data about the extended
duration over which C. difficile colonized individuals may revert to a noncolonized state. The Kaplan-Meier estimate of median carriage duration was 13 weeks; nevertheless, 2 resi- dents (5.7%) had persistent positive cultures beyond 10 months. The marked variation in duration of colonization has also been shown in other longitudinal studies; colonization for >3 months ranged from 0 to 19%.22,23 In facilities where standard measures fail to control C. difficile transmission, screening and performing contact precautions on colonized residents should be considered. Our study has a few limitations. First, 75 residents did not consent to the study. The sample size was relatively small; and
the multivariable analysis included only 18 outcome events, namely, C. difficile colonized residents of the 4 nursing homes at baseline. The 95% CI of the only significant independent vari- able—presence of nasogastric tube—was very wide, which indicates that our data might not be representative. Second, the CDI history of residents could not be reliably obtained because C. difficile toxin testing was requested for a minority of diarrheal patients. Third, molecular typing was performed for the first C. difficile strain isolated from each resident. For residents with persistent carriage, repeated acqui- sition could not be excluded. Finally, our sampling frequency might not have been great enough to accurately determine the duration of C. difficile carriage and the origin of acquisition. In summary, our study demonstrates that nursing home residents in Hong Kong are at substantial risk of C. difficile colonization and acquisition. Carriage could be prolonged for >3 months for most patients. The presence of a nasogastric tube was an independent risk factor associated with carriage. This finding underscores the importance of adherence to hand hygiene in procedures such as diaper change and nasogastric tube feeding. The predominance of C. difficile ribotype 002 confirms that nursing homes are epicenters of sustained transmission across the continuum of care.
acknowledgments
We are grateful to the nursing home staff who helped collect the stool samples. We thank Ms Eleanor Ma for liaison with the nursing home staff. Financial support: No financial support was provided relevant to this article. Potential conflicts of interest: All authors report no conflicts of interest rele-
vant to this article. Address correspondence to Dr Shik Luk, 12/F, Department of Pathology,
Block G, Princess Margaret Hospital, Hong Kong, China (
sluk@ha.org.hk).
references 1. Magill SS, Edwards JR, Bamberg W, et al. Multistate point- prevalence survey of health care-associated infections. N Engl J Med 2014;370:1198–1208.
2. Wong SH, Ip M, Hawkey PM, et al. High morbidity and mortality of Clostridium difficile infection and its associations with ribotype 002 in Hong Kong. J Infect 2016;73:115–122.
3. Cheng VCC, Yam WC, Lam OTC, et al. Clostridium difficile iso- lates with increased sporulation: emergence of PCR ribotype 002 in Hong Kong. Eur J Clin Microbiol Infect Dis 2011;30:1371–1381.
4. Curry SR, Muto CA, Schlackman JL, et al. Use of multilocus variable number of tandem repeats analysis genotyping to determine the role of asymptomatic carriers in Clostridium diffi- cile transmission. Clin Infect Dis 2013;57:1094–1102.
5. Riggs MM, Sethi AK, Zabarsky TF, Eckstein EC, Jump RLP, Donskey CJ. Asymptomatic carriers are a potential source for transmission of epidemic and nonepidemic Clostridium difficile strains among long-term care facility residents. Clin Infect Dis 2007;45:992–998.
6. Jinno S, Kundrapu S, Guerrero DM, Jury LA, Nerandzic MM, Donskey CJ. Potential for transmission of Clostridium difficile by asymptomatic acute care patients and long-term care facility
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