Infection Control & Hospital Epidemiology
Table 3. Distribution of Restriction Endonuclease Analysis Types for 37 Healthcare-Associated Clostridium difficile Infection Cases and 29 Long-Term Care Facility Residents With Asymptomatic Carriage of Toxigenic C. difficilea
REA Group BI
DQ
Nonspecific type J
G M
BK DH
Other
C. difficile Infection, No. (%)b
13 (35.1) 8 (21.6) 5 (13.5) 2 (5.4) 2 (5.4) 2 (5.4) 2 (5.4) 0
3 (8.1)
Asymptomatic Carriage, No. (%)b
11 (37.9) 5 (17.2) 2 (6.9) 1 (3.4) 0 0
1 (3.4)
3 (10.3) 4 (13.8)
NOTE. REA, restriction endonuclease analysis. aAsymptomatic carriers were detected by rectal screening of current residents and new admissions to the long-term care facility between February 16, 2012, and August 31, 2012;
C. difficile cases included those diagnosed between March 1, 2012, and August 31, 2012. bData are no. (%) of patients, unless otherwise specified.
recipient CDI cases for each putative transmission. The 5 transmissions linked to asymptomatic carriers were attributed to 4 carriers. Furthermore, 2 of the carriers linked to transmission events were colonized with identical (ie, 0 SNP differences) REA BI group 1 strains (Fig. 2A); thus, either carrier was considered a potential source. Each of the carriers linked to transmission was a persistent carrier with >25 colonies of C. difficile recovered from perirectal swab cultures and positive groin, skin, and/or envir- onmental cultures on 1 or more occasions (Table 2). Of 4 carriers linked to transmission, 3 (75%) had previous CDI: 2 carriers had had CDI within the past 90 days, and 1 carrier had had CDI 6 years prior to the transmission event. In addition to the 7 putative transmissions based on 2 or fewer
SNP differences, 3 possible transmission events were based on 4 SNP differences between donor and recipient strains. Among them, 2 of the putative donors carried epidemic BI strains and 1 carried the binary toxin-positive DQ strain. Only 1 of the 3 possible transmission events involved direct ward exposure.
Discussion
In a Veterans Affairs hospital and its affiliated LTCF, we found that 19% of healthcare-associated CDI cases were linked to LTCF residents with asymptomatic carriage of toxigenic C. difficile or LTCF-associated CDI. The epidemic BI strain was the most common strain type recovered from CDI cases and asymptomatic carriers, and this strain accounted for all transmission events. These results suggest that LTCF residents with asymptomatic carriage of C. difficile or CDI may contribute substantially to transmission in LTCFs and in hospitals during acute-care admissions. Although 19% of healthcare-associated CDI cases could be
linked to LTCF residents, the source of the remaining 81% of cases is unknown. Based on REA typing and ward exposures, approximately one-third of hospital-associated CDI cases were potentially linked to other hospital-associated cases. However, none of these potential linkages met criteria for transmission
913
based on WGS analysis. In addition, no nonward-based linkages were identified between hospital-associated CDI cases. Our results are consistent with other recent studies that demonstrated that a minority of hospital-associated CDI cases may be linked to other hospital-associated cases based on highly discriminatory mole- cular typing methods such as WGS.26 Notably, the lack of transmission by CDI cases in the study facility occurred in the context of intensive efforts to improve environmental disinfection and a C. difficile stewardship initiative that included isolation of patients with suspected CDI.17,28 Asymptomatic carriers in the hospital are a potential source of transmission that was not accounted for in our study because we did not screen for asymptomatic carriage in the hospital. In a previous culture survey in our facility, only 6% of hospitalized patients with asymptomatic carriage of toxigenic C. difficile were LTCF residents.29 Several recent studies that have suggested that asymptomatic carriers may be an underappreciated source of transmission.12–14 Curry et al12 reported that incident CDI cases in a tertiary-care hospital were linked as frequently to asympto- matic carriers as to symptomatic CDI cases. Longtin et al13 reported that a hospital-based intervention involving detection and isolation of C. difficile carriers was associated with a sig- nificant decrease in the incidence of healthcare-associated CDI. Neither of these studies reported the proportions of carriers that were transferred from LTCFs. A novel aspect of our study is that we included an assessment
of the potential for transmission by asymptomatic carriers based on the burden of carriage and the presence of skin and/or environmental shedding.15 All 4 of the carriers linked to trans- mission had a relatively high burden of carriage (ie, >25 colonies per perirectal swab) and groin, skin, and/or environmental shedding, suggesting that such carriers may present the greatest risk for transmission. In addition, 2 of the carriers linked to transmission had recent CDI with continued asymptomatic shedding of spores after treatment and one had been diagnosed with CDI 6 years prior to the study. We have previously demonstrated that asymptomatic shedding of spores is common after CDI treatment.7,16 In this study, 3 putative transmissions linked to LTCF resi-
dents occurred in the absence of ward exposure. For each transmission, the donor was an LTCF resident with asymptomatic carriage and the recipient was an LTCF resident on a separate ward who developed LTCF-associated CDI. Other investigators have also reported that many transmissions identified using highly discriminatory molecular typing methods are nonward based. Curry et al.12 found that more than half of transmissions linked to asymptomatic carriers and to CDI cases had no shared ward exposure. Eyre et al26 reported that 9% of transmissions based on WGS occurred in patients who shared time in the hospital but were never on the same ward. Such nonward transmissions might occur due to staff members working on multiple wards or direct or indirect contact between patients or LTCF residents. Our study has several limitations. The study population was predominantly male, and the epidemic BI strain was the most common strain type recovered. Additional studies are needed in other settings. Our results may underestimate the importance of LTCF residents in transmission because not all eligible LTCF residents were enrolled and LTCF residents transferred from community facilities were not included in the study. As noted previously, our results also underestimate the contribution of asymptomatic carriers to transmission in the hospital because we
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