Center for Child Health Care Studies, Department of Ambulatory Care and Prevention, Harvard Pilgrim Health Care and Harvard Medical School, Boston, Massachusetts
Division of Infectious Diseases, Children's Hospital Boston, Boston, Massachusetts
Department of Population and International Health, Harvard Center for Population and Development Studies, Harvard School of Public Health, Boston, Massachusetts
International Health Institute and Department of Pediatrics, Brown University, Providence, Rhode Island
Clinical Research Institute, Tufts–New England Medical Center, Boston, Massachusetts
ABSTRACT
Objectives. The widespread use of child care has altered the epidemiology of respiratory and gastrointestinal (GI) infection in the community. Our primary objective was to measure transmission of respiratory and GI illnesses among families with children enrolled in child care. We also sought to examine potential predictors of reduced illness transmission in the home in a secondary analysis.
Methods. We performed an observational, prospective cohort study to determine transmission rates for respiratory and GI illnesses within families with at least 1 child between 6 months and 5 years of age enrolled in child care. A survey about family beliefs and practices was mailed at the beginning of the study. Symptom diaries were provided for families to record the timing and duration of respiratory and GI illnesses. To ensure the accuracy of symptom diaries, biweekly telephone calls were performed to review illnesses recorded by participants. Families with 4 weeks of data recorded were included in the analysis. Families were recruited from 5 pediatric practices in the metropolitan Boston area. Of 261 families who agreed to participate in the study, 208 were available for analysis. Secondary transmission rates for respiratory and GI illnesses were measured as illnesses per susceptible person-month.
Results. We observed 1545 respiratory and 360 GI illnesses in 208 families from November 2000 to May 2001. Of these, 1099 (71%) respiratory and 297 (83%) GI illnesses were considered primary illnesses introduced into the home. The secondary transmission rates for respiratory and GI illnesses were 0.63 and 0.35 illnesses per susceptible person-month, respectively. Only two thirds of respondents correctly believed that contact transmission was important in the spread of colds, and fewer than half believed that it was important in the spread of stomach flus. Twenty-two percent of respondents reported use of alcohol-based hand gels all, most, or some of the time; 33% reported always washing their hands after blowing or wiping a nose. In multivariate models, use of alcohol-based hand gels had a protective effect against respiratory illness transmission in the home.
Conclusions. In homes with young children enrolled in child care, illness transmission to family members occurs frequently. Alcohol-based hand gel use was associated with reduced respiratory illness transmission in the home.
Key Words: child care illness transmission respiratory gastrointestinal alcohol-based hand gels
Abbreviations: GI, gastrointestinal
In 1999, 7.5 million children who were younger than 5 years were enrolled in child care in the United States.1 These numbers continue to rise as women enter the workforce in greater numbers and the number of single-parent homes climbs.2 In turn, the widespread use of child care facilities has influenced the epidemiology of infectious diseases in the community.3 Viral upper respiratory and gastrointestinal (GI) infections are the 2 most common illnesses that occur among those enrolled in child care.4–12 The concentration of young children whose developmental status promotes transfer of secretions via contaminated hands of caregivers and objects results in enhanced transmission of these infections within the child care setting.13,14
An illness in a child may affect not only that child but also parents, who may miss work to care for a sick child, or any family member because of secondary illness transmission.3,15–20 Within families, secondary attack rates can be as high as 27% for respiratory illnesses and 70% for gastroenteritis.21–24 In addition, intrafamilial spread compounds the economic impact of child care–associated infections.25–27
Previous studies have focused on interrupting the spread of transmission of infection through improved hand hygiene within child care facilities and elementary schools.28–36 However, few studies have focused on potential hand hygiene interventions in the home setting. In 1979, Hendley et al37 studied 22 families in a crossover study using iodine to disinfect hands. When a person was sick at home, the mother was instructed to dip her hands in iodine every 3 to 4 hours. The secondary attack rate was 7% in the iodine group compared with 20% in the control group. It was an effective but intensive intervention for which compliance rates may have been exceptionally high (96%) because study nurses observed practices in the home. Although not a practical intervention, this study provided important "proof of concept" for the potential role of hand antisepsis in reducing the risk for transmission in the home. More recently, Larson et al38 conducted a randomized, double-blind, clinical trial that examined the effect of antibacterial handwashing and cleaning products on infectious disease symptoms in the home. The authors found no significant difference between the intervention group that received antibacterial products and the control group, although these products may not have had optimal antiviral efficacy.
Waterless alcohol-based hand gels are considerably more convenient than traditional sink-based hand hygiene. Use of these gels is now widely advocated in health care settings because studies have demonstrated virucidal activity and reduced antimicrobial counts on hands of health care workers who use these agents.39,40 Alcohol-based hand gels also are associated with reduced illness and absenteeism in schools.36,41,42 Finally, these hand gels have been associated with improved compliance likely as a result of ease of use,43–45 which may be particularly important for busy caregivers, whether in child care, school, or home.
Unless other effective prevention strategies become available, such as vaccines for colds and gastroenteritis, hand hygiene will continue to play a key role in preventing transmission of infections in the home setting. Our objective was to perform a descriptive study to measure secondary illness transmission among families with children in child care. In addition, we explored potential predictors of reduced illness transmission in the home.
METHODS
Study Design and Study Population
We performed an observational, prospective cohort study to determine transmission rates for respiratory and GI illnesses within families with children enrolled in child care. The study was reviewed and approved by the Institutional Review Boards of Children's Hospital Boston and Harvard Pilgrim Health Care. Families were recruited from 5 pediatric practices in the metropolitan Boston area. We chose 3 urban practices and 2 suburban practices to include a diverse study population with respect to socioeconomic status and race/ethnicity. A random-number generator was used to identify 250 families from each practice for a total of 1250 families. Subjects were sent recruitment letters and subsequently screened for eligibility and recruited by telephone to participate in the study.
Inclusion criteria for the families were (1) at least 1 child 6 months to 5 years of age, (2) at least 1 child in child care with at least 5 other children for 10 hours per week anticipated for the duration of the study, (3) family planned to reside in the metropolitan Boston area for the duration of study, (4) family had access to a telephone, and (5) primary caregiver could speak English or Spanish. Families were excluded when their homes also functioned as family child care centers for 5 or more children or when a household member's occupation included working with children 6 months to 5 years of age for 10 hours per week. Because the primary objective of this study was descriptive, a sample size of 250 families was considered sufficient to provide reasonable confidence intervals (CIs) for calculated illness transmission rates. Thus, we considered study enrollment to be complete when at least 50 families were enrolled per pediatric practice.
Those who agreed to participate were mailed a survey and a symptom diary at the beginning of the study. The survey asked questions about demographic information, beliefs about illness transmission, and practices regarding hand hygiene in the home. Completed surveys were mailed back to study investigators at the beginning of the study. Structured symptom diaries also were provided so that families could record the timing and duration of respiratory and GI illnesses that occurred among family members in the home. In biweekly telephone calls, we reviewed the illnesses recorded by participants. In addition, 7 families with computer and Internet access were selected to record illness data by handheld personal digital assistants (PDAs). These families synchronized the information via Internet with a secure database at Children's Hospital Boston every 2 weeks rather than receiving telephone calls. All written materials were available in English and Spanish. Telephone interviews were also conducted in English and Spanish.
Respiratory Illnesses
A 7-member expert panel that was composed of pediatric infectious disease and study design experts from academia and industry was convened in June 2000 to determine definitions of illness and illness transmission for this study (see Acknowledgments). On the basis of consensus of our expert panel and literature review, a respiratory illness was defined as 2 of the following symptoms for 1 day or 1 of the following symptoms for 2 consecutive days, not including 2 consecutive days of cough alone, sneezing alone, or fever alone: (1) runny nose, (2) stuffy or blocked nose or noisy breathing, (3) cough, (4) feeling hot or feverish or having chills, (5) sore throat, or (6) sneezing.37 A new or separate respiratory illness was defined as 1 of the following: (1) the occurrence of a respiratory illness (as defined above) after a period of 3 illness-free days or (2) if the caregiver stated that the child or other household member had a new illness.37,46 A secondary illness was defined as an illness that occurred in a household member no sooner than 2 days after the onset in the index case and no later than 7 days after the onset in the index case.21,37,46
GI Illnesses
A GI illness in adults and children 6 years was defined as 1 or both of the following on the basis of our expert panel and literature review: (1) any episode of watery or much looser than normal bowel movements or stools or (2) vomiting. In children 0 to 5 years of age, a GI illness was defined as 1 or both of the following: (1) 2 or more watery or much looser than normal bowel movements or stools over a 24-hour period or (2) any episode of vomiting or forceful expulsion of stomach contents, not including spit-ups for infants or young children.29,30,47–50 New or separate GI illnesses were defined as 1 of the following: (1) the occurrence of a GI illness (as defined above) after a period of 3 illness-free days or (2) if the caregiver stated that the household member had a new illness.30 A secondary illness was defined as an illness in a household member that began no sooner than 2 days after the onset in the index case and no later than 7 days after the onset in the index case.21,51
Outcome Measures
Our primary outcome measures were the rates of secondary illness transmission, defined as the number of illnesses per susceptible person-month, for respiratory and GI illnesses. The susceptibility period for a healthy family member was defined as the period 2 to 7 days after a primary illness was introduced into the home. We examined potential predictors of secondary illness transmission in the home in a secondary analysis.
Data Analysis
Families with 4 weeks of data recorded were included in the analysis of secondary illness transmission. Because our data collection methods were different for the handheld PDA group, we excluded from additional analysis the 7 families who used PDAs. To measure secondary illness transmission, we calculated the number of primary illnesses introduced in each family, determined the susceptibility period of each family member after exposure to illness, and then measured the number of secondary illnesses that occurred during each susceptibility period. The incidence rate for secondary illnesses was defined as the number of secondary illnesses divided by the total number of susceptible person-months within a family. The 95% confidence intervals were calculated for incidence rates assuming a Poisson distribution.
To examine potential predictors of reduced illness transmission, we performed Poisson regression at the family level. The outcome was the number of secondary illnesses that occurred within a family; the denominator was the number of susceptible person-days within the family. We initially conducted bivariate analyses to examine the association between clinically relevant variables available from the survey, such as family characteristics and hand hygiene practices, and secondary illness transmission rates. Site of enrollment was included as a fixed effect to account for potential differences between families who attended different health care centers. Variables regarding frequency of hand hygiene product use (water, plain soap, antibacterial soap, and alcohol-based hand gels) and hand hygiene practices (after wiping or blowing a nose, changing a diaper, and using the bathroom) were examined as ordinal variables in bivariate analyses. Predictors were considered significant at P < .05.
Multivariate analyses were performed using forward and backward stepwise Poisson regression models with set at .15 to enter and remove terms from the model to identify significant independent predictors of secondary illness transmission rates in the home. Because of small cell sizes for hand hygiene practices, variables were dichotomized as frequent users (all, most, or some of the time) versus infrequent users (a little or none of the time) for the multivariate model. As before, site of enrollment was included as a fixed effect in multivariate models to account for potential differences as a result of enrollment methods. All analyses were performed in Stata Intercooled 7.0.52
RESULTS
Study Participants
Of the 1250 families randomly selected (Fig 1), 49% did not meet eligibility criteria, 22% were eligible and contacted for study participation, and 29% were not contacted because study enrollment was complete for each pediatric practice. Of the 278 eligible families who were contacted, 17 families refused to participate and 261 (94%) families were enrolled in the study from November 2000 to May 2001. A total of 215 (82%) families completed at least 4 weeks of illness transmission data for the study either by telephone follow-up (208) or handheld PDA (7). Forty-six families were withdrawn from the study for the following reasons: study team unable to reach participants for 4 consecutive weeks (19), participants did not have time to complete study (9), telephone disconnected (3), parent left area (1), child no longer in child care (1), other (3), and unknown (10).
A total of 208 families had 105352 person-days of observation. The total study population consisted of 837 people (287 children 5 years of age including those enrolled in child care, 152 children 6–17 years of age, 395 adults 18 years of age, and 3 whose ages are unknown). Families were observed for an average of 128 days (range: 29–174 days). A total of 185 (89%) families returned completed surveys. Information about education, income, race/ethnicity, family size, household density, and site of enrollment is described in Table 1. Hispanic or Latino families described themselves as Puerto Rican (12), Dominican (17), Mexican (1), Central or South American (6), and Puerto Rican/Dominican (1). Other families included in the study were Asian or Pacific Islander (13), Black Caribbean (6), and Black Caribbean/American Indian (1) or Alaskan Native (1). Primary caregivers were mostly female (96%), and the average age of respondents was 34.6 years (range: 20–50 years).
Survey Responses
We asked individuals about their beliefs regarding illness transmission for "colds" and "stomach flus" (Table 2). Almost all respondents believed that colds could be transmitted by kissing a sick person or having someone cough or sneeze on them (large droplet transmission). Approximately two thirds of respondents believed that colds could be transmitted by shaking hands with a sick person or touching objects that a sick person touched (transmission by direct and indirect contact). However, fewer than half of the respondents believed that stomach flus were transmitted by direct or indirect contact or the fecal-oral route.
When asked about household practices regarding hand hygiene, respondents reported using the following all, most, or some of the time: water alone (30%), soap (90%), antibacterial soap (75%), and alcohol-based hand gels (22%; Fig 2). Use of antibacterial soaps and alcohol-based hand gels was positively correlated (r = 0.417, P < .001), whereas use of antibacterial soaps and plain soaps was negatively correlated (r = –0.198. P = .009). Most respondents reported washing their hands all of the time after changing a diaper (72%) or using the bathroom (84%). However, only 33% reported always washing their hands after blowing or wiping a nose. Of note, parents who reported frequent alcohol-based hand gel use were also more likely to report frequent handwashing after blowing or wiping a nose (r = 0.215, P = .004).
Respiratory Illness Transmission
The total number of respiratory illnesses in 208 families (287 children 5 years, 152 children 6–17 years, 392 adults, and 2 unknown age) was 1545 illnesses over 105352 person-days of observation, or 0.45 respiratory illnesses per person-month. Of these illnesses, 1099 (71%) were introduced into families as primary illnesses. A total of 239 children 5 years were responsible for 592 (54%) primary illnesses, whereas 76 children 6 to 17 years of age were responsible for 135 (12%) primary illnesses. Among adults, 234 people introduced 371 (34%) primary illnesses into the family. One person who had a primary illness was of unknown age. A total of 446 secondary respiratory illnesses occurred over 21452 susceptible person-days of observation, or 0.63 illnesses per susceptible person-month (95% CI: 0.58–0.69). Among those whose age was known, 168 (38%) secondary illnesses occurred in children 5 years, 51 (11%) in children 6 to 17 years, and 225 (50%) in adults, 147 (65%) of whom were primary caregivers.
In bivariate analyses (Table 3), only reported use of alcohol-based hand gels was associated with reduced respiratory illness transmission. In the multivariate model, frequent use (all, most, or some of the time) of alcohol-based hand gels was associated with lower rates of secondary illness transmission in the home (Table 4).
GI Illness Transmission
The total number of GI illnesses was 360 during 105352 person-days of observation, or 0.1 GI illnesses per person-month. Of these, 297 were primary GI illnesses. A total of 123 children 5 years introduced 171 (58%) illnesses into the home, 39 children 6 to 17 years of age introduced 47 (16%) new GI illnesses into the home, and 63 adults were responsible for 79 (27%) primary GI illnesses. Sixty-three secondary illnesses (22 [35%] in children 5 years, 7 [11%] in children 6–17 years, 34 [54%] in adults, 17 [50%] of whom were considered primary caregivers) occurred over 5500 susceptible person-days of observation, or 0.35 GI illnesses per susceptible person-month (95% CI: 0.27–0.45). There were no significant differences in rates of secondary GI illness transmission in families with and without diapered children in the home.
Bivariate analyses revealed that higher educational level and Medicaid insurance were significantly associated with increased rates of secondary transmission for GI illnesses (Table 3). Use of alcohol-based hand gels seemed to reduce secondary GI illness transmission; however, this trend was not significant. In multivariate analyses, only Medicaid insurance remained a significant predictor of increased secondary illness transmission in the home (Table 4).
DISCUSSION
Our study is one of the few longitudinal studies to examine illness transmission rates in the home since use of child care facilities became widespread in the United States. We found an average of 0.45 respiratory illnesses per person-month and 0.1 GI illnesses per person-month from November 2000 to May 2001. In earlier longitudinal studies such as the Tecumseh study (1976–1981) and the Seattle Virus Watch (1965–1969), only 0.16 to 0.29 respiratory illnesses per person-month were reported.53,54 In the well-known Cleveland Family Study (1948–1957) that followed 86 families over a 10-year period, Dingle et al21 established the overall incidence of common respiratory and GI illnesses to be 0.47 and 0.13 per person-month, respectively. Although our illness rates were measured during the peak season for respiratory and GI illnesses, they seem comparable to these previous studies. In addition, we chose to focus on secondary transmission because these infections are potentially preventable episodes through household intervention. In our study, 0.63 respiratory and 0.35 GI illnesses per susceptible person-month occurred in households with children enrolled in child care. Young children were most likely to introduce respiratory and GI illnesses into the household, although adults were also unexpectedly responsible for a substantial number of primary respiratory illnesses.
We found that several misconceptions may exist regarding mechanisms of illness transmission. Only two thirds of respondents correctly believed that contact transmission was important for the spread of colds, and fewer than half believed that it was important in the spread of stomach flus. Almost all families shared the common misconception that kissing was an efficient means of spreading colds.55 Perhaps more surprising, fewer than half stated that changing a diaper or eating food prepared by a person with gastroenteritis (fecal-oral transmission) were important in spreading stomach flus.
It is interesting that parents reported washing their hands very frequently after changing a diaper or using the bathroom, although they did not necessarily believe that fecal-oral transmission was important. Conversely, fewer parents reported washing their hands after blowing or wiping a nose, although the majority believed in large droplet and contact spread of cold viruses. It may be that parents are likely to overreport the frequency of behaviors such as handwashing after bathroom use because of perceived social expectations.56–58 It may also be that parents wash their hands for reasons other than reducing the spread of germs—for example, to remove dirt. Regardless, we would have expected the more likely predictor of transmission to be actual practices rather than beliefs.
Reported hand hygiene practices in the home relied principally on soap and water, with approximately half of respondents using antibacterial soaps all or most of the time and another quarter using these agents some of the time. Such frequent use of antibacterial products is not surprising given that 75% of liquid and 29% of bar soaps that are available to US consumers contain antibacterial ingredients.59 In contrast, only 8% reported use of alcohol-based hand gels all or most of the time, and 14% used these products some of the time. Given the convenience, tolerability, and rapid virucidal activity of alcohol-based products,39,45,60–64 we might expect increased use of these products in the home over time, similar to the rise that we have seen in the hospital setting over the past 5 years.43,45,62
In multivariate models, we found that reported alcohol-based hand gel use was associated with reduced secondary transmission of respiratory illnesses. Our findings are supported by a recent study in which use of an alcohol gel hand sanitizer in the classroom was found to decrease absenteeism as a result of respiratory, flu, and GI illnesses in elementary school students.36 Another study by Fendler et al65 also demonstrated efficacy of alcohol-based hand gels in reducing nosocomial respiratory tract infections in extended care facilities. Ours is the first study to suggest that using alcohol-based hand gels for hand hygiene may reduce secondary respiratory infection rates in the home setting.
In our analysis of secondary GI illness transmission, we observed a pattern of reduced transmission among users of alcohol-based hand gels in bivariate analyses; however, we may not have had the power in this exploratory analysis to detect a statistically significant effect as a result of the relatively small number of GI illnesses seen during this study period. In addition, the reported use of alcohol-based hand gels by primary caregivers was used as a proxy for the family, which may have reduced our ability to detect a significant difference if all family members did not share similar hand hygiene behaviors. Finally, the lack of a statistically significant effect may also be explained by the variable activity of alcohol against GI pathogens. For example, studies have demonstrated an excellent virucidal effect of alcohol when used for rotavirus-contaminated surfaces, whereas handwashing with plain soap may actually further spread the virus.66–68 However, other viral causes of child care–associated GI illnesses such as noroviruses may not be killed efficiently by alcohol-based hand gels.47
One of the strengths of our study is the measurement of the incidence rate of secondary illnesses, rather than just the total number of illnesses that occurred in each family. We believe that this is a more appropriate measure because we would not predict that a household intervention would necessarily reduce the number of primary illnesses that occurred in the family, unless home practices were applied vigorously outside the household. We also attempted to enroll families from diverse socioeconomic and racial/ethnic backgrounds by recruiting from urban and suburban settings and conducting the survey and telephone interviews in both English and Spanish. Thus, our population may be more representative of illness transmission rates in the community, especially when compared with the Cleveland Family Study (1948–1957), which purposely selected families who lived in suburban areas, had high educational levels, and were recommended to study investigators by their family physicians or pediatricians.21
There are several limitations to this study that should be acknowledged. First, our outcome measure was based on reported symptoms or illnesses by the family caregiver. We were unable to validate the cause of these illnesses by microbiologic diagnoses or serologic assays. However, previous work has suggested that self-reported symptoms for respiratory and GI illnesses are a valid proxy for physician-reported symptoms.38,69,70 Second, we relied on parental reports of frequency of hand hygiene practices. We were unable to validate independently the quantity of hand hygiene product used or the frequency of hand hygiene practices after common household events such as using the bathroom. Although parents may overreport the frequency of these hand hygiene practices to conform to social expectations,56–58 the impact of overreporting, if all else were equal, would be to reduce our ability to detect a significant difference in secondary illness transmission rates through misclassification. The finding that use of alcohol-based hand gels was associated with reduced secondary transmission in the home therefore might reflect a conservative estimate of potential impact.
Finally, use of alcohol-based hand gels may simply serve as a proxy for good hand hygiene behaviors. Families who use these products may have had increased awareness of the importance of hand hygiene in the interruption of illness transmission, as suggested by the association between alcohol-based hand gel use and handwashing after blowing or wiping a nose. Thus, the product itself may not necessarily be responsible for the observed protective effect. Unfortunately, we were not able to answer this question definitively through our observational study. For determining the true impact of alcohol-based hand gels on illness transmission, a randomized controlled trial in the home setting should be performed.
In conclusion, our study demonstrates that frequent transmission of illnesses is occurring in the home of families with young children enrolled in child care. Alcohol-based hand gel use was associated with reduced respiratory illness transmission in the home. Targeted educational interventions about the importance of hand hygiene and use of alcohol-based hand gels should be considered for use in the future.
ACKNOWLEDGMENTS
Dr Lee was supported by an Agency for Healthcare Quality and Research training grant (T32 HS 000063), and Dr Friedman was supported by a Health Research and Services Administration Training grant (T32 PE 10018). This study was funded by Reckitt-Benckiser, Inc. No promotional product or materials were used during this study.
We gratefully acknowledge the pediatric practices and all of the families who participated in this study. We also thank our expert panel members for invaluable input: Donald Goldmann, MD; Penelope Dennehy, MD; Girish Dixit, MD; J. Owen Hendley, MD; Patricia Hibberd, MD, PhD; W. Charles Huskins, MD, SM; and Joseph Rubino.
FOOTNOTES
Accepted Aug 19, 2004.
No conflict of interest declared.
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