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Figure 1.
Perianal condylomata acuminata and chronic ulcers (case 14). A 38-year-old man with condylomata and chronic HSV ulcers of 45 days' duration: CD4 cell count, 6 cells/µL; herpes simplex virus 2 was isolated on culture of the ulcer and exudate. Cytomegalovirus was found in the ulcer.

Perianal condylomata acuminata and chronic ulcers (case 14). A 38-year-old man with condylomata and chronic HSV ulcers of 45 days' duration: CD4 cell count, 6 cells/µL; herpes simplex virus 2 was isolated on culture of the ulcer and exudate. Cytomegalovirus was found in the ulcer.

Figure 2.
Oral and perioral chronic ulcers (case 17). A 34-year-old woman (an injection drug user) with ulcers of 4 months' duration (CD4 cell count, 14 cells/µL). Herpes simplex virus 1 was isolated on a culture of the ulcer and exudate. Cytomegalovirus was found in lesional tissue.

Oral and perioral chronic ulcers (case 17). A 34-year-old woman (an injection drug user) with ulcers of 4 months' duration (CD4 cell count, 14 cells/µL). Herpes simplex virus 1 was isolated on a culture of the ulcer and exudate. Cytomegalovirus was found in lesional tissue.

Figure 3.
Trigeminal herpes zoster (case 4). A 45-year-old woman with hemifacial crusted vesicles of 21 days' duration. Lesions of disseminated herpes zoster were found on the trunk and legs; the CD4 cell count was 36 cells/µL. Cytomegalovirus was found in lesional skin.

Trigeminal herpes zoster (case 4). A 45-year-old woman with hemifacial crusted vesicles of 21 days' duration. Lesions of disseminated herpes zoster were found on the trunk and legs; the CD4 cell count was 36 cells/µL. Cytomegalovirus was found in lesional skin.

Table 1. 
Clinical Data Regarding the Patients With CMV in Mucocutaneous Lesions (Study 1)*
Clinical Data Regarding the Patients With CMV in Mucocutaneous Lesions (Study 1)*
Table 2. 
Histologic and Microbiological Data Regarding the Patients With CMV in Mucocutaneous Lesions (Study 1)*
Histologic and Microbiological Data Regarding the Patients With CMV in Mucocutaneous Lesions (Study 1)*
1.
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3.
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Penneys  NHicks  B Unusual cutaneous lesions associated with acquired immunodeficiency syndrome. J Am Acad Dermatol. 1985;13845- 852Article
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Husain  SEvans  LRabinowitz  AGrossman  M Cytomegalovirus inclusion disease presenting as a cutaneous ulcer in AIDS. Arch Dermatol. 1994;1301312- 1315Article
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Friedman  MBrenski  ATaylor  L Treatment of aphthous ulcers in AIDS patients. Laryngoscope. 1994;104566- 570Article
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Syrjanen  SLeimola-Virtanen  RSchmidt-Westhausen  AReichart  PA Oral ulcers in AIDS patients frequently associated with cytomegalovirus (CMV) and Epstein-Barr virus (EBV) infections. J Oral Pathol Med. 1999;28204- 209Article
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Liang  GDaikos  GSerfling  U  et al.  An evaluation of oral ulcers in patients with AIDS and AIDS-related complex. J Am Acad Dermatol. 1993;29563- 568Article
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Cohen  SSchmitt  SLucas  FWexner  S The diagnosis of anal ulcers in AIDS patients. Int J Colorectal Dis. 1994;9169- 173Article
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Horn  THood  A Cytomegalovirus is predictably present in perineal ulcers from immunosuppressed patients. Arch Dermatol. 1990;126642- 644Article
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LaGuardia  KLWhite  MSaigo  PHoda  SMcGuinness  KLedger  W Genital ulcer disease in women infected with human immunodeficiency virus. Am J Obstet Gynecol. 1995;172553- 562Article
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Macasaet  FHolley  KSmith  TKeys  T Cytomegalovirus studies of autopsy tissue, II: incidence of inclusion bodies and related pathologic data. Am J Clin Pathol. 1975;63859- 865
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Smith  THolley  KKeys  TMacasaet  F Cytomegalovirus studies of autopsy tissue, I: virus isolation. Am J Clin Pathol. 1975;63854- 858
22.
Boudreau  SHines  HHood  A Dermal absesses with staphylococcus aureus, cytomegalovirus and acid-fast bacilli in a patient with AIDS. J Cutan Pathol. 1988;1553- 57Article
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Toome  BBowers  KScott  G Diagnosis of cutaneous cytomegalovirus infection: a review and report of a case. J Am Acad Dermatol. 1991;24860- 863Article
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Duran  RFraga  JSanz  J Infección por citomegalovirus oral en un paciente con síndrome de inmunodeficiencia adquirida [letter]. Med Clin (Barc). 1991;97276
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Ghigliotti  GCanessa  APastorino  AMazzarello  GMarchi  RdGambini  C Vasculite nécrosante produite par le cytomégalovirus chez une malade atteinte du syndrome d'immunodéficience acquise. Ann Dermatol Venereol. 1994;121820- 822
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Nicolas  MTribo  MBarranco  LDrobnic  LGimenez-Camarasa  J Ulcera cutánea por citomegalovirus en paciente con SIDA. Med Cut ILA. 1995;2329- 32
27.
Kwan  TKaufman  H Acid-fast bacilli with cytomegalovirus and herpes virus inclusions in the skin of an AIDS patient. Am J Clin Pathol. 1986;85236- 238
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Lee  YPeel  R Concurrent cytomegalovirus and herpes simplex virus infections in skin biopsy specimens from two AIDS patients with fatal cytomegalovirus infection. Am J Dermatopathol. 1989;11136- 143Article
29.
Fleischmann  MMilpied  BDreno  B  et al.  Ulcérations cutanées à cytomégalovirus au cours du SIDA: diagnostic par hybridation in situ et réponse au traitement. Ann Dermatol Venereol. 1992;119877- 879
30.
Regezi  JAEversole  LRBarker  BFRick  GMSilverman Jr  S Herpes simplex and cytomegalovirus coinfected oral ulcers in HIV-positive patients. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1996;8155- 62Article
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Nuñez  MMiralles  ESHilara  YPintado  VHarto  ALedo  A Concurrent cytomegalovirus, M. tuberculosis and M. avium-intracellulare cutaneous infection in an HIV patient. J Dermatol. 1997;24401- 404
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Pariser  R Cytomegalovirus infection in an immunosuppressed man. J Am Acad Dermatol. 1985;12720- 721Article
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Michiels  JFMonteil  RAHofman  P  et al.  Oral leishmaniasis and Kaposi's sarcoma in an AIDS patient. J Oral Pathol Med. 1994;2345- 46Article
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Garcia-Patos  VPujol  RCurell  RMoragas  JD CMV-induced cytopathic changes in skin biopsy specimens: clinicopathologic study in patients with the acquired immunodeficiency syndrome and an active extracutaneous CMV infection. Arch Dermatol. 1992;1281552- 1553Article
40.
Wilcox  CMChalasani  NLazenby  ASchwartz  DA Cytomegalovirus colitis in acquired immunodeficiency syndrome: a clinical and endoscopic study. Gastrointest Endosc. 1998;4839- 43Article
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Study
April 2001

Mucocutaneous Presence of Cytomegalovirus Associated With Human Immunodeficiency Virus InfectionDiscussion Regarding Its Pathogenetic Role

Author Affiliations

From the Departments of Dermatology (Drs Daudén, Fernández-Buezo, Fraga, and García-Díez), Pathology (Dr Fraga), and Microbiology (Dr Cardeñoso), Hospital de la Princesa, Autonoma University of Madrid, Madrid, Spain.

Arch Dermatol. 2001;137(4):443-448. doi:10-1001/pubs.Arch Dermatol.-ISSN-0003-987x-137-4-dst00030
Abstract

Objectives  To investigate the significance of cytomegalovirus (CMV) in mucocutaneous lesions in patients with human immunodeficiency virus (HIV), and to elucidate its pathogenetic role in lesions genesis.

Design  Retrospective (study 1) and prospective (studies 2 and 3) surveys.

Setting  Departments of Dermatology, Pathology, and Microbiology at a university hospital in Madrid, Spain.

Patients  Seventeen HIV-infected patients with CMV presenting any type of mucocutaneous lesions (study 1); 27 HIV-positive patients with mucocutaneous vesicles and/or ulcers of any type and location (study 2); and 12 severely immunosuppressed HIV-positive volunteers (study 3).

Interventions  Mucocutaneous biopsy specimens from the lesions (studies 1 and 2) and from nonlesional skin (study 3) were analyzed by light microscopy, immunohistochemical analysis, and microbiological analysis (standard viral culture and shell-vial technique).

Main Outcome Measures  Clinical data; histologic, immunohistochemical, and microbiological findings.

Results  (1) Studies 1 and 2: Most of the lesions where CMV was found were ulcers localized mainly on perianal, genital, and perigenital areas, usually as part of polymicrobial infections, particularly herpes simplex and varicella-zoster virus infections. The finding of CMV was confirmed in all cases by light microscopy; microbiological analysis was rarely useful. The finding of mucocutaneous CMV inclusions allowed their early detection in extracutaneous locations. (2) Study 3: Cytomegalovirus was present on healthy skin of the perianal area in 3 patients, and on the forearm in 1 patient.

Conclusion  Cytomegalovirus does not play any significant pathogenetic role at least in most of the cutaneous lesions where it is found.

THE CYTOMEGALOVIRUS (CMV) is a β-herpesvirus that has recently become important as an opportunistic agent in different immunosuppressive conditions, particularly in human inmunodeficiency virus (HIV) infection.1 There are still numerous controversial aspects of the natural history of CMV infection and its pathogenetic role in the induction of lesions in the tissues, especially in the skin and in the mucous membranes. To better characterize the significance of CMV in mucocutaneous lesions in HIV-infected patients, and to elucidate its pathogenetic role, we performed a clinicopathologic and microbiological study with 3 steps.

PATIENTS AND METHODS
STUDY 1

From March 1987 until December 1999, all biopsy material and records of 17 patients infected with the HIV with CMV in any type of mucocutaneous lesions were retrospectively reviewed. We performed immunohistochemical analysis on formalin-fixed, paraffin-embedded tissue. We applied a standard protocol with the avidin-biotin-peroxidase method, using monoclonal antibodies against the immediate early and early antigens of human CMV (1:25 Dako; Copenhagen, Denmark). The biopsy specimens and the exudate of the lesions were cultured and incubated for at least 1 month in a monolayer of human embryonic pulmonary fibroblasts (MRC-5 cell line) using standard viral culture. For the shell-vial technique, we used fluorescent antibodies against immediate early and early antigens of human CMV (CMV Microtrak; Syva Company, St Louis, Mo), with review after 24 and 48 hours.

STUDY 2

Based on study 1, which demonstrated that the mucocutaneous lesions in which CMV was most frequently found were vesicles or ulcers, we started a prospective study including 27 consecutive patients infected with HIV with mucocutaneous vesicles and/or ulcers of any type and location. A lesional skin or mucous membrane biopsy specimen was analyzed, both histologically (multiple sections stained with hematoxylin-eosin) and microbiologically (standard viral culture and shell-vial technique). The exudates from the ulcers or the content of the vesicles were also cultured microbiologically. Informed consent was obtained from all patients.

STUDY 3

Based on studies 1 and 2, in which the presence of CMV was most prevalent in the perianal area, and considering the hematological dissemination of the CMV, we carried out a prospective study on 12 patients who came to our department with different dermatoses. All the patients were infected with HIV and were severely immunosuppresed (CD4 cell count less than 150 cells/µL). We performed 2 nonlesional cutaneous biopsies on the perianal region and the external aspect of the forearm, respectively. They were studied histologically and microbiologically. Informed consent was obtained from all patients.

RESULTS
STUDY 1

The data for study 12,3 are summarized in Table 1 and Table 2. All the patients fulfilled criteria for AIDS. Most of the men were homosexuals with anal practices. Most of the patients were studied before highly active antiretroviral therapy was available, having received treatment with only 1 or 2 reverse transcriptase inhibitors, mainly zidovudine. Only 1 patient had CMV extracutaneously (case 10, retinitis) when he was first treated in our department. Most of the lesions in which CMV was found were ulcers (82.3%) mainly localized in the perianal, genital, and perigenital areas (70.5%) (Figure 1). All but 1 of the patients with ulcers localized in the perianal, genital, and perigenital areas were gay men. The rest of the lesions were vesicles in different locations (Figure 2). Most of the patients had more than 1 lesion (15 of 17 cases). In most cases, the CMV was part of polymicrobial infections with herpes simplex virus (HSV) 1 or 2, or varicella-zoster virus (VZV) (Figure 3). In the case of 1 patient, CMV was associated with bacillary angiomatosis. As for the remaining 4 patients with nonetiologically diagnosed ulcers, 2 of them had been previously treated with acyclovir, and in the other 2, the biopsy specimen included only the center of the ulcer, without epidermis. These data, together with the fact that several of these patients reported the presence of pruriginous grouped vesicles prior to the eruption of ulcers, led us to consider the diagnosis of herpes simplex as the most probable.

Cytomegalovirus was always found using light microscopy with hematoxylin-eosin stain. The most characteristic finding was a granulation tissue in which the cytomegalic cells were found. Their number was very variable, and sometimes it was necessary to carry out a meticulous investigation using numerous sections of the biopsy. The cytomegalic inclusions were most frequently found within the endothelial cells in the mid dermis, though they also occurred free in the dermis and within the vessel lumina. Signs of herpetic infection (11 of 17 patients) occurred in the epidermis close to the ulcer, sometimes involving the follicles and eccrine glands. Eccrine squamous syringometaplasia occurred in 2 patients. By means of immunohistochemical analysis, the presence of CMV was confirmed in all patients but 1. The CMV was isolated from neither the biopsy specimens nor from ulcer exudates. The shell-vial technique detected CMV in the skin of only 1 patient.

All patients had antibodies against CMV (titers ranging from 1:8 to 1:2048) and were severely immunosuppressed (fewer than 100 CD4+ cells/µL in 15 of 17 patients). In 4 patients, the demonstration of CMV was carried out simultaneously with the diagnosis of HIV infection. The finding of cytomegalic cells in mucocutaneous lesions led to the simultaneous detection of CMV in other tissues and/or fluids in 6 patients. During the follow-up, the early detection of CMV in 5 more patients resulted in a prompt treatment. The extracutaneous involvement included the retina, central nervous system, lung, esophagus, stomach, colon, rectum, liver, and blood. Most of the cutaneous lesions disappeared when treated with acyclovir, even in 3 cases in which neither HSV nor VZV were detected. New outbreaks had a satisfactory response with the same treatment. The patient with bacillary angiomatosis did not respond to ganciclovir but was cured with erythromycin. The follow-up ranged from 1 to 36 months and, at the end of it, 11 patients had died and 5 were in a terminal situation. The remaining patient was lost to follow-up.

STUDY 2

We studied 27 HIV-infected patients, 4 women and 23 men (aged 25-54 years). Most were either homosexuals (13/27) or injection drug users (10/27). All but 4 (85.2%) had a CD4 cell count lower than 200 cells/µL. Anti-CMV antibiotics were found in 16 of 16 patients. The diagnoses of the mucocutaneous lesions from which biopsies were taken were as follows: 13 herpes simplex (9 perianal, 2 oral, and 1 lumbar ulcer and 1 disseminated herpes simplex), 11 herpes zoster (6 costal, 2 trigeminal, 2 disseminated, and 1 lumbosacral), 1 patient with luetic oral ulcers, and 2 patients with nonetiologically diagnosed ulcers. Only 2 patients had received acyclovir prior to the study. Findings of a histopathologic evaluation revealed CMV in 6 patients (22.2%), all of whom had perianal ulcers. In 4 patients, CMV coincided with signs of herpetic infection in the epidermis from the same sections; in 1 patient, HSV was cultured from the same lesion. Cytomegalovirus was found alone in the remaining patient, who had received treatment with acyclovir during the previous 7 days. Five patients were homosexual and 1 was an injection drug user. They were all severely immunosuppressed (CD4 cell count lower than 100 cells/µL). The CMV was isolated (using the shell-vial technique to analyze the biopsy specimens) in only 1 patient. The standard viral culture (biopsy specimen and exudate) and shell-vial technique of the exudate demonstrated the presence of HSV-1, HSV-2, and VZV, but not of CMV. The detection of CMV in the skin allowed a subsequent finding of CMV in different extracutaneous locations (meninges, retina, lung, and blood) in 4 patients.

STUDY 3

We studied 12 patients (11 men and 1 woman) aged from 26 to 54 years. Nine of them were homosexuals, 1 was heterosexual, and 1 was an IDU. All of them had antibodies against CMV. The presenting problems varied: 9 patients had perianal ulcers (7 with HSV infection [3 of whom also had cytomegalic inclusions] and 2 with CMV alone); 1 had lumbar-sacral herpes zoster; 1, perianal condylomas; and 1, herpetic oral ulcers. A histopathologic study on healthy skin of the perianal area revealed the presence of CMV in 3 cases. In 1 case it was found in the forearm. The latter 3 patients had surrounding perianal ulcers with CMV. Standard viral culture and shell-vial findings were negative for CMV in all cases. The CMV was detected in extracutaneous locations in 4 patients (including the 3 with CMV in healthy skin).

COMMENT

Cytomegalovirus infection is common in HIV-infected patients, but its presence in mucocutaneous lesions is rarely reported. The reported clinical presentations have been very variable, including ulcers, vesicles, purpuric macules, verrucous lesions, prurigo nodularis–like lesions, erythematous and crusted papules, and digital infarcts.312 Several studies with variable and even contradictory results have investigated the role of CMV in ulcers in different locations in HIV-positive patients.1319 Our data confirm that while there were no characteristic mucocutaneous lesions diagnostic for CMV infection, the presence of persistent anogenital ulcers and, less frequently, oral ulcers in HIV-infected patients should make one suspect and search carefully for the presence of CMV in these lesions.

There is a controversy regarding the comparative sensitivity among the different diagnostic techniques used to determine the presence of CMV in mucocutaneous lesions,.18,20,21 From our experience, light microscopy with hematoxylin-eosin stain is the most sensitive tool. Because the number of cells containing CMV is very variable, and sometimes only 1 or 2 infected cells are found in each section of the tissue, we recommend a meticulous search and a serial sectioning of the samples. Cytomegalovirus inclusions are mostly found in the endothelial cells but, occasionally, they have also occurred inside the keratinocytes,5,7 in sweat gland epithelial cells,5 and in macrophages2224 and fibroblasts.7,25,26 The smears from the ulcers are rarely if ever useful. Immunohistochemical analysis is useful to confirm the diagnosis in certain cases (eg, intense inflammation). The standard viral culture of mucocutaneous biopsy specimens is not useful to diagnose CMV infection. Since coinfection with HSV/VZV is often present, these viruses destroy the monolayer of human fibroblasts and prevent the growth of CMV. The shell-vial technique, with an early evaluation at 24 hours, is an attempt to avoid this problem, but in our series its usefulness was very low.

Nevertheless, the finding of CMV in the skin/mucosa raises several questions: What is the predictive significance of its presence in immunosuppressed patients? Second, is CMV alone capable of inducing tissue damage of the skin and/or mucosa? And finally, why are most CMV lesions located in the perianal region? The interpretation of the presence of CMV in the skin and/or mucosa is controversial. Its presence could indicate that CMV plays a pathogenetic role, both in the origin of the lesions and in their chronicity. But, it could also simply be the expression of the endothelial colonization that occurs during the course of a hematogenous disseminated infection (sometimes the detection of CMV within the skin is simultaneous with the viremia5). It might also be that the CMV has reactivated within the endothelial cells, which have thus acted as reservoirs during the latency period. Or the presence of CMV might be a consequence of an autoinoculation by the shedding of CMV through the feces, the urine, or the saliva. It is difficult to establish a cause-effect relationship between the clinical lesion and the presence of CMV in that lesion. In other words, the presence of CMV does not necessarily indicate the etiology of the pathologic process.

The following could be arguments in favor of a pathogenetic role: (1) The causality of CMV in retinitis has been accepted. However, the same is not true for CMV in the blood, the urine, the lung, or in stool. (2) There are reports of histopathologic reactions (inflammatory infiltrate, necrosis, etc) in association with the presence of CMV and signs of cytopathic viral effect without evidence of other antimicrobial agents.14 Our experience does not agree with these previous reports. (3) It has been reported that there is a correlation between the intensity of the inflammatory infiltrate and the number of cytomegalic cells that are apparently responsible for that reaction. However, it is also true that the greater number of vessels and inflammatory cells provides increased potential expression of CMV during viremia. (4) There is an absence of CMV in most lesional skin biopsy specimens from different cutaneous diseases in patients with systemic CMV infection and viremia.

Arguments against a pathogenetic role of CMV are as follows: (1) Cytomegalovirus is frequently observed or cultured with other infectious agents that have a recognized pathogenetic role and alone could induce the etiologic process. Apart from the well-known association of CMV with HSV,3,7,14,18,2730 its presence has also been associated with Staphylococcus aureus and acid-fast bacili.22,27,31 Our results indicate that most mucocutaneous CMV lesions are associated with either HSZ or VZV infection. The reasons for not finding these viruses in some cases could be (a) the minimal portion or absence of epidermis in some biopsy specimens (cases 5 and 6 in study 1); (b) marked epidermal necrosis; (c) false-negative findings in diagnostic techniques16,28,32; or (d) previous treatment with acyclovir, which might have made the HSV/VZV, but not the CMV, disappear (cases 2 and 16 in study 1). (2) Unexpected findings of CMV have occurred in unrelated skin lesions (patient 3),2 in 2 other patients with bacillary angiomatosis,33,34 in a case of Kaposi sarcoma,3538 and even in a case of a posttraumatic scar,39 all of which are conditions with a well-developed vascularity. (3) Cytomegalovirus has occurred in apparently healthy skin. In our study 3, three patients had CMV in perianal healthy skin, 1 with inclusions on the skin of the forearm, far from the lesions in which CMV had been observed. This finding has also been described in a patient with active extracutaneous CMV infection.39 And (4) spontaneous healing has occurred of lesions in which CMV was isolated.11,24

On the basis of all these data, we believe that CMV does not play any significant pathogenetic role in at least most mucocutaneous lesions where it is found. Whether it contributes to the maintenance of the lesion once the primary pathogen is eliminated cannot be answered. The predilection of CMV for anogenital ulcers has been clearly confirmed in our study. We believe that it is very probable that the cytomegalic inclusions reach the area as a consequence of the autoinoculation after shedding through the feces, urine, or even the semen in a herpes simplex–induced ulcer. It is well known that the colon, an organ with a special tropism for the virus, is frequently colonized.40,41 The possibility of CMV hematogeneously reaching the granulation tissue of anogenital ulcers or of a reinfection through anal coitus in homosexuals cannot be ruled out.

As our study shows, it is very important to search for and detect CMV because its presence frequently represents the first sign of CMV infection,28 or even the first expression of HIV infection.42 But apart from this, the detection of CMV has a high prognostic value because its presence in the skin and/or mucosa usually indicates a concomitant generalized CMV infection. This fact should encourage us to search for infection in other tissues (retina, blood, etc) and, if it is found, to start treatment as soon as possible. In summary, on the basis of our findings that CMV is usually associated with HSV and VZV infections, and is found unexpectedly in cutaneous abnormalities of known diagnosis (ie, bacillary angiomatosis) or even in apparently healthy skin, we believe that the CMV does not play any significant pathogenetic role in at least most cutaneous lesions in which it is found.

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Article Information

Accepted for publication December 26, 2000.

Preliminary results were presented as a poster at the 53rd Annual Meeting of the American Academy of Dermatology, New Orleans, La, February 1995.

The present study was presented as a poster at the Ninth Congress of the European Academy of Dermatology and Venereology, Geneva, Switzerland, October 2000.

Corresponding author: Esteban Daudén, MD, PhD, Department of Dermatology, Hospital de la Princesa, Autonoma University of Madrid, c/Diego de León, 62, 28006 Madrid, Spain (e-mail: edaudent@medynet.com).

References
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2.
Lopez-Elzaurdia  CFraga  JSols  MBurgos  ESanchez-Garcia  MGarcia-Diez  A Bacillary angiomatosis associated with cytomegalovirus infection in a patient with AIDS. Br J Dermatol. 1991;125175- 177Article
3.
Daudén  EPeñas  PFBuezo  GFFraga  JGarcía-Díez  A Reticular erythematous mucinosis associated with human immunodeficiency virus infection. Dermatology. 1995;191157- 160Article
4.
Penneys  NHicks  B Unusual cutaneous lesions associated with acquired immunodeficiency syndrome. J Am Acad Dermatol. 1985;13845- 852Article
5.
Bournerias  IBoisnic  SPatey  O  et al.  Unusual cutaneous cytomegalovirus involvement in patients with acquired immunodeficiency syndrome. Arch Dermatol. 1989;1251243- 1246Article
6.
Thiboutot  DBeckford  AMart  CSexton  MMaloney  M Cytomegalovirus diaper dermatitis. Arch Dermatol. 1991;127396- 398Article
7.
Smith  KSkelton  HJames  W  et al.  Concurrent epidermal involvement of cytomegalovirus and herpes simplex virus in two HIV infected patients. J Am Acad Dermatol. 1991;25500- 506Article
8.
Wade  TFinan  MStahr  BWhite  WTroy  J Self assessment. J Cutan Pathol. 1993;20515- 516Article
9.
Chiewchanvit  SThamprasert  KSiriunkgul  S Disseminated cutaneous cytomegalic inclusion disease resembling prurigo nodularis in a HIV-infected patient: a case report and literature review. J Med Assoc Thai. 1993;76581- 584
10.
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