Human Papillomavirus Infections in Adults and Children

Sreedhar K. Krishna, Ankeet S. Jethwa

  Open Access OPEN ACCESS  Peer Reviewed PEER-REVIEWED

Human Papillomavirus Infections in Adults and Children

Sreedhar K. Krishna1,, Ankeet S. Jethwa2

1Institute of Public Health, University of Cambridge, United Kingdom

2Department of Surgery, University Hospitals of Leicester, United Kingdom

Abstract

Human papillomavirus infections (HPV) are incredibly common in both adults and children, with the vast majority of infections being subclinical. Using a systematic approach, this review paper aims to describe the epidemiology of HPV infections by time, person and place.

At a glance: Figures

Cite this article:

  • Krishna, Sreedhar K., and Ankeet S. Jethwa. "Human Papillomavirus Infections in Adults and Children." American Journal of Epidemiology and Infectious Disease 1.2 (2013): 11-19.
  • Krishna, S. K. , & Jethwa, A. S. (2013). Human Papillomavirus Infections in Adults and Children. American Journal of Epidemiology and Infectious Disease, 1(2), 11-19.
  • Krishna, Sreedhar K., and Ankeet S. Jethwa. "Human Papillomavirus Infections in Adults and Children." American Journal of Epidemiology and Infectious Disease 1, no. 2 (2013): 11-19.

Import into BibTeX Import into EndNote Import into RefMan Import into RefWorks

1. Introduction

Papillomaviruses are ancient viruses which are believed to have concomitantly evolved with their hosts, resulting in much diversity of both species- and host-specific viruses [1] Papillomaviruses are non-enveloped DNA viruses which replicate exclusively in the basal layer of body tissues. Each virus is highly host-tropic and thus is rarely thought to be transmitted between animals and humans [2]. While the majority of human papillomavirus (HPV) infections are asymptomatic, there is a subset of HPV genotypes which cause warts (noncancerous skin growths), as well as cancers of the cervix, vulva, vagina, oropharynx and anus. It is thought that between 30 and 40 HPV genotypes are transmitted through sexual contact and infect the anogenital region. Some HPV genotypes which are transmitted through sexual contact are known to cause genital warts. Persistent infection with ‘high-risk’ HPV genotypes (i.e. HPV-16 or -18) – which are different from those that cause cutaneous warts – may progress to pre-cancer and sometimes cancer [3]. It must be noted, however, that most infections with these high-risk genotypes do not cause disease. Much of the recent focus on HPV has centred around the HPV vaccines such as Cervarix and Gardasil which are confer protection against HPV-16 and -18, which cumulatively account for 70% of cervical cancer cases [4, 5].

The current classification system, which separates over 100 known human papillomaviruses into groups based on similarities in genomic sequences, correlates well with the three clinical categories of HPV infection:

● Non-genital cutaneous disease (e.g. common warts, plantar warts)

● Anogenital disease (e.g. condyloma acuminata, Bowen’s disease) and non-genital mucosal disease (e.g. conjunctival papilloma, oral carcinoma)

● Epidermodysplasia verruciformis (EV) – a rare autosomal-recessive disorder in which sufferers have grossly impaired immune responses to HPV infection; otherwise minor HPV infections may result in widespread wart-like eruptions that may occur anywhere on the body.

Within the category of non-genital cutaneous warts, there are several different types. These include:

● Common warts – these have a characteristic ‘cauliflower-like’ surface which are typically raised compared to their surrounding skin surface. These are most often found on the hands and feet, but may occur in other areas such as the elbows or knees.

● Plantar warts - as the Latin root suggests, these affect the soles of the feet. These can grow inwards which may make walking painful.

● Flat warts – these most often affect the arms, face and forehead. They are characterised by very slightly raised, smooth flesh-coloured bumps which range in size from 1 to 5mm in size.

This essay will examine the descriptive epidemiology of HPV infections affecting non-genital cutaneous surfaces. HPV inoculation into epithelium causes proliferation of squamous cells culminating in a clinically apparent warty papule or plaque. In contrast to the generous funding allocated to the surveillance and control of cervical cancer and genital warts, the epidemiology of non-genital cutaneous warts has hitherto attracted little attention. The choice of this disease for this essay has been driven due to its prevalence, its deleterious impact on sufferers with many individuals reporting pain and being stigmatised due to their lesions [6]. It has been stated that most people will experience cutaneous warts at some stage of their lives [7]; if even a small proportion of affected individuals consequently experience psychological distress then this may constitute a significant public health issue.

There is something of a mythology surrounding the best treatment for non-genital cutaneous warts; hypnosis as well as garlic extract have variously been proposed as possible agents, with neither showing benefit beyond placebo [8]. In view of the relative lack of knowledge surrounding the disease, and in view of the transmissible nature of warts, one may be better equipped to prevent this disease if the factors which govern its appearance are better understood.

2. Methodology

2.1. Condition of Interest

As stated above, this essay will focus on the descriptive epidemiology of non-genital cutaneous HPV infection. HPV infection often leads to visible warts (clinical disease), but the virus may also exist in subclinical and latent forms as has been demonstrated by the use of laboratory enhancing techniques (e.g. acetic acid) [9]. For the purpose of this essay as well as for epidemiological study, a case of disease will be defined as the presence of clinically visible warts which occur on non-genital cutaneous surfaces. This case definition and its consequences will be discussed further in the Discussion section.

2.2. Population of Interest

Nongenital cutaneous HPV infection is an under-researched area which, despite its frequency, suffers a relative paucity of data. For this reason, the population of interest is adults and children worldwide.

Search strategy

A literature search was conducted on PubMed, to identify all published studies on the epidemiology of HPV cutaneous infection in adults and children. The retrieved references were either included or excluded as per the criteria described below in Table 1.

Table 1. Table describing the search strategy employed to find studies

It is recognised that PubMed may neglect those studies which have been published in more obscure journals (i.e. those not indexed on PubMed) and that a truly comprehensive approach would utilise alternative engines such as EMBASE, Scirus or LILACS (Literatura Latino-Americana e do Caribe em Ciências da Saúde).

While these engines have their own strengths and weaknesses, PubMed was settled upon for a number of reasons:

1. The ability to use Boolean operators in a multi-stage search – a feature not supported by Google Scholar.

2. The automatic comparison and mapping of keywords from a user query to lists of pre-indexed terms (e.g. Medical Subject Headings or MeSH). This reduces the risk of key studies being missed due to a poor choice of search term.

3. Papers are presented in reverse-chronological order which means that the latest data is examined earlier in the search – this can be an advantage for gaining perspective where the later papers summarise earlier work.

The process of searching published biomedical literature on PubMed is detailed in Figure 1 below.

Figure 1. Flow diagram detailing how the final 229 articles were retrieved

The process of reference snowballing describes the retrieval of papers from the reference list of already included studies. Reverse snowballing identifies those papers which subsequently cite already-included studies ad by using both approaches, one can retrieve more recent as well as older related articles. By utilising this method, the efficiency of the search strategy was increased by enabling the identification of high-quality in more obscure locations resulting in the subsequent inclusion of 15 more studies.

Surveillance data was searched for on a number of sources:

1. Health Protection Agency (HPA) – Health Protection Reports, HPA Syndromic Surveillance Systems

2. Hospital Episode Statistics

3. Centers for Disease Control and Prevention (CDC) – CDC Surveillance Resource Center, National Center for Health Statistics (NCHS)

4. World Health Organization – Global Health Repository

While these sources largely focused on HPV infections leading to cervical cancer and anogenital warts, there was a concerted effort by the NCHS to evaluate the prevalence of skin disease across the United States. This data is presented later in this essay.

3. Results

Data from hospital-based studies is presented below in Table 2. The data is grouped by geographical region.

Table 2. Cases of viral warts recorded in hospital-based studies

Figure 2. Number of wart cases attending the Department of Dermatology at the Royal Infirmary of Edinburgh between 1937 and 2010

Figure 2 below is a scatterplot representing the absolute number of wart cases attending the Dermatology Department at the Royal Infirmary of Edinburgh, United Kingdom.

Population studies

Table 3 below shows the population prevalence estimates produced by three separate studies.

Table 3. Studies examining population prevalence estimates across three different locations

Table 4. Studies examining population prevalence in children of pre-school and school age. Data is ordered by ascending lower age limit

There are four population-based studies aiming at estimating the prevalence of warts in a general population of all ages, three of which are summarised above. The third study by Beliaeva, despite its impressive sample size of 30,518, has been excluded since only the abstract was available in English [23].

There has also been an attempt by authors to describe the prevalence of warts specifically in children of pre-school and school-age. These studies are summarised below in Table 4.

Age

Figure 3 below plots the prevalence of wart cases between age groups by study author.

Gender

Figure 4 and Figure 5 plot the sex-specific prevalence of warts in adults and children respectively.

Occupation

The relative risks of various occupations are presented below in Table 5.

Figure 3. Bar chart plotting the prevalence of warts at different ages (by study)
Figure 4. Bar chart plotting sex-specific prevalence of warts in adults
Figure 5. Bar chart plotting sex-specific prevalence in children

Table 5. Table describing the relative risk of warts in exposed and unexposed occupational groups

Figure 6. Bar chart illustrating relative risk between exposed and control occupational groups

Occupational studies which have utilised a control group (i.e. one which is not exposed to raw meat) enable the calculation of a relative risk. These are presented graphically in Figure 6 below.

4 Discussion

4.1. Limitations
4.1.1. Case Definition

As described earlier, the case definition used for this work is pragmatic and constitutes clinically visible warts affecting non-genital cutaneous surfaces. If one is trying to describe the epidemiology of HPV infection affecting non-genital cutaneous surface, it would clearly be more sensitive to utilise a virological case definition (i.e. microbiological evidence of HPV infection in the skin). In reality, however, these studies have not been performed to date perhaps due to the expense and labour-intensity of establishing HPV infection of the skin. It must be noted that if we use our clinical case definition, we are only identifying a small subset of the actual burden of HPV infection afflicting non-genital cutaneous surfaces (i.e. those infections which progress into warts). Some cases may be minor or transient such that they do not evoke sufficient concern for the patient to seek medical care thereby remaining unidentified cases in the disease iceberg.

Case-in-point, it has already been established that cutaneous HPV DNA is frequently detected in clinically normal skin [39, 40]. Additionally, it must be noted that in the genital tract, clinically apparent warts may make up only a small proportion of the total infected population. Previous work has shown that in a cohort of U.S. college students (n=545) only 2% had visible anogenital warts while 11.4% had detectable HPV DNA or antigen in cervical specimens [41].


4.1.2. Search Strategy

While the search strategy did eventually yield 30 studies, 1 of these papers was excluded due to only the abstract being available in English. The excluded population-based study by Beliaeva [23] has a sample size of 30,518 and describes the prevalence of warts in Russia. Its exclusion introduces a form of publication bias – as the sole reason for this study not being included is due to its language of publication and thus we are losing a significant quantity of useful data. Moreover, the use of snowball searching while being a powerful tool for finding papers may introduce bias into our search. It may be postulated that authors cite previous work by authors who draw similar conclusions to their own. Thus, by trawling through reference lists we may inadvertently end up with a perspective which is unduly influenced by a small group of authors.


4.1.3. Population Versus Hospital-Based Statistics

Stern et al. has estimated that less than 10% of patients with viral warts are referred into secondary care which makes it very difficult to estimate the prevalence of the disease [42]. There are a multitude of factors including economic and social which may influence the general practitioner’s decision to refer to a specialist – these factors may vary widely over decades.

Studies on the incidence of HPV infection are available from both hospital-based and population studies, both of which yield useful information but which must be viewed with the knowledge of their limitations. Case-in-point, one might assume that the hospital dermatologist will be more proficient (and therefore more accurate) in their clinical diagnosis of viral wart than a general physician. A case series of 250 viral warts showed that the clinical diagnosis of viral wart was confirmed by subsequent histologic analysis in 89% of cases [43], while in a separate study general practitioners who were referring patients to secondary care made a diagnosis of viral wart which concurred with the specialist’s opinion in 82% of cases [44]. As stated above, estimating population prevalence from hospital studies is fraught with difficulty since the factors which may influence the generalist to refer to a specialist may vary widely between locations and over time. Additionally, the subset of patients who are referred may represent those recalcitrant or particularly florid cases which may not be representative of the disease as a whole, limiting generalizability of the findings.

Figure 2 examines the prevalence of wart cases at the Dermatology Department of the Royal Infirmary of Edinburgh. It can be seen that there is a gradual increase in wart referrals from 1934 to 1949, when there appears to be a dramatic rise in overall cases of the total new patient workload. The creation of the National Health Service in 1948 may be account for this sudden increase in referrals, which was only curtailed when specific viral wart clinics (with waiting lists of several months acting as a disincentive for referral) were established. Treatments with some efficacy were introduced into primary care between 1960s and 1980s which may account for the relatively low levels of cases which presented to secondary care over this period [45]. Furthermore, the decision to remunerate GPs for cryotherapy in the 1990 GP Contract (despite any evidence demonstrating superiority over conventional topical therapies) may explain the further drop in referrals [46]. This data therefore illustrates the inherent dangers in making inferences on population prevalence from the subset of hospital-based studies.


4.1.4. Paucity of Data

The lack of data in this disease makes drawing conclusions particularly difficult. Referring back to Figure 2, there is no data between 1957 and 1981. Since one safely cannot extrapolate from the existing data, it is unclear what happened over this period thus making it impossible to elucidate any trends.


4.1.5. Reporting of Studies

A cursory glance at the tables included in this study shows that the reporting of the included studies differs significantly. There are no confidence intervals reported for any outcome which limits the reader’s ability to assess the role of chance in any statistical outcomes. There is also poor reporting of the characteristics of the people included in the study as well as response rates which inhibit the assessment of generalisability of findings.

4.2 Conclusions

The above limitations notwithstanding, one can try and draw conclusions from the studies presented in this work.


4.2.1. Time

Due to the relative lack of longitudinal data in multiple locations, it is difficult to confidently declare the presence or absence of any time-based trend. Comparing population prevalence of different populations over time renders may at best be used to draw weak inferences due to the unpredictable interplay of geography and temporal trends. If we explore the prevalence of wart cases in Figure 2, we can see that there is an increasing proportion of viral wart cases until the 1960s; this may reflect a true increase in the incidence of the disease although it might be plausibly be ascribed to the higher threshold of individuals in earlier times to seek specialist care for less troublesome conditions (e.g. medical care was more expensive or less readily accessible). Perhaps in a slightly self-congratulatory tone, physicians in modern times may have a greater clinical sensitivity (owing to improved medical education facilities) which may explain some of the increase in cases. Furthermore, the potential role of confounding in this apparent trend should not be neglected. If warts are more prevalent in older age groups, then the aging demographic over this period may be responsible for some of this increase.


4.2.2. Age

Figure 3 illustrates the prevalence of warts across different age groups. There appears to be little consensus over prevalence trends between different age groups. While Kilkenny et al. found that the prevalence in the 16-18 age group (24.0%) was twice that of the 4-6 age bracket (12.0%), this is in direct opposition to the findings of Larsson and Lidén (age 12: 25.9% versus age 16: 19.0%). Unfortunately, no study adequately explains the method by which schools were selected thereby meaning that selection bias could play a role in any measured outcome.

As can be seen from Table 4, there is significant heterogeneity in the overall prevalence estimates produced by the above studies. van Haalen et al. reports in her study that 56% of children diagnosed with warts only have one wart on their entire skin surface. If this lesion is small and unobtrusive or if clinical examination is limited, it may easily escape diagnosis. In view of this, it may be postulated that the very low prevalence reported by non-specialist medical officers who were merely recording warts as one of many medical diagnoses may represent significant underreporting. Furthermore, those studies which focus solely on the prevalence of warts (e.g. van Haalen et al.) may be expected to be more sensitive in diagnosis than those studies which look for any skin pathologies (e.g. Popescu et al.). The extent of skin examination varies between studies: while dermatologists in Kilkenny’s study [30] examine the entire skin surface, Chen et al. omits hands and feet. Conversely, Kilkenny excludes schools which have less than 100 pupils enrolled which may introduce selection bias into the study. In view of the transmissibility of warts, one may postulate smaller schools may have lower prevalences than larger schools owing to the lower rate of infectious contacts in small schools.


4.2.3. Gender

Figure 4 shows the prevalence ratios of males and females in adult populations. Apart from Furue et. al [19], which did not detect any difference in prevalence, men appear to have a higher prevalence of warts as compared to women.

Figure 5 illustrates the prevalence ratios of boys and girls; conversely, all studies except Van Haalen et al. [29] and Williams et al. [30] show warts to be more frequent in girls. As stated above, however, no study adequately explains the method by which schools were selected.


4.2.4. Place

It is impossible to ascertain the prevalence of viral warts throughout the world as there few population-based studies of skin disease (as seen in Table 2), and the methodology of conducted surveys of prevalence differ. Moreover, since these surveys were conducted at different times, it makes it difficult to compare regions meaningfully.

As can be seen from Table 2 and Table 3, there is limited agreement in the observed rates although this may be a result of genuine variation between regions, the effect of differing study design, or perhaps the confounding influence of differences in population age composition.


4.2.5. Occupation

Viral warts are so common within the meat handling industry that there is a subset of cutaneous HPV infection termed “butcher’s warts”. All studies which utilise a control group show an increased prevalence in those involved in meat handling as compared to their control group. It must be noted that some studies were triggered by factory workers or local authorities becoming concerned with the unusually high prevalence of workers in certain factories and therefore may not be representative of prevalence rates within meat handlers as a whole (e.g. the study by Stehr-Green et al.).

Alternatively, it may be argued that the chronic maceration and trauma sustained by the meat handler during the course of his or her day, combined with humid hands and constant contact with animal fluids provides the perfect storm for infection. Table 5 and Figure 6 both provide strong evidence for the additional risk conferred by occupations which handle meat.

4.3 Recommendations for Future Work

Conducting the literature search has revealed that there are no prior reviews which attempt to bring together the incidence and prevalence data for warts by time, person and place. There remains a woeful lack of population-based studies in non-genital cutaneous HPV infection which could be a fruitful area for future work. The lack of evidence on worldwide prevalence means that more work is needed to assess the burden of this disease on a global scale.

References

[1]  Gottschling M, Göker M, Stamatakis A, Bininda-Emonds OR, Nindl I, Bravo IG. Quantifying the phylodynamic forces driving papillomavirus evolution. Mol Biol Evol 2011; 28(7): 2101-13.
In article      CrossRefPubMed
 
[2]  Mistry N, Wibom C, Evander M. Cutaneous and mucosal human papillomaviruses differ in net surface charge, potential impact on tropism. Virol J 2008; 5: 118.
In article      CrossRefPubMed
 
[3]  Schiffman M, Castle PE. Human papillomavirus: epidemiology and public health. Arch Pathol Lab Med 2003; 127(8): 930-4.
In article      PubMed
 
[4]  Kahn JA. HPV vaccination for the prevention of cervical intraepithelial neoplasia. N Engl J Med 2009; 361(3): 271-8.
In article      CrossRefPubMed
 
[5]  Lowy DR, Schiller JT. Prophylactic human papillomavirus vaccines. J. Clin. 2006; 116(5): 1167-73.
In article      
 
[6]  Ciconte A, Campbell J, Tabrizi S, Garland S, Marks R. Warts are not merely blemishes on the skin: a study of the morbidity associated with having viral cutaneous warts. Australas J Dermatol 2003; 44(3): 169-73.
In article      CrossRefPubMed
 
[7]  Sterling JC. Viral infections. In: Burns DA, Breathnach SM, Cox N, Griffiths C editor(s). Rook Textbook of Dermatology. 7th Edition. Oxford: Blackwell Scientific Publications Ltd, 2004.
In article      CrossRef
 
[8]  Mulhelm E, Pinelis S. Treatment of nongenital cutaneous warts. Am Fam Physician 2011; 84(3): 288-293.
In article      
 
[9]  Wikström A, Hedblad MA, Johansson B, Kalantari M, Syrjänen S, Lindberg M, von Krogh G. The acetic acid test in evaluation of subclinical genital papillomavirus infection: a comparative study on penoscopy, histopathology, virology and scanning electron microscopy findings. Genitourin Med 1992; 68(2): 90-9.
In article      PubMed
 
[10]  McCall AT. Analysis of 10,000 consecutive cases of skin disease met with in hospital practice, in Diseases of the Skin, 2nd Edn, Charles Griffin & CO, London, 1894.
In article      
 
[11]  Ratzer MA. The incidence of skin disease in the west of Scotland. Br J Dermatol 1969; 81: 456-61.
In article      CrossRefPubMed
 
[12]  Hall R, Burrows D. Diagnostic review of hospital dermatology in Northern Ireland 1954-66. Br J Dermatol 1968 Apr;80:261-4.
In article      CrossRefPubMed
 
[13]  Peterkin GAG. The changing patterns of dermatology. Arch Dermatol 1959; 80(1): 1-4.
In article      CrossRef
 
[14]  Benton EC, Hunter JAA. The dermatology out-patient service: a study of out-patient referrals in a Scottish population. Br J Dermatol 1984; 110: 195-201.
In article      CrossRefPubMed
 
[15]  Harris DWS, Benton EC, Hunter JAA. The dermatology out-patient service: a study of out-patient referrals in a Scottish population. 1990; 123: 745-9.
In article      
 
[16]  McKenna DB, Shepherd S, Russell S, Benton EC. Dermatology out-patient workload in the south-east of Scotland. Br J Dermatol 2001; 145 (Suppl. 59): 74.
In article      
 
[17]  Benton EC, Kerr OA, Fisher A. The changing face of dermatological practice: 25 years’ experience. Br J Dermatol 2008; 159: 413-18.
In article      CrossRefPubMed
 
[18]  Holme, S.A., Scott-Lang, V.E., Ooi, E.T., Matthews, A.G., Darling, M.I., Needham, D. and McCormack, S.K.A. The south-east Scotland dermatology workload study: 30 years’ analysis. Br J Dermatol 2012; 167: 123-130.
In article      CrossRefPubMed
 
[19]  Furue M, Yamazaki S, Jimbow K, Tsuchida T, Amagai M, Tanaka T, Matsunaga K Muto M, Morita E, Akiyama M, Soma Y, Terui T, Manabe M. Prevalence of dermatological disorders in Japan: A nationwide, cross-sectional, seasonal, multicenter, hospital-based study. J Dermatol 2001; 38(4): 310-320.
In article      CrossRefPubMed
 
[20]  Johnson ML, Roberts J. Skin conditions and related need for medical care among persons 1-74 years. U.S. Department of Health Education and Welfare Publication 1978; 1660(11): 212.
In article      
 
[21]  Rea JN, Newhouse ML, Halil T. Skin disease in Lambeth. A community study of prevalence and use of medical care. Br J Prev Soc Med. 1976; 30(2): 107-114.
In article      PubMed
 
[22]  Plunkett A, Merlin K, Gill D, Zuo Y, Jolley D, Marks R. The frequency of common nonmalignant skin conditions in adults in central Victoria, Australia. Int J Dermatol 1999; 38(12): 901-8.
In article      CrossRefPubMed
 
[23]  Beliaeva TL. The population incidence of warts. Vestn Dermatol Venerol. 1990; (2): 55-8. [Article in Russian]
In article      PubMed
 
[24]  Toossi P, Nabai L, Alaee Z, Ahmadi H, Saatee S. Prevalence of Skin Diseases and Cutaneous Manifestations Among Iranian Children: A Survey of 1417 Children. Arch Dermatol. 2007; 143(1): 115-26.
In article      CrossRefPubMed
 
[25]  The East Anglia branch of the Society of Medical Officers of Health. The incidence of warts and plantar warts amongst school children in East Anglia. Med Off 1955; 94: 55.
In article      
 
[26]  Van Haalen FM, Bruggink SC, Gussekloo J, Assendelft WJJ, Eekhof JAH. Warts in primary schoolchildren: prevalence and relation with environmental factors. Br J Dermatol 2009; 161(1): 148-52.
In article      CrossRefPubMed
 
[27]  Kilkenny M, Merlin K, Young R, Marks R. The prevalence of common skin conditions in Australian school students: 1. Common, plane and plantar viral warts. Br J Dermatol 1998;138: 840-845.
In article      CrossRefPubMed
 
[28]  Chen GY, Cheng YW, Wang CY, Hsu TJ, Hsu MML, Yang PT, Chen WC. Prevalence of skin diseases among schoolchildren in Magong, Penghu, Taiwan: a community-based clinical survey. J Formos Med Assoc 2008; 107(1): 21-9.
In article      CrossRef
 
[29]  Popescu R, Popescu CM, Williams HC, Forsea D. The prevalence of skin conditions in Romanian school children. Br J Dermatol 1999; 140(5): 891-6.
In article      CrossRefPubMed
 
[30]  Williams HC, Pottier A, Strachan D. The descriptive epidemiology of warts in British schoolchildren. Br J Dermatol 1993; 128(5): 504-11.
In article      CrossRefPubMed
 
[31]  Larsson PA, Lidén S. Prevalence of skin diseases among adolescents 12--16 years of age. Acta Derm Venereol. 1980; 60(5): 415-23.
In article      PubMed
 
[32]  de Peuter M, de Clercq B, Minette A, Cachapelle JM. An epidemiological survey of virus warts of the hands among butchers. Br J Dermatol 1977; 96(4): 427-31.
In article      CrossRefPubMed
 
[33]  Gabal MS, el Geweily M. Dermatologic hazards among slaughterhouse workers. J Egypt Public Health Assoc. 1990; 65(1-2): 191-206.
In article      PubMed
 
[34]  Stehr-Green PA, Hewer P, Meekin GE, Judd LE. The Aetiology and Risk Factors for Warts among Poultry Processing Workers. Int J Epidemiol 1993; 22(2): 294-298.
In article      CrossRefPubMed
 
[35]  Guillet G, Borredon J, Duboseq MF. Prevalence of warts on hands of poultry slaughterers and poultry workers. Arch Dermatol 1987; 123(6): 718-9.
In article      CrossRefPubMed
 
[36]  Litt JZ. Warts in meat-cutters. Arch Dermatol. 1969; 100(6): 773.
In article      CrossRefPubMed
 
[37]  Mergler D, Vezina N, Beauvais A. Warts among workers in poultry slaughterhouses. Scand J Work Environ Health. 1982; 8( Suppl 1): 180-4.
In article      PubMed
 
[38]  Keefe M, Al-Ghamdi A, Coggon D, Maitland NJ, Egger P, Keefe CJ, Carey A, Sanders CM. Cutaneous warts in butchers. Brit J Dermatol 1994;130: 9-14.
In article      CrossRefPubMed
 
[39]  Chen AC, McMillan NAJ, Antonsson A. Human papillomavirus type spectrum in normal skin of individuals with or without a history of frequent sun exposure. J Gen Vir 2008; 89: 2891-7.
In article      CrossRefPubMed
 
[40]  Escutia B, Ledesma E, Serra-Guillen C, Gimeno C, Vilata JJ, Guillén C, Nagore E. Detection of human papilloma virus in normal skin and in superficial and nodular basal cell carcinomas in immunocompetent subjects. J Eur Acad Dermatol Venereol. 2011; 25(7): 832-8.
In article      CrossRefPubMed
 
[41]  Kiviat NB, Koutsky LA, Paavonen JA, Galloway DA, Critchlow CW, Beckmann AM, McDougall JK, Peterson ML, Stevens CE, Lipinski CM. Prevalence of genital papillomavirus infection among women attending a college student health clinic or a sexually transmitted disease clinic. J Infect Dis 1989; 159(2): 293-302.
In article      CrossRefPubMed
 
[42]  Stern RS, Johnson ML, DeLozier J, Anderson PC. Utilization of Physician Services for Dermatologic Complaints The United States, 1974. Arch Dermatol. 1977; 113(8): 1062-6.
In article      CrossRefPubMed
 
[43]  Parslew, RAG Rhodes, LE. Accuracy of diagnosis of benign skin lesions in hospital practice: a comparison of clinical and histological findings. J Eur Acad Dermatol Venereol 1997; 9: 137-41.
In article      CrossRef
 
[44]  Basarab T, Munn SE Russell Jones R. Diagnostic accuracy and appropriateness of general practitioner referrals to a dermatology out-patient clinic. Br J Dermatol 1996; 135(1): 70-3.
In article      CrossRefPubMed
 
[45]  Gibbs S, Harvey I, Sterling J, Stark R. Local treatments for cutaneous warts: systematic review. BMJ. Aug 2002;325(7362):461.
In article      CrossRefPubMed
 
[46]  Pockney P, George S, Primrose J, Smith H, Kinley H, Little P, Lattimer V, Lowy A, Kneebone R. Impact of the introduction of fee for service payments on types of minor surgical procedures undertaken by general practitioners: observational study. J Public Health Oct 2004; 26(3): 264-7.
In article      CrossRefPubMed
 
  • CiteULikeCiteULike
  • Digg ThisDigg
  • MendeleyMendeley
  • RedditReddit
  • Google+Google+
  • StumbleUponStumbleUpon
  • Add to DeliciousDelicious
  • FacebookFacebook
  • TwitterTwitter
  • LinkedInLinkedIn