BACKGROUND AND OBJECTIVE: Cutaneous warts are common in primary schoolchildren; however, knowledge on the routes of transmission of human papillomavirus (HPV) causing warts is scarce. This study examines the association between the degree of HPV exposure and incidence of warts in primary schoolchildren to support evidence-based recommendations on wart prevention.
METHODS: In this prospective cohort study, the hands and feet of all children in grades 1 to 7 (aged 4–12 years) of 3 Dutch primary schools were inspected for the presence of warts at baseline and after 11 to 18 months of follow-up. Data on the degree of HPV exposure included information obtained from parental questionnaires: preexistent warts, warts in family, prevalence of warts at baseline in the class, and use of public places (eg, swimming pools).
RESULTS: Of the 1134 eligible children, 97% participated; the response rate from parental questionnaires was 77%, and loss to follow-up was 9%. The incidence for developing warts was 29 per 100 person-years at risk (95% confidence interval [CI] 26–32). Children with a white skin type had an increased risk of developing warts (hazard ratio [HR] 2.3, 95% CI 1.3–3.9). Having family members with warts (HR 2.08, 95% CI 1.52–2.86) and wart prevalence in the class (HR 1.20 per 10% increase, 95% CI 1.03–1.41) were independent environmental risk factors.
CONCLUSIONS: The degree of HPV exposure in the family and school class contributes to the development of warts in schoolchildren. Preventive recommendations should focus more on limiting HPV transmission in families and school classes, rather than in public places.
- CI —
- confidence interval
- HPV —
- human papillomavirus
- HR —
- hazard ratio
What’s Known on This Subject:
Current recommendations to prevent warts focus on limiting the personal spread of human papillomavirus and transmission in public places, such as swimming pools; however, evidence on risk factors for developing warts is limited.
What This Study Adds:
Cutaneous human papillomavirus in primary schoolchildren is primarily transmitted in the family and school class. This suggests that recommendations should shift toward reducing transmission in families and school classes.
Cutaneous warts are benign papillomas of the skin. Warts are highly prevalent in the general population, especially among primary schoolchildren, for whom the prevalence ranges from 4% to 33%.1–3 Although ∼67% of warts resolve within 2 years without treatment,4 family physicians are often consulted for treatment because of physical or psychological discomfort.5 Based on registries in the United Kingdom and the Netherlands, the annual episode incidence rate of cutaneous warts for the age group of 5 to 14 years in family practice ranges from 3 to 5 per 100 children6,7; however, incidence rates in the general population are unknown.
Cutaneous warts are caused by infection with human papillomavirus (HPV), which is transmitted by direct contact with contaminated skin or indirectly via objects carrying the virus.8,9 Increased exposure to HPV theoretically increases the risk of developing warts.10 Based on studies exploring which risk factors are most important,3,11–18 recommendations to prevent warts focus on limiting the personal spread of HPV and transmission in public places. For example, the use of communal showers is considered to be a risk factor for acquiring plantar warts because wet floors are assumed to be HPV reservoirs.12 Based on this assumption, the following types of recommendations are issued: “Wear flip-flops in communal showers,”19 “Cover the wart with a waterproof plaster when swimming,” or “Do not go barefoot in public places.”20 However, data from studies on risk factors for warts are contradictory, and all studies have a cross-sectional design, thus precluding determination of causal relationships. This prospective cohort study examined the incidence rate of warts in primary schoolchildren and assessed whether the degree of exposure to HPV contributes to the risk of developing warts, so as to provide evidence-based recommendations for wart prevention.
A trained medical student inspected the hands and feet of all children in grades 1 to 7 from 3 primary schools (in and around the city of Leiden, the Netherlands) for the presence of warts. Details of the baseline examination are already published.3 One year later, another trained medical student inspected the hands and feet of all children who were also examined at baseline (now in grades 2–8), again for the presence of warts. Parents were asked to give informed consent before both examinations. Apart from this, children were free to refuse participation during examinations. Because of practical reasons and taking into consideration the school class agenda, the follow-up period ranged from 11 to 18 months. The study was approved by the Medical Ethical Committee of the Leiden University Medical Center, as well as by the boards of the participating schools.
Development of Warts
At baseline and follow-up, the type and number of warts were recorded on standard forms with schematic representation of hands and feet. A distinction was made between plantar warts (located on the soles of the feet) and common warts (located on the dorsal side of the feet or hands). More than 5% of all baseline and follow-up examinations were supervised by an experienced family physician, with no discordance in wart diagnosis. The examiners were unaware of the answers given in the parental questionnaires.
Personal factors were recorded during baseline examination: age, gender, and skin type; the latter was coded according to Fitzpatrick to stratify into white and non-white subgroups.21 The degree of exposure to HPV was ranked according to a conceptual model (Fig 1), which we operationalized by defining potential environmental risk factors for warts.3 Information on the presence of these risk factors was obtained during baseline examination and through parental questionnaires before baseline examinations:
Individual factors: preexistent warts (yes versus no);
School factors: school (school A versus B versus C), and the prevalence of warts in school class at baseline (per 10% increase),3 presence of warts in at least 1 of 3 closest school friends (yes versus no);
Incidence rates with 95% confidence intervals (CIs) were calculated, dividing the incident cases by the sum of the person-time of children at risk. An incident case was defined as a child who had developed 1 or more new warts at the follow-up examination, irrespective of preexistent warts. Also calculated were incidence rates stratified for plantar and common warts, and the incidence rate of new warts in children without warts at baseline.
Cox proportional-hazards model was used to identify risk factors for developing warts. First, univariate analysis was performed for the risk factors to estimate hazard ratios (HRs) with 95% CIs, in which P < .05 was considered as significant risk factor. Multivariate analysis was performed to assess whether the degree of exposure to HPV contributed to the risk of developing warts. We included age, gender, and skin type as personal factors, as well as environmental risk factors representing the various degrees of HPV exposure: preexistent (individual factor), presence of family members with warts (family factor), presence of warts in school class (school factor), and use of public swimming pools (public factor). In addition, an exposure sum score in which each of the 4 environmental risk factors equally contributed (range 0–4) was entered into the model to explore a possible dose-response effect.
The participation rate of 1134 eligible children at baseline was 97%; 23 children (2%) were absent from school at the time of baseline examinations and 12 children (1%) did not provide parental or child consent (Fig 2). Loss to follow-up was 9%; 65 children (6%) left school, 23 children (2%) did not provide parental or child consent at follow-up examination, 9 children (1%) were absent at follow-up examination, and data were missing for 1 child (<1%). Median age of the 1001 children was 7 years (range 4–12, interquartile range 5–9), 48% were boys, 80% had a white skin type, and 33% had warts at baseline (Table 1). At baseline, the parents’ response rate to the questionnaires was 77%.
Development of Warts
The incidence for developing new warts was 29 per 100 person-years at risk (95% CI 26–32). When stratified for the type of warts, incidence rates were 14 per 100 person-years (95% CI 12–16) for plantar warts, 9 per 100 person-years (95% CI 7–11) for common warts (mostly on hands), and 5 per 100 person-years (95% CI 4–7) for a combination of plantar and common warts (Fig 3). The median number of new warts was 1 per child (range 1–10; interquartile range 1–2). The incident rate in children without warts at baseline was 25 per 100 person-years (95% CI 21–30), and in children with preexistent warts, 37 per 100 person-years (95% CI 21–30) (P < .001).
Relation With Potential Risk Factors
Univariate analysis showed no relation with gender, but increasing age was related to increased incidence of warts (Table 2). There was a high incidence rate in children with a white skin type; also, several individual, family, and school factors were significantly related to the development of warts (Table 2). Although the use of public swimming pools almost reached significance level, no significant public factors were identified.
In multivariate analysis, there was no relation with age or gender, but white skin type was a significant personal factor: HR 2.3, 95% CI 1.3–3.9 (Table 3). The degree of exposure, indicated by the presence of family members with warts (HR 2.1, 95% CI 1.5–2.9) and the prevalence of warts in the school class (HR 1.2 per 10% increase, 95% CI 1.0–1.4) were independent environmental risk factors for the development of warts. However, preexistent warts was not an independent risk factor (HR 0.9, 95% CI 0.7–1.3). The use of public swimming pools showed a small nonsignificant risk (HR 1.17, 95% CI 0.75–1.83). A dose-response effect was present in the exposure sum score of the 4 environmental risk factors; the risk of warts increased by 3.5 (95% CI 2.9–4.2) per extra positive factor.
In the subgroup of children with plantar warts, and the subgroup of children without warts at baseline, similar results were found.
Summary of Main Findings
The incidence rate of new cutaneous warts in primary schoolchildren was 29 per 100 person-years. Exposure to HPV in families and school class was associated with the development of warts, whereas no independent associations were found for the presence of warts at baseline and public risk factors.
Strengths and Limitations of the Study
The development of warts was objectively established by physical inspection of hands and feet. Warts on other parts of the body were potentially missed, but account for only ∼4% of all warts.22 The causal associations between the incidence of warts and environmental risk factors were supported by the biological model of HPV exposure and the dose-response effect in our data. The sufficient numbers of children in this study with a participation rate of 97% and the presence of 20% non-white skin types (mostly originating from Morocco, Turkey, China, Netherlands Antilles, and Surinam), resemble the general Dutch primary school population.23 Although transmission patterns may differ to some extent owing to local customs, the ways of HPV exposure are probably comparable in Western countries.
A limitation of the study was that some risk factors related to HPV exposure were not considered because they are difficult to measure; for example, the sharing of personal items or close contact to children with warts during specific hobbies. Although unlikely, suboptimal interobserver agreement in assessment of warts or the parental assessment of some risk factors could have diluted associations. For example, parents could have been misinformed about the presence of warts among family members. Last, binary analysis of factors did not allow assessment of dose-effect relationships within factors.
Comparison With Existing Literature
To our knowledge, no other recent studies on incidence rates of warts in the general population are available. Based on entries in family physician registers in the United Kingdom and the Netherlands, the annual episode incidence of cutaneous warts for the age group of 5 to 14 years in family practice ranges from 3 to 5 per 100 children.6,7 The discrepancy with the much higher incidence rates we observed (29 per 100 person-years) is explained by the fact that many warts are unnoticed by children and parents,3 and many warts are treated with over-the-counter medication, or not treated at all.
Studies on environmental risk factors for warts are contradictory and all have a cross-sectional design.3,11–18 Furthermore, a validated model on the degree of HPV exposure is lacking. This is the first study with a prospective design, which also allows for exploring possible causal relations. The risk factors we identified partially confirm the theoretical degree of HPV exposure in the environment; having a family member with warts was a more important risk factor than school class prevalence, which was more important than any public factor (Fig 1).3 However, preexisting warts (expected to be the main risk factor according to the individual degree of HPV exposure), was not independently associated with the development of warts. This could be explained by the fact that, besides HPV exposure, immunogenicity and susceptibility of the host to specific HPV type are important to develop warts.10 In other words, the immune system of the child with warts could already be triggered and might therefore be more effective against the specific HPV type the child is exposed to. To a lesser extent, genetic aspects of the susceptibility of the child could play a role within families, but identification of school class prevalence as a risk factor confirms that HPV exposure is an important component. Future studies on HPV antibody seroprevalence and HPV typing in families/schools should provide evidence on immunogenicity and the susceptibility to specific HPV types.
Regarding public transmission, exposure to HPV was probably too low to be detected with the risk factors and number of children in this study. A possible explanation could be that some preventive measures had already been effectively carried out. Although there are informal leaflets with advice on warts from public health institutions in the Netherlands, there are no formal regulations for persons with warts; they are neither actively banned from swimming activities nor recommended to cover their warts with plasters in public places.
This study reveals that the incidence of warts in primary schoolchildren is high and that cutaneous HPV is primarily transmitted via the family and school class. Current preventive recommendations mainly focus on limiting the personal spread of HPV (“Avoid scratching lesions”) and reducing the risk of transmission in public places (“Wear flip-flops in communal showers” ).19 Our findings suggest that recommendations should shift toward reducing transmission among families and school classes. For example, covering warts at home potentially prevents transmission more effectively than covering warts in the swimming pool.
The authors thank all the primary schoolchildren and their parents for their enthusiastic participation. We also thank Femke van Haalen for the collection of baseline data.
- Accepted January 29, 2013.
- Address correspondence to Sjoerd C. Bruggink, MD, Department of Public Health and Primary Care, Leiden University Medical Center, PO Box 9600, 2300 RC, Leiden, Netherlands. E-mail:
Dr Bruggink contributed to the design of the study, created materials for data collection, performed analyses, and drafted the manuscript; Dr Eekhof was responsible for study design, supervised data collection including quality assurance, and critically reviewed the manuscript; Dr Egberts reviewed literature, contributed to data analyses, and critically reviewed the manuscript; Ms van Blijswijk performed field activities, contributed to data analyses, and critically reviewed the manuscript; Dr Assendelft contributed to the concept of the study and the interpretation of data, and critically reviewed the manuscript; Dr Gussekloo contributed to the concept of the study, devised the analytic strategy, contributed to the interpretation of data, and critically reviewed the manuscript; and all authors approved the final manuscript as submitted.
FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.
FUNDING: Supported by the Netherlands Organisation of Health Research and Development, Fund Common Diseases (grant 80-81000-98-066). The organization did not have any influence on the study design; the collection, analysis, or interpretation of data; the writing of the report; or the decision to submit the article for publication.
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- Copyright © 2013 by the American Academy of Pediatrics