Prospective, Controlled Study of Vinyl Glove Use to Interrupt clostridium difficile Nosocomial Transmission STUART JOHNSON, M.D., DALE N. GERDING, M.D., MARY M. OLSON, R.N., MARY D. WEILER, R.N., RITA A. HUGHES, M.T., CONNIE R. CLABOTS, M.T., LANCER. PETERSON, M.D. Minneapolis, Minnesota

PURPOSE Despite recognition that Clostridizzm diffide diarrhea/colitis is a nosocomial infection, the manner in which this organism is transmitted is still not clear. Hands of health care workers have been shown to be contaminated with C. d7.S tile and suggested as a vehicle of transmission. Therefore, we conducted a controlled trial of the use of disposable vinyl gloves by hospital personnel for all body substance contact (prior to the institu- tion of universal body substance precautions) to study its effect on the incidence of C. dY.fKcae dis- ease.

PATIENTS AND MEXHODS: The incidence of nosoco- mial C. &IM.Ze diarrhea was monitored by active surveillance for six months before and after an in- tensive education program regarding glove use on kvo hospital wards. The interventions included ini- tial and periodic in-services, posters, and place- ment of boxes of gloves at every patient’s bedside. Two comparable wards where no special interven- tion was instituted served as controls.

RESULTS: A decrease in the incidence of C. cZXfi- tile diarrhea from 7.7 cases/l,000 patient dis- charges during the six months before intervention to 1.5/1,000 during the six months of intervention on the glove wards was observed (p = 0.015). No significant change in incidence was observed on the two control wards during the same period (5.71 1,000 versus 4.2/1,000). Point prevalence of asymp- tomatic C. &.fEcae carriage was also reduced sig- nificantly on the glove wards but not on the con- trol wards after the intervention period (glove wards, 10 of 37 to four of 43, p = 0.029; control wards, five of 30 to five of 49, p = 0.19). The cost of 61,500 gloves (4,505 gloves/100 patients) used was $2,768 on the glove wards, compared with $1,895 (42,100 gloves; 3,532 gloves/100 patients) on the con- trol wards.

CONCLUSIONS: Vinyl glove use was associated with a reduced incidence of C. &EciZe diarrhea and is indirect evidence for hand carriage as a means of nosocomial C. dif”tcae spread.

From the Infectious Disease Section, Department of Medicine, the Microbi- ology Section, Department of Laboratory Medicine and Pathology, Veter- ans Administration Medical Center, and University of Minnesota Medical School, Minneapolis, Minnesota. This work was presented in part at the 88th Annual Meeting of the American Society for Microbiology, Miami Beach, Florida, May 8-13. 1988, and was supported by the Veterans Ad- ministration and the National Foundation for Infectious Diseases/Beecham Laboratories 1987 Postdoctoral Fellowship in Nosocomial Infection Re- search (SJ). Requests for reprints should be addressed to Dale N. Gerding, M.D., lnfectrous Disease Sectton/lllF, MVAMC, 1 Veterans Drive, Minne- apolis, Minnesota 55417. Manuscript submitted July 18, 1989, and accept- ed In revised form December 6. 1989.

C lostridium difficile is an important cause of colitis and diarrhea in patients exposed to certain antibi-

otics [1,2]. In addition to the risk of antibiotic expo- sure, there is a growing consensus that C. difficile is acquired nosocomially. The prevalence of asymptom- atic C. difficile carriage is high in hospitalized popula- tions [2,3] and low in the general adult population [4,5], and numerous hospital outbreaks and case clus- ters have been reported [3,6-lo]. The mode of C. diffi- tile transmission, however, is not clear. C. difficile has been recovered from the environment and from poten- tial fomites, but most studies show high recovery rates only in the immediate environment of clinical cases or from likely contaminated items such as toilet seats or bedpans [11,12]. The relative importance of fomite or environmental acquisition in the hospital transmis- sion of C. difficile remains unknown.

C. difficile has also been recovered from the hands of hospital personnel [13-161. Transmission of C. diffi- tile from patient to patient via the hands of hospital personnel may be an important mode of transmission that could be interrupted by the use of gloves by per- sonnel when handling body substances, particularly feces. To test this hypothesis, we studied the effect of intensive vinyl glove use for all body substance contact as a means to reduce the incidence of C. difficile-asso- ciated diarrhea and asymptomatic carriage on two hospital wards.

PATIENTS AND METHODS Active surveillance of C. difficile-associated diar-

rhea was performed throughout the study period (July 1,1986, to July 31,1987) by daily review of all positive cultures and cytotoxin assays for C. difficile in the clinical microbiology laboratory and follow-up of the patients. Both culture and toxin assays are routinely performed at the Minneapolis Veterans Administra- tion Medical Center (MVAMC) when C. difficile-asso- ciated diarrhea/colitis is suspected. C. difficile diar- rhea was defined as a minimum of six unformed bowel movements in a 36-hour period in a patient with a positive stool culture and/or cytotoxin assay for C. difficile, or endoscopic evidence of pseudomembran- ous colitis and no other explanation for diarrhea [2]. All potential cases were investigated by one observer (M.M.O.),. and diarrhea was not attributed to C. diffi- tile if cathartics, enteral feedings, inflammatory bowel disease, or other diarrheaI pathogens were present. Only nosocomial cases were included in this analysis. Cases were defined as nosocomial if diarrhea started more than 48 hours after hospital admission or, for patients with diarrhea at admission, if they had been hospitalized within the previous two weeks (the case was then attributed to the ward from that previous hospitalization). Vinyl glove usage was determined from the hospital supply record of distribution of box-

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GLOVE USE AND C. DIf~/C/~ETRANSMlSSlON / JOHNSON ET AL

es of gloves (100 gloves/box) to individual wards. The record of glove distribution for the first six-month period of study (prior to the intervention) was not available; however, glove use for the whole hospital increased during these two time periods: 848.3 boxes of gloves/month from July to December 1986 to 1,099.5 boxes/month from February to July 1987 (p <0.05).

Four hospital wards with historically high inci- dences of C. difficile diarrhea were chosen for study: two surgical (5B, a 46-bed ward; and 3A, a 40-bed ward) and two medical wards (5AW, a 40-bed ward; and 6B, a 44-bed ward). The study was divided into two six-month periods: the first period before inter- vention (July 1,1986, to December 31,1986) and the intervention period (January 22, 1987, to July 31, 1987). The two periods were separated by a three-week intensive education period regarding glove use when handling any body substances (blood, urine, feces, sputum, and other fluids or secretions), which was given to the nursing staff on one surgical and one med- ical ward, 5B and 5AW, hereafter referred to as the “glove” wards. Education consisted of in-services, posters specifically directed at wearing gloves when handling stool (Figure I), and follow-up visits that were continued throughout the second six-month peri- od. In addition, for user convenience, boxes of vinyl gloves were placed at each patient’s bedside and re- placed when empty. The other two wards (3A and 6B) served as control wards, where no special intervention was instituted. Vinyl gloves were stocked in supply rooms on these wards, but were not placed at the bed- side. Hospital policy throughout the entire study was to place patients with C. difficile diarrhea in private rooms with enteric precautions if they were inconti- nent of stool or unable to use good hygiene in manag- ing their diarrhea.

Stool specimens and rectal swabs were cultured for C. difficile using selective CCFA media (cefoxitin 16 pg/mL, cycloserine 500 pg/mL, fructose agar) and in- cubated anaerobically for 48 hours [17]. The point prevalence of C. difficile carriage was determined by rectal swab culture of all patients on the study wards on December 29, 1986, and on August 5, 1987. The swabs (Culturette, Marion Laboratories, Kansas City,

Figure 1. Educational reminder posted at nursing stations on the two glove wards. (Poster concept courtesy of Robert A. Weinstein, M.D., Michael Reese Medical Center, Chicago, Illi- nois).

Missouri) were transported to the laboratory within 30 minutes of collection and have been shown to be of comparable sensitivity to stool culture [2,18]. Rinses of hands of 10 randomly selected personnel (five nurses and five physicians) per ward were cultured unan- nounced on two occasions using a CCFB broth rinse technique whereby 30 mL of reduced CCFB (cefoxitin 8 pg/mL, cycloserine 250 pg/mL, fructose broth) was poured over the hands, incubated anaerobically for 48 hours, and subcultured onto selective and non-selec- tive agar media [19,20]. Appropriate positive (inocula- tion of broth with C. difficile strain ATCC 9689) and negative control broth samples were processed simul- taneously. C. difficile isolates were identified by colo- ny morphology, Gram stain, and gas-liquid chroma- tography. C. difficile cytotoxin assay was performed on filtered stool supernatants using HEp-2 cell mono- layers and confirmed by Clostridium sordellii antitox- in neutralization [21].

Fisher’s exact test was used to compare the inci- dence of C. difficile diarrhea and carriage prevalence on the glove and control wards.

RESULTS The incidence of C. difficile diarrhea was 7.7 cases

per 1,000 patient discharges (n = 1,171) on the glove wards during the six months prior to intervention, which decreased to 1.5 per 1,000 (n = 1,365) during the six months of intensive gloving (p = 0.015). There was no significant change in the incidence of C. difficile diarrhea on the control wards during the same time period [5.7 per 1,000 (n = 1,230) versus 4.2 per 1,000 (n = 1,192) (p = 0.20, Figure 2, Table I)]. One case of C. difficile diarrhea occurred on a control ward during the 21 days between the two study periods and was not included in the analysis. The incidence of C. difficile diarrhea in the hospital as a whole was the same during both time periods [3.2 cases per 1,000 patient dis- charges (n = 9,999) from July through December 1986 and 3.2 cases per 1,000 (n = 10,386) from February through July 19871. Case ascertainment bias could not explain the difference in diarrheal incidence between the glove and control wards as more C. difficile cul- ture/toxin assays were ordered per 100 patients on the

138 February 1990 The American Journal of Medicine Volume 88

GLOVE USE AND C. DIFFICILETRANSMISSION / JOHNSON ET AL

Figure 2. Cases of C. diticilediarrhea by month on the glove and control wards. One case occurred on a control ward during the education period between the study periods (January 1 to 21, 1987) and is not included in the figure.

3

GLOVE INTERVENTION

1 GLOVE

lx 5- it (

NO

INTERVENTION 1

5 4- I 2 I CONTROL I !

3- WARDS I 1 I I

2- - ’ I I

I -

I I

I 1 I I 1 I I I JASONDJFMAMJJ

MONTH

glove wards than on the control wards [8.9/100 (n = 1,365) versus 5.7/100 (n = 1,192, p <0.05)]. The num- ber of tests ordered on the glove wards before the intervention (9.9/100, n = 1,171) was not significantly different after the intervention (8.9/100, n = 1,365). The patients on the glove wards and the control wards were also similar with respect to mean age (65.3 years versus 64.2 years, p >0.5) and length of hospitalization (8.3 days versus 9.2 days, p >O.l). The incidence of C. difficile diarrhea was lower on the glove wards (1.5/ 1,000) than on the control wards (4.2/1,000) during the intervention period, but this was not significant (p = 0.14).

The point prevalence of C. difficile carriage was de- termined just before and after the second six-month period by rectal swab cultures of all patients on the four wards at those times. The asymptomatic C. diffi- tile colonization rate was lower after the study on all four wards, although the change was significant on the glove wards only. Twenty-seven percent of the pa- tients (10 of 37) were colonized prior to the interven- tion period, compared with 9% (four of 43) after the intervention on the glove wards (p = 0.029, Table I). The difference in prevalence from 17% (five of 30) to 10% (five of 49) on the control wards was not signifi- cant (p = 0.19, Table I). There was no significant dif- ference in C. difficile point prevalence between the glove and control wards before (p = 0.14) or after the intervention period (p = 0.27, Table I).

Usage of gloves on glove wards during the second six-month period was 61,500 at a cost of $2,768. How- ever, 42,100 gloves (cost $1,895) were used on the con- trol wards. The mean glove use per 100 patients per month was 4,539 on the glove wards compared with 3,603 on the control wards (0.1 < p < 0.5). Hand cul- tures of 80 personnel (five nurses and five physicians from each ward) taken unannounced prior to and at the end of the glove intervention period were all nega- tive for C. difficile.

COMMENTS The incidence of C. difficile diarrhea was signifi-

cantly reduced on two hospital wards during a period of intensive personnel gloving, whereas the incidence was unchanged on two wards without intervention during the same time period. The reduction occurred at a time when the overall hospital incidence was un- changed. This study provides indirect evidence that personnel hand carriage is an important means of no- socomial C. difficile transmission. Contamination of the hands of hospital personnel, however, was not doc- umented during either of the two surveys in this study. Other investigators have both documented 113-161 and failed to document hand carriage [7,9,22]. A broth rinse technique was used for hand cultures during this

L cc f( tF *t §F

TABLE I

C. difficiile Diarrhea Incidence and Carriage Prevalence before and after Institution of Intensive Vinyl Glove Use on the Glove Wards

Wards

Six Months Before Six Months After CD CD CD CD

Diarrhea Carriage Diarrhea Carriage p Incidence* Prevalence7 Incidence* Prevalence5 Value

Glove wards ::w 5/488

4/683 Total Total g/1,171

Control Wards 2 3/438

4/792 Total Total 7/1,230

:;:i 10/37

l/11 4/19 5/30

l/473 l/892

2/1,365

l/16 3/27 4/43 0.029

0.015

5/1,192

l/18 4/31 5/49

) = C. dffW/e; NS = not wgnificant. Zases of C. difficile per patient d&charge from July 1, 1986, to December 31, 1986. ‘omt prevalence of CD carnage by patients on December 29, 1986. :ases per patlent discharge from January 22. 1987, to July 31, 1987. ‘oint prevalence of CD carriage by patients on August 5, 1987.

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GLOVE USE AND C. D/Ff/C/~ETRANSMISSION / JOHNSON ET AL

study because of negative results in the past at this institution when using an agar hand/finger impression technique [2]. A recent study documented positive hand cultures for C. difficile (by agar hand/finger im- pression) in 59% of health care workers who had con- tact with infected patients by culturing workers’ hands immediately after patient contact [23]. It is like- ly that hand carriage of C. difficile is a transient, albeit important, phenomenon. The 80 personnel from whom cultures were obtained in this study may not have been an adequate sample population to docu- ment hand carriage, or the broth rinse technique may be inadequate for detecting anaerobic bacteria on hands.

Glove usage on the control wards was higher than expected and suggested “contamination” of the con- trol group by interventive practices. High glove use on the control wards may have been due, in part, to the rising concern of AIDS risk to health care workers [24], but formal introduction of universal body substance precautions to this medical center did not occur until April 1988, well after completion of this study. Alter- natively, exchange of patient care information be- tween control-ward and glove-ward personnel may have led to increased glove use on the control wards. The trend toward decreased asymptomatic C. difficile colonization of the patients on all four wards may also have been a reflection of this “contamination,” but the change was statistically significant on the glove wards only.

Despite higher-than-expected control ward glove usage, a significant decrease in C. difficile diarrhea and asymptomatic carriage on the glove wards was nonetheless documented. The nurses on the glove wards gave positive feedback regarding the ready ac- cessibility of vinyl gloves on their wards and this may have been the key intervention in our study. Data regarding efficacy of gloving as a barrier isolation tech- nique are limited [25,26]. The findings of this study support the effectiveness of glove use when handling body substances, as recommended by Body Substance Isolation policies [25], to interrupt transmission of mi- croorganisms such as C. difficile.

There is no reason that a carefully followed hand- washing policy should not be as effective at interrupt- ing C. difficile spread as the gloving policy used in this study. However, achieving high-level compliance with handwashing has always been difficult, and recent data suggest that use of a non-disinfectant soap is not effective in eliminating C. difficile from hands [23]. Based on data from this study, we recommend review of patient care practices regarding body substance contact and use of vinyl gloves as a means to interrupt C. difficile transmission when nosocomial C. difficile diarrhea is a concern.

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