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Anais Brasileiros de Dermatologia

Print version ISSN 0365-0596

An. Bras. Dermatol. vol.85 no.5 Rio de Janeiro Sept./Oct. 2010 



Clinical and histopathological characterization and typing of the human papillomavirus in common warts of kidney transplant recipients



Flavia Martelli-MarzagãoI; Alberto Shodi YamashiroII; Marilia Marufuji OgawaIII; Gildo Francisco dos Santos JrIV; Jane TomimoriV; Adriana Maria PorroVI

ICurrently participating in the postgraduate program in Clinical and Surgical Dermatology, Federal University of São Paulo (UNIFESP), São Paulo, SP, Brazil
IIUndergraduate medical student participating in the Scientific Initiation Program, Federal University of São Paulo (UNIFESP), São Paulo, SP, Brazil
IIIPhysician; Master's Degree, Department of Dermatology, Federal University of São Paulo (UNIFESP), São Paulo, SP, Brazil
IVPhD, Biomedical Scientist. Association Funding Incentives for Psychopharmacology (AFIP), Laboratory Medicine, São Paulo, SP, Brazil
VAssociate Professor, Department of Dermatology, Federal University of São Paulo (UNIFESP), São Paulo, SP, Brazil. Advisor of students in the scientific initiation and postgraduate programs, Federal University of São Paulo (UNIFESP), São Paulo, SP, Brazil
VIAdjunct Professor, Department of Dermatology. Co-Advisor of students in the scientific initiation and postgraduate programs, Federal University of São Paulo (UNIFESP), São Paulo, SP, Brazil

Mailing address




The prevalence of skin lesions caused by the human papillomavirus (HPV) is high in kidney transplant patients. Twenty recipients of kidney transplants with a diagnosis of common warts were evaluated. HPV detection was performed by polymerase chain reaction (PCR) using the MY09/MY11 and RK91 primers. HPV typing was performed by restriction fragment length polymorphism analysis and direct sequencing. The presence of HPV was identified in 10 patients (50%) and the types identified were HPV-2, 27, 29, 34 and 57.

Keywords: Human papillomavirus infections; Kidney transplant; Warts



Kidney transplant recipients have a 15-50% likelihood of developing common warts associated with the human papillomavirus (HPV) in the first year following the transplant and a 77-95% likelihood within five years.1 With respect to the detection and typing of HPV in common warts, few publications are available of studies conducted in the Brazilian population, the only study having been carried out in an immunocompetent population infected by the human immunodeficiency virus (HIV) and in patients with epidermodysplasia verruciformis.3 Therefore, the objective of the present study was to evaluate the clinical and histopathological characteristics of common warts in kidney transplant recipients and identify the types of HPV present in the lesions.

Twenty kidney transplant recipients with a clinical and histopathological diagnosis of common warts were evaluated and submitted to HPV detection (using polymerase chain reaction [PCR] with the MY09/11 and RK91 primers) and typing (using restriction fragment length polymorphism analysis [RFLP] and/or direct sequencing).

The mean age of the patients was 47.9 years. There was no difference in the incidence of the condition between the sexes (Table 1).

Eighty percent of the patients had more than one common wart, with 25% having more than 20 lesions, thus confirming the ease of infection and dissemination of HPV in kidney transplant recipients (Figure 1).



After six months of high-dose immunosuppressive therapy (induction phase), the dose of immunosuppressive drugs administered to the kidney transplant recipients was reduced in the so-called maintenance phase. In agreement with other reports in the literature,4 it was in this phase that the highest frequency of common warts was found. The mean time since transplantation in patients in this study was 76.9 months.

Typical histopathological findings in common warts of immunocompetent individuals, such as hyperkeratosis, hypergranulosis and papillomatosis, were also found in the kidney transplant recipients. With respect to the histopathological signs of viral activity in these common warts, a high frequency of koilocytosis was found (85%) and, to a lesser extent, the presence of clumps of keratohyalin granules (70%). Parakeratosis was a less frequent finding (20%). This may represent a histological characteristic of old warts and, indirectly, the chronicity of this process in kidney transplant recipients, and is in agreement with the long duration of the condition, as reported by the patients. Analyzing the presence of vacuolization of the keratinocytes, which also characterizes viral infection, this was found principally in the upper layers of the epidermis, in agreement with lesions described in the literature (Figure 2).5

The HPV types described in the international literature as being the most frequently found in common warts of immunocompetent individuals are HPV-2, HPV-27 and HPV-57. 6 In the present study, the presence of HPV was detected in 10 patients (50%). HPV2, HPV-34 and HPV-57 were detected in two samples each and HPV-27 and HPV-29 in one sample each (Table 2). In two patients, the HPV types were not identified despite their positivity for the MY09/MY11 and RK91 primers. HPV-2, HPV-27, HPV-29 and HPV57 have already been described in common warts of kidney transplant recipients. 7-9 One interesting finding was that HPV-34, an alpha-papillomavirus commonly described in mucosal infections, was identified in two of the patients in the present study. On the other hand, HPV-2, HPV-27, HPV-29 and HPV-57 have been detected all over the skin. The MY09/11 and RK91 primers failed to detect any of the types described in epidermodysplasia verruciformis in the patients in the present study. 10

Depending on the HPV type, skin infection may be associated with an increase in the incidence of carcinomas, particularly squamous cell carcinoma. In kidney transplant recipients, the proliferation of keratotic lesions in exposed areas often results in diagnostic confusion between common warts, actinic keratoses and seborrheic keratoses as well as squamous cell carcinoma. The presence of multiple, polymorphic and atypical skin lesions was also found in the population of the present study, principally in exposed areas subject to micro-traumatisms and sun exposure such as the upper and lower limbs.

The low detection rate of HPV in the lesions of patients in this study may be explained by the presence of unusual HPV types not commonly found in common warts. In this case, repeating PCR using other primers may increase the likelihood of HPV detection.



1. Glover MT, Niranjam N, Kwan J, Leigh IM. Warts and skin cancer in renal allograft recipients: the extent of the problem and a strategy for management. Br J Plastic Surg. 1994;47:86-9.         [ Links ]

2. Porro AM, Alchorne MM, Mota GR, Michalany N, Pignatari AC, Souza IE. Detection and typing of human papillomavirus in cutaneous warts of patients infected with human immunodeficiency virus type 1. Br J Dermatol. 2003;149:1192-9.         [ Links ]

3. de Oliveira WR, He Q, Rady PL, Hughes TK, Festa Neto C, Rivitti EA, Tyring SK. HPV Typing in brazilian patients with epidermodysplasia verruciformis: high prevalence of EV-HPV 25. J Cutan Med Surg. 2004;8:110-5.         [ Links ]

4. Ferreira RMCXC, Coelho MRCD, Guimarães PB, Montarroyos UR, Ferreira CZ. Freqüência de verrugas virais em transplantado renal. Revista Paraense de Medicina. 2003;17:12-17.         [ Links ]

5. Burns T, Breathnach S, Cox N, Griffiths C, eds. Rook's textbook of dermatology. 7th ed. Oxford: Blackwell Science; p. 25.42-25.60, 36.40.         [ Links ]

6. Rübben A, Kalka K, Spelten B, Grussendorf-Conen EI. Clinical features and age distribution of patients with HPV 2/27/57-induced common warts. Arch Dermatol Res. 1997;289:337-40.         [ Links ]

7. Shamanin V, Glover M, Rausch C, Proby C, Leigh IM, zur Hausen H, et al. Specific types of human papillomavirus found in benign proliferations and carcinomas of the skin in immunosuppressed patients. Cancer Res. 1994;54:4610-3.         [ Links ]

8. de Villiers EM, Lavergne D, McLaren K, Benton EC. Prevailing papillomavirus types in non-melanoma carcinomas of the skin in renal allograft recipients. Int J Cancer. 1997;73:356-61.         [ Links ]

9. Berkhout RJ, Bouwes-Bavinck JN, ter Schegget J. Persistence of human papillomavirus DNA in benign and (pre)malignant skin lesions from renal transplant recipients. J Clin Microbiol. 2000;38:2087-96.         [ Links ]

10. Wieland U, Pfister H. Papilomavirus em patologia humana: epidemiologia, patogênese e papel oncogênico. In: Gross G, Barrasso R, ed - Infecção por papilomavirus humano/ Atlas clínico de HPV. Porto Alegre: Artes Médicas; 1999. p.1-18.         [ Links ]



Mailing address:
Adriana Maria Porro
Alameda Jauaperi, 975, ap. 31, Moema
04523 014 São Paulo - SP - Brazil
Telephone.: +55 11 5576 4804

Received on 28.04.2009.
Approved by the Advisory Board and accepted for publication on 19.03.10.
Conflict of interest: None
Financial funding Funding was received from a CNPq-PIBIC grant for the undergraduate student, and from CAPES, which provided support for the Postgraduate Program in Clinical and Surgical Dermatology, Federal University of São Paulo (UNIFESP).



* Study conducted at: the Federal University of São Paulo, Escola Paulista de Medicina, São Paulo, SP, Brazil.

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