In the control of communicable diseases, it is important to have accurate information about incubation periods and periods of infectiousness. The incubation period of an infectious disease can be used to estimate the time during which further cases may occur and to indicate the most effective time for the introduction of control measures such as passive immunization and prophylactic antibiotics. The period of infectiousness can be used to define an exclusion period for conditions in which cases represent a risk to the health of other individuals. Knowledge of both the incubation period and the period of infectiousness of communicable diseases is also needed to inform epidemiologic studies and investigations.
In practice, information about incubation periods and periods of infectiousness is usually obtained from textbooks and manuals. 1–4 This information and recommendations for exclusion periods are also available in various national and local guidelines for the control of communicable diseases in schools and preschools. 5–9 The values in these sources are rarely referenced, and the origin of the data is unclear. In the case of exclusion periods some existing recommendations may be excessive or ineffective, and the removal of children from school could place an unnecessary financial and organizational burden on families in an era when both parents work and increasing proportions of children are cared for by a single parent. It is therefore imperative that any disruption to schooling is supported by the best available evidence.
We were commissioned by the UK Government Department for Education and Employment and the Department of Health to prepare national guidelines on the control of communicable diseases in schools and preschools. We took this opportunity to undertake a thorough systematic review of the incubation period and period of infectiousness of childhood infections and to determine whether exclusion would influence secondary transmission. The resulting evidence-based information is presented below.
Information was collected on 41 infections and infestations. The conditions were selected on the basis that they are common, or are a particular concern, in immunocompetent children of school or preschool age. For each disease information was collected on the incubation period, period of infectiousness and a number of other properties (Table 1). Information on the effectiveness of exclusion was also sought. Data on duration of shedding and serial interval were collected because these can be used to estimate periods of infectiousness in the absence of direct information. The serial interval depends on both the incubation period and the period of infectiousness. Thus if the incubation period is known, the serial interval can be used to estimate the period of infectiousness. If, for example, the serial interval is shorter than the incubation period, the period of infectiousness occurs before the onset of clinical illness.
Information was collected by performing a thorough MEDLINE computerized literature search of articles published between 1966 and 1998. 10, 11 Original epidemiologic or experimental studies on the chosen aspects of each infection were sought. Review articles were also sought as a source of references and to assess the risk of transmission. Further original papers were identified from the bibliographies of articles obtained from the computerized search. Papers were also identified by consulting United Kingdom authorities on individual infections or organisms (see Acknowledgments for details). If more than one paper yielded the required information, the most useful papers were identified on the basis of the number of cases reported, the age of cases (school age children preferred), the location (school preferred to community or family setting) and geography (industrialized world preferred). In addition the type of study was taken into consideration. Epidemiologic or observational studies were preferred, especially when these involved a brief exposure to a point source of infection.
Levels of evidence and grades of recommendation
Data were collated and the quality of the information available on each variable was indicated by ascribing it to a level of evidence on a scale of I to IV as shown in Table 2. Proposals on the need for exclusion were originally produced by the authors according to the perceived seriousness of the disease and the likely effectiveness of exclusion. Exclusion periods were suggested in the light of the evidence obtained. The evidence base and proposals on exclusion were then circulated among members of the professional groups represented by the authors. These included groups with interests in pediatric infectious diseases, community child health, public health and epidemiology (see Acknowledgments). Opinions were sought from these groups, and the authors then produced the final recommendations on exclusion. Grades of recommendation were used to support the exclusion periods (Table 2). Grades A, B and C can be considered to represent strongly, reasonably and poorly evidence-based recommendations respectively. The levels of evidence and grades of recommendation used in this project were derived from those commonly applied in evidence-based medicine. 12, 13
In the course of this study >3000 articles were obtained and read. Of these ∼20% yielded useful information. Information on the risk of transmission, incubation period, duration of shedding, period of infectiousness and serial interval of the 41 selected infections is summarized in Table 3. Recommended exclusion periods for schools and preschools are shown in the final column. For ease of presentation only the highest quality references are provided.
Exclusion periods have been recommended for 25 infections. In school age children examples include: 5 days from the onset of clinical illness for chickenpox, measles, mumps and rubella; 5 days from the commencement of appropriate antimicrobial therapy for pertussis and scarlet fever; and 24 h from the last episode of diarrhea for most gastrointestinal infections. Exclusion is not recommended for 16 infections and infestations, usually because the condition is mild or exclusion would be ineffective. Examples include common childhood conditions such as head lice, threadworms and warts and verrucas. For three herpesvirus infections (herpes simplex, infectious mononucleosis and roseola infantum), it was judged that although prevention of secondary cases might be desirable, exclusion would be impractical because of prolonged excretion of the virus. Similarly exclusion was not recommended for fifth disease (erythema infectiosum) and hepatitis A because the evidence suggests that children are probably infectious only before the onset of clinical illness.
The quantity and quality of information obtained varied widely between diseases. For some infections such as chickenpox and tuberculosis, evidence of Level I or II was widely available. For others such as head lice and gastroenteritis, very little useful information was obtained. The quality of evidence also varied between the properties studied. For incubation periods Level I or II evidence was available for 25 infections. Data on periods of infectiousness could be found for only 11 infections (Level I or II evidence for 3 infections), and data on the effectiveness of exclusion were found for only 4 infections. We were able to make Grade A recommendations on exclusion for 3 infections. There were 17 Grade B and 21 Grade C recommendations.
As far as we are aware this study represents the first attempt to develop evidence-based guidelines for the control of communicable diseases in schools and preschools. This approach was necessary because the origin of most existing information is unclear and the strength of the data and the reliability of any recommendations is uncertain.
In general we found that the values obtained for incubation periods are similar to those given in commonly used, unreferenced texts. 1–4 Where there are discrepancies, these are largely in infections where the only available evidence was weak. It is difficult to compare periods of infectiousness with those quoted in existing texts because this variable could be identified for only about one-fourth of the infections. In practice, periods of infectiousness usually had to be estimated from other data such as duration of shedding and serial interval.
There is good accord between this study and existing texts as to which infections require exclusion. However, the decision to exclude largely depends on the perceived seriousness of the condition and cannot therefore be truly evidence-based. When exclusion periods have been recommended in this project, the duration of these is in broad agreement with those given in existing texts. Nevertheless there are a few decisions on exclusion that require particular comment. We concluded that exclusion for 5 days was sufficient for the control of chickenpox, measles, mumps and rubella. Some texts suggest that longer periods of exclusion are required for mumps and rubella (from 7 to 9 days and 7 days, respectively). 1, 2, 4 Although we were unable to find evidence about the precise periods of infectiousness of these conditions, data on the duration of shedding and serial interval suggest that 5 days is sufficient. 102, 117, 118, 129, 131 Some authorities suggest that children with chickenpox should be excluded from school until all lesions have crusted over. 3, 4 We could find no evidence to support this practice, but there was good evidence to support the 5-day rule. 19–22 Our guidelines also differ on the bacterial gastrointestinal infections, such as salmonellosis, shigellosis, typhoid and paratyphoid. Some authorities suggest that children with these conditions should be kept away from school until negative stool samples have been obtained. 3, 4 We could find no evidence to support or refute this practice, and we have suggested that schoolchildren should be excluded only while they have diarrhea. This approach is in accord with recent guidelines on the control of gastrointestinal infections. 1, 178
We also identified a number of infections in which exclusion would not be fully effective because cases are infectious before they develop a clinical illness. This situation applies to many of the childhood exanthems, including chickenpox, measles and rubella. 19, 103, 130, 179, 180 In some infections, notably hepatitis A and fifth disease, the period of infectiousness has probably passed before the illness becomes apparent. For this reason we have not recommended exclusion for schoolchildren with these conditions. In the case of hepatitis A this advice is contrary to existing guidelines which state that children should be excluded for at least 7 days. 1–4 We found that children with hepatitis A are infectious 2 weeks before the onset of symptoms, but the precise duration of infectiousness is not known. 81–84 However, we also found that most virus is excreted before the onset of illness 78–80 and that the serial interval is shorter than the incubation period. 76, 85, 78–80 In addition to this evidence of early transmission, it could also be argued that exclusion is not necessary because hepatitis A is usually a mild disease in children. 181 Despite these findings exclusion has been recommended for younger children and those who are unable to maintain personal hygiene. This is because children attending day-care centers are a recognized source of hepatitis A in adults, 86, 181 and adults typically have a more severe form of the disease.
One of the major findings of this study is the lack of knowledge about the incubation period and period of infectiousness of certain communicable diseases. These include common childhood ailments such as head lice, threadworms and warts, as well as a number of gastrointestinal infections. This lack of scientific information is a hindrance to the development of guidelines for communicable disease control. Hopefully the finding of deficiencies in our database can be used to identify areas for future epidemiologic research. We would suggest that research into gastrointestinal infections would be particularly useful because diarrheal diseases account for the majority of disease outbreaks in schools and preschools. 182 Research into the effectiveness of exclusion policies would also be valuable. In this study we identified only four conditions in which the implementation of an exclusion period had been shown to terminate an outbreak. 69, 124, 133, 183 We also found some evidence that widely recommended exclusion periods are not effective in schools. 179, 180 Ideally studies of interventions to limit the spread of communicable diseases should include a control group. Such studies have only rarely been undertaken in childhood populations, 184, 185 and none has assessed the effectiveness of exclusion.
In summary we have attempted to develop evidence-based guidelines for the control of communicable diseases in children by collecting data on the incubation period and period of infectiousness of 41 infections and infestations. We were able to make strongly or reasonably evidence-based recommendations for approximately one-half of the diseases. We believe that this research has been valuable in demonstrating the strengths and weaknesses of our knowledge of the epidemiology of infectious diseases. The guidelines given in the extensive summary table represent the best evidence available for the control of communicable diseases in children.
We acknowledge the following individuals and organizations who provided information and commented on our findings and recommendations: Hilarie Williams, Laura Cunningham and officials from the Department for Education and Employment; Hugh Nicholas, Ros Skinner and officials from the Department of Health; Norman Begg, Liz Miller, Gordon Nichols, Mary Ramsay, John Watson and other members of the Public Health Laboratory Service (which was represented on the writing group by Angus Nicoll); Graham Davies, Paul Heath, Mike Sharland and other members of the British Paediatric Immunology and Infectious Diseases Group (represented by Martin Richardson); British Association for Community Child Health (represented by David Elliman); Consultants in Communicable Disease Control (represented by John Simpson); Public Health Medicine Environmental Group (represented by John Simpson); Communicable Diseases Surveillance Centre Regional Epidemiologists (represented by Helen Maguire).
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The information on exclusion periods from this article is incorporated in a poster that has been distributed to schools and preschools in England and Wales. The poster also includes guidance on other topics such as hygiene, universal precautions, immunization and vulnerable children and members of staff. Copies of the poster, Guidance on Infection Control in Schools and Nurseries, and an accompanying wallet-sized leaflet are available from Department of Health, P.O. Box 777, London SE1 6XH, UK. Details are available at http://www.phls.co.uk/advice/schools/summary.htm. The website also contains a fully referenced database of the evidence identified in this study.