Acute gastroenteritis (AGE) is one of the main causes of sickness and mortality among children all over the world. Acute diarrhea is the third most important reason for seeking primary pediatric attention (after cough and fever) and attending hospital emergency units1,2 and hospital admissions.3–6 There are many studies on AGE in children <5 years of age,4,6–9 fewer have been done about older children.10
Handwashing is the most important and effective preventive measure affecting transmission of infectious agents.11,12 Hydroalcoholic gels or hand sanitizers are excellent virucides and bactericides against gastrointestinal and respiratory pathogens.13–16 A systematic review of the effectiveness of alcohol solutions for hand hygiene showed that they eliminate organisms, require a shorter length of time and irritate the skin less than handwashing with soap and water or other antiseptic detergents.17
There are studies that assess the impact of handwashing programs on a reduction in the transmission of infectious diseases in nurseries,18–21 households,21 university residence halls22 and schools.23–28 Meta-analyses29,30 found that handwashing can reduce the risk of diarrhea by 31–47%. Studies carried out in schools25,31,32 on handwashing programs using hand sanitizer observed that school absenteeism caused by AGE decreased by 9–44%.
Problems such as lack of time, handwashing facilities, soap and hand tissues in schools hinder the practice of good handwashing hygiene in pupils. Hand sanitizers are an alternative hand-cleaning technique, which requires only the liquid and dispenser and minimum maintenance. Studies in different countries show the efficacy of handwashing programs in reducing AGE. However, long-term randomized studies carried out with school children in developed countries are scarce. No such research has been published on a Spanish population. The aim of this study was to assess the impact of such a program on school absenteeism due AGE and its relation to sociodemographic characteristics (housing, family size, immigration, parents occupation), personal background and handwashing awareness and habits.
MATERIALS AND METHODS
A randomized, controlled and open study was designed of 2 cohorts of primary school children between the ages of 4 and 12, attending 5 state schools in Almería province (Spain). This study was conducted during 8 months (October 2009 to May 2010). The schools were randomized for the study after the administration of each 1 had agreed to participate in it.
The experimental group (EG) washed their hands with soap and water, followed by the use of the hand sanitizer, while the control group (CG) practiced usual handwashing.
Considering a 14% decrease in AGE in the EG, a typical (standard) joint deviation of 0.59 and a rate of 0.79 episodes of AGE per child per year,33 a study powering of 90% and a confidence level of 95%, the minimum number of subjects required for the study was 606 children in each study group, with a total of 1212 children. Considering the loss of 24% follow ups, it was necessary to randomize 753 children per Group.
This study was carried out during 8 months in 5 state schools within the Almería province. The municipalities were selected as they had already participated in a previous study done by the University of Almería regarding water and sustainability. Two of these towns had 2 primary education centers (4–12 years of age), thus 1 was randomly assigned to the CG and the other 1 to the EG. The other town only had 1 school; therefore, the randomization there was done by randomly selecting from the 29 class groups, 14 for the EG and 15 for the CG. Comparing within the same towns and schools was done to attempt to avoid possible sociodemographic biases. To decide which school/class would be the EG/CG, a random number table was used.
Eligible school children were aged between 4 and 12 in October 2009, enrolled in the above mentioned schools, and whose parents/tutors had signed an informed consent agreement. School children with chronic illnesses that could affect their likelihood of contracting an infection or the duration of their absence from school, were excluded.
Parents were informed by mail from school administration, including the following documents: an information sheet about the study, an authorization form and a questionnaire on sociodemographic characteristics and when and how their children washed their hands. Before the start of the study, the parents authorized their children’s participation in it and knew which group their children belonged to.
The pupils and teachers in the EG, attended 2-hour handwashing workshops. These took place 1 month before the beginning of the study. Their content included education about infections most frequently transmitted in schools, how infections are transmitted and prevented, instructions on how and when hands should be washed, use of hand sanitizers and possible side effects. Every fortnight, the research assistant and the teachers did activities linked to hand hygiene and infection transmission (stories, songs, posters in the classroom). The younger children were supervised by their teachers when using hand sanitizer. In some cases, this was administered by the teacher. The researchers checked the handwashing technique during visits to the classrooms.
Children in the EG were instructed by the researchers, teachers and research assistants to maintain the usual handwashing procedure after going to the toilet and when their hands were visibly dirty. They were also told to use the hand sanitizer correctly in the following circumstances: after coming into the classroom, before and after lunch, after the break and after physical education lessons and when they went home, after coughing, sneezing or blowing their noses. In the EG classrooms, hand sanitizer dispensers were installed and an information brochure about when and how to wash their hands was available. The EG teachers were responsible for ensuring that hand sanitizer was correctly used and readily available and for recording negative effects related to the procedure. The CG followed usual handwashing without any recommendations or reinforcements on the part of the teacher.
Characteristics of the hand sanitizer (ALCO ALOE GEL; Americo Govantes Burguete, S.L. Madrid, Spain): chlorhexidine digluconate at 20% solution, phenoxythanol 1%, benzalkonium chloride 0.1%, aloe Barbadensis 5%, Renat ethyl alcohol 70% and excipients c.s.p. 100 mL. Alcohol between 65–70% degrees, pH = 7–7.5.
Data Collection and Illness Definitions
The parents of both groups who agreed to participate in our study completed the survey that collected the following variables: age, gender, country of origin, number of household members, parents´ profession, according the classification proposed by the Spanish Epidemiology Society,34 housing (flat, house, semidetached house, others), size of dwelling in square meters, sleeping arrangements (own or shared bedroom), pets, children’s personal background, use of hand sanitizer at home and questions about hand hygiene about when and how their children washed their hands.
Parents of children who were absent from school due to AGE, recorded AGE symptoms and gave the completed form to the teacher. One research assistant collected the absence sheets of the participating classes weekly, telephoned the parents of absent children to enquire about the cause of their absence, visited the classrooms and collaborated with the teachers in hand hygiene activities.
We used the case definition proposed by the International Collaboration on Enteric Disease Burden of Illness Studies. A case of AGE was defined as a person with 3 or more loose stools or some vomiting, in 24 hours.35
To assess the accuracy of the symptoms reported by the parents, the research pediatricians reviewed all the medical records of the absent pupils due to AGE, using the database of the Department of Health of Andalusia to have medical diagnoses available. The final diagnosis was done by the medical researchers on the basis of the symptoms described above and of the revision of the medical history of absent children because of AGE. Permission to revise the medical records and publish results was granted by the ethical review board for clinical trials at the Hospital Torrecardenas, Almería (Spain).
In this study, a school absenteeism case (episode) was defined as failure of a child to attend school due to a AGE. Common infectious illnesses, such as conjunctivitis and skin infections, were not included. Other causes for absenteeism, such as doctors’ appointments, family vacations and accident injuries, were excluded.
We defined a new episode of AGE as the occurrence of AGE after a period of 3 symptom-free days.20 Duration of absenteeism was defined as the number of school days missed due to AGE (excluding weekends and holidays).
To improve the accuracy and credibility of the school absenteeism register, the research assistant collected the absence sheets weekly sent by the parents, comparing them monthly with the absence register kept by the teachers using the SENECA program (an IT Program for registering absenteeism from the Department of Education of Andalusia) and telephoned the parents of those children whose cause for absenteeism recorded by the teacher was unclear.
The incidence rate of AGE was calculated dividing the number of episodes of AGE by the number of pupils during the period of this study who were susceptible to the infection.
Incidence Rate Ratio
Incidence rate ratio indicates the ratio between incidence rate in both study groups. Percentage of AGE absent days in both groups was calculated as the ratio of AGE absence days to all possible days of attendance. Rates were calculated for the overall academic year (October to May). Total possible days of attendance was calculated as total number of students multiplied by possible days of attendance
The sociodemographic characteristics of the CG and the EG were compared using Pearson’s χ2 test for qualitative variables and Student’s t-test for quantitative variables, with a 5% significance level. Analyses were conducted according to the intention-to-treat with children assigned to their original group (EG or CG) and including the new students enrolled in the schools.
The IRR was obtained using of the Poisson regression model. Comparisons of the rates were carried out between the CG and the EG adjusted through a multivariate Poisson regression. The model includes gender, country of origin, age, family size, dwelling type, pets home, profession of the parents, hand sanitizer, correct handwashing and AGE-preventive behaviors. The percent days absent in both groups were compared with the Z-test.
This study was not analyzed by cluster because there are varying levels of randomization (and correlations) within the same study design. Randomization units were different (2 municipalities by school and 1 by classes). The statistical analysis was carried out using the IT program SPSS version 17.0 (SPSS Inc., Chicago, IL).
Of 1640 school children, 98.5% of parents authorized their participation in the study, the tracking failed in 33 cases due to families moving to a different area (19 CG and 14 EG) and 27 new children joining the school (14 CG and 13 EG). One child in the EG showed worsening of atopic dermatitis due use of the hand sanitizer gel and was excluded from the group. The questionnaire was answered by 83% of the parents, 720 parents from the CG and 621 from the EG, the final sample was 1341 (Fig. 1).
The sociodemographic characteristics of both groups were similar (Table 1). Although significant differences exist in our study in terms of types of dwelling, this potential bias was controlled including this variable in the multivariate analysis.
During the school year, 420 absenteeism episodes occurred due to AGE (285 CG and 161 EG) of which diagnoses were confirmed by a doctor in 61.1% of the cases (61.1% of absent pupils due to AGE had seen a doctor who confirmed that they all had AGE). The children in the EG presented 0.27 (95% confidence interval (CI): 0.22–0.31) absenteeism episodes/per child/per academic year versus 0.40 (95% CI: 0.35–0.45) episodes/per child/per school year of the CG, with a number needed to treat (NNT) = 7.32 (95% CI: 5.37–11.50).
Figure 2 shows absenteeism episodes due to AGE per month during the 2009–2010 academic year. An increase of AGE in both groups was observed in winter and spring. The rate of absenteeism were significantly lower in the EG during the months of February, March and May (P < 0.05).
Pupils missed 725 school days due to AGE (EG: 274 days vs. 451 days in the CG); the total possible days of attendance in the EG and CG were 88,182 and 102,204 days, respectively. Percent absent days was significantly lower in the EG (EG: 0.31%, 95% CI: 0.28–0.35 vs. CG: 0.44% 95% CI: 0.40–0.48, P <0.001). The number of days absent per episode AGE during academic year was ranged from 0 to 7 days in both groups. The 31.2% students in CG missed ≥ 1 day compared with 21.1% students in the EG.
In the bivariate analysis, the only factor significantly linked to school absenteeism due to AGE was not taking part in the handwashing program (IRR EG: 0.65, 95% CI: 0.54–0.79, P < 0.001). The multiple regression analysis (Table 2) show that the adjusted absenteeism rate for AGE was significantly lower in the EG [IRR: 0.64 (95% CI: 0.52–0.78); P < 0.001].
Our study is 1 of the few randomized studies carried out with school children in a developed country to assess the effectiveness of a multifactorial handwashing program including hand sanitizer to reduce school absenteeism due to AGE. Most studies about handwashing with soap and water are carried out in low-income countries.28,36,37 Handwashing with soap can lower the risk of diarrhea by 42–48% in those countries38 and can effectively reduce pathogens of fecal origin on hands.39 However, there are pathogens, like rotavirus, that are not removed by routine handwashing with soap and water, but alcohol reliably kills them.15
The 36% reduction in absenteeism due to AGE in our study concurs with previous studies,25,31,32 reporting a 9–44% reduction. A 2012 Cochrane review,40 considering only trial results adjusted by cluster randomization, interventions promoting handwashing resulted in a 39% reduction in diarrhea episodes in children in institutions in high-income countries and a 32% reduction in such episodes in children living in communities in low- or middle-income countries. The greatest reduction found in our study with regard to another randomized study32 was probably due to the fact that the later was carried out over a shorter period (3 months) and the strategy of our study was also different, because we reinforced handwashing education during the tracking and pupils washed their hands more often.
The children in the EG had 0.27 absenteeism episodes/per child/per school year versus 0.40 episodes/per child/per school year is the CG. This is similar to the report by Prazuk et al41 of 0.31 in the treatment group and 0.53 in the CG.
The pupils in the EG missed fewer school days due to AGE than those in the CG. These results coincide with those from previous studies.25,31 The 21.1% and 31.2% of children in the EG and the CG, respectively, missed 1 or more school days due to AGE. Between the 2 groups, we found similar differences to those in Sandora´s study,32 which were of 16% EG to 24% CG.
As in other studies,19,20,32 the multivariate model (Table 2) demonstrated less absenteeism risk due to AGE in the EG. Although girls had more absences than boys, the difference was not statistically significant (P = 0.057) coinciding with Nandrup´s10 study 2009.
There was an increase in AGE infections in the months of February, March and May. A similar seasonal influence has been reported in other industrialized countries.41,42 This information supports the importance of intervention to reduce episodes of AGE in peak months, which could include hand sanitizer gels in the classroom with teacher supervision of their use. As detailed by Prazuk et al,41 leading to a significant difference in the gastroenteritis rate among pupils, which reduced school absenteeism, medical visits, as well as working days missed by parents.
In our study, a NNT of 7.32 shows the need to include 7.32 children in the handwashing program to avoid 1 case of absenteeism due to AGE. According to these results, with 65,435 school children between the ages of 4 and 12 years, 8939 episodes of absenteeism due to AGE could be avoided every academic year in our province. Lee et al43 in a review of gastrointestinal outbreaks in schools found that, although gastrointestinal illness is generally of short duration, 5.5% of pupils required hospitalization, adding to the burden of health care costs and to the loss of parental productivity
Our study required the participation of families from various socioeconomic levels and different countries of origin, as we consider that our population can be representative of AGE infection episodes occurring among school children in our area. Any intervention that can reduce the AGE could have a relevant impact on public health and on the use of resources. In spite of this and other similar findings, handwashing is not consistently practiced or promoted in state schools. Perhaps if handwashing became part of the school curriculum, it would produce changes in pupils’ behavior and habits in School and in their homes.
This study has several limitations. The illness documentation is based on symptoms reported by parents/tutors and we lack microbiological confirmation and medical diagnosis data in all cases. To address this limitation, the medical histories of the participants with absenteeism due to AGE were reviewed using database records; thus, 61.1% of cases were confirmed with a doctor’s diagnosis. The absence of masking both in participants and researchers was due to the characteristics of this study. However, the statistical analysis was masked. Our study did not measure separately the impact of handwashing with soap versus rubbing hands with hand sanitizer versus educational effort. However, previous studies have proved that each measure is individually effective22,24,27,36 and better results are obtained when multifactorial programs are used.21,23
In conclusion, our study demonstrates that specific educational efforts on sanitation, complemented by regular supervision of handwashing and the availability of soap and hand sanitizers, are effective measures to reduce the days absent and number of school absenteeism cases due to AGE. Schools should consider incorporating these measures (including hydroalcoholic gel dispensers in the classrooms) to reduce absenteeism due to common infectious illnesses.
The authors wish to thank the following for their valuable help: participating schools and their head teachers: Mr. Juan Rafael Fernández Rumi (Simon Fuentes School), Mr. Fernando Molero Garzón (García Lorca School), Ms. Dolores García Jiménez (Reyes Católicos School), Ms. Antonia Rodríguez Mulero (Asensio Granados School), Mr. Serafín Portaz Sánchez (Alvarez de Sotomayor School) as well as their teachers and research assistant of this study Mercedes Salinas. The authors also thank local councils through their lord mayors and councilors, who never hesitated to offer their facilities for the various events held in their towns, and companies participating in this project: Endesa (Mr. José Ribelles Martínez), Saepro (Mr. Jorge Ruiz López), Electraferre (Mr. José Ferre Segura e hijos S.R.L.), Galasa, all of them concerned about the environmental problems and in particular the precious resources, water and electricity. The authors thank the children and parents who took part in this project which would not have been possible without their cooperation. Collaborators are Department of Health and Education and the University of Almería.
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