Print version ISSN 0365-0596
An. Bras. Dermatol. vol.85 no.1 Rio de Janeiro Jan./Feb. 2010
Transepidermal elimination of parasites in Jorge Lobo's disease*
Mario F. R. MirandaI; Vivian S. da CostaII; Maraya de Jesus S. BittencourtIII; Arival C. de BritoIV
IAdjunct Professor of Dermatology, Grade IV, Federal University of Pará (UFPA). Head of the Dermatopathology Laboratory, Department of Dermatology, Health Sciences Institute, Federal University of Pará (UFPA), Belém, PA, Brazil
IIUndergraduate Medical Student, Health Sciences Institute, Federal University of Pará (UFPA), Belém, PA, Brazil. Participating in Project # 3CCS010403C
IIIDermatologist. Medical Residency in Dermatology completed at the Hospital of the Santa Casa de Misericórdia Foundation, Federal University of Pará (UFPA), Belém, PA, Brazil
IVDoctorate in Dermatology awarded by the Federal University of Pará (UFPA). Faculty, Federal University of Pará (UFPA). Professor of the Postgraduate Program in Tropical Diseases, Institute of Tropical Medicine, Federal University of Pará. Professor in the Postgraduate Program in Biology of Infectious and Parasitic Agents, Biological Sciences Institute, Federal University of Pará (UFPA), Belém, PA, Brazil
BACKGROUND: Few studies have focussed on the transepidermal elimination of parasites in Jorge Lobo's disease (lobomycosis).
OBJECTIVE: To identify the morphological features of the transepidermal elimination of parasites in lobomycosis.
METHODS: Sections were obtained from paraffin-embedded biopsy specimens of patients with lobomycosis and stained with hematoxylin-eosin for microscopic examination. Only the presence of parasites in epidermal structures was considered to constitute transepidermal elimination.
RESULTS: Forty biopsies from 37 patients were included in the study (31 males and 6 females). The mean age of patients was 51.03 years (range 29-80 years). Biopsies performed over a period of 37 years (1967-2003) were used, from which 511 sections were obtained (a mean of 12.77 sections per case; range 2-39 sections per case). Transepidermal elimination of parasites was found in 110/511 (21.52%) and was absent in 401/511 sections (78.48%) (p<0.0001). Features consistent with the phenomenon were found in 15/37 patients (40.5%) and were absent in 22/37 (59.5%) (p>0.05). Parasites in the epidermis were detected within hyperplastic infundibula, either connected in chains or as isolated units, associated or not with inflammatory cells.
CONCLUSION: Features consistent with transepidermal elimination of parasites were found in a statistically nonsignificant number of patients in the sample (p>0.05), suggesting that in Jorge Lobo's disease, this phenomenon invariably occurs through the infundibular epithelium. Future studies are required to evaluate the significance of this finding in the epidemiology of mycosis.
Key words: Lobomycosis; Jorge Lobo's disease; chronic granulomatous disease; mycoses; mycoses/pathology; skin.
Jorge Lobo's disease, also known as lobomycosis, keloidal blastomycosis and lacaziosis, among other names, is a deep skin infection caused by the Lacazia loboi (L. loboi) yeast. The disease is named after a Brazilian dermatologist, Jorge Lobo, who published a description of the first case in 1931.1 The majority of infected individuals are male forestry or farm workers living in the South American Amazon region. The mycosis has also been found in dolphins in river estuaries and on the Atlantic coast of Suriname, Florida, France (one human case probably acquired from an animal source) and in the Brazilian state of Santa Catarina.2-5 The precise inoculation mechanisms remain to be clarified; however, it is generally agreed that humans acquire the infection through implantation of the fungi into the skin following mechanical trauma.6,7 The skin lesions appear predominantly on the lower limbs and consist of keloidal nodules, tumors and verrucous plaques that occasionally become ulcerated. Extensive skin involvement due to lymphatic dissemination is rare. Mucosae and internal organs are not affected, even in generalized cases in which a hematogenous route of dissemination is suspected.
Histopathological findings in Jorge Lobo's disease6-10 tend to be fairly typical; therefore, diagnosis is straightforward. The findings consist of a granulomatous, generally diffuse infiltrate, rich in histiocytes, with a large number of yeast-like bodies arranged as single units or clustered together in chains within the cytoplasm of the multinucleated histiocytes. Lymphocytes and plasmocytes are rare. Asteroid bodies may occasionally be found. The granulomas tend to circumscribe the dermis, surrounded by delicate fibrous strands. Aggregates of large histiocytes of clear or eosinophilic, finely granular, xanthomatous cytoplasm may be found, with no parasites in their cytoplasm (pseudo-Gaucher cells). In the epidermis, there is a flattening of the interpapillary ridges or atrophy, and a narrow subepidermal Grenz zone is frequently found. However, acanthotic areas associated with spongiosis and collections of neutrophils containing varying quantities of parasites may be found, suggesting transepidermal elimination of parasites. In Jorge Lobo's disease, transepidermal elimination of parasites can also be confirmed by direct mycological examination using starch-covered adhesive tape and a clarifying solution of 10% potassium hydroxide in 40% dimethyl-sulfoxide, for example, in which parasites are easily identified.11 The objective of this study was to evaluate morphological features associated with the transepidermal elimination of parasites in lobomycosis.
MATERIAL AND METHODS
Material obtained from paraffin-embedded biopsy specimens of cases diagnosed as lobomycosis and available in the archives of the dermatopathology laboratory of the Dermatology Department, Health Sciences Institute, Federal University of Pará was used in this study. New sections were cut from each paraffin block, routinely processed and then stained using hematoxylin-eosin (HE). The number of sections obtained per block varied according to the limitations imposed by the state of conservation of the sample. Clusters of parasites mixed with serous secretion and/or inflammatory cells distributed over the stratum corneum were not interpreted microscopically as constituting transepidermal elimination of parasites, only those whose presence in the epidermal structures was indisputable. For some of the cases included in the study sample, only well preserved slides were available, since the respective paraffin blocks had already been completely depleted in previous investigations. Statistical analysis, when pertinent, was performed using the Bioestat software program, version 5.0.
A total of 40 biopsies performed over a period of 37 years (1967-2003) were included in the study. The biopsy specimens had been obtained from 37 patients (31 men and 6 women) with a mean age of 51.03 years (range 29-80 years). A total of 511 sections were obtained from these specimens and subsequently analyzed (a mean of 12.77 sections per case, range 2-39 sections per case). Aspects consistent with the transepidermal elimination of parasites were found in 110/511 of the sections examined (21.52%) but were absent in 401/511 (78.48%). This difference was highly significant (p < 0.0001). nevertheless, with respect to the patients (n=37), aspects consistent with the transepidermal elimination of parasites were found in 15 (40.5%), while in the remaining 22 (59.5%), no indications were found (p>0.05). Parasites in the epidermis were invariably detected in hyperplastic infundibula, arranged in clusters, forming chains or as single units (Figure 1A). There was an associated, predominantly neutrophilic inflammatory infiltrate (sometimes in the form of microabscesses) and/or of histiocytes and lymphocytes (Figure 1B and 1C). When present in the stratum corneum and other infundibular epithelial structures, the parasites were found both in crusts (Figure 1D) and dissociated from inflammatory cells (Figure 2A and 2B).
Transepidermal elimination, originally described by Mehregan in 1970,12 constitutes a process by which the skin releases inflammatory cells, tissue components, foreign material and microorganisms. It represents an essential feature of the group of so-called perforating dermatoses such as Kyrle's disease, reactive perforating collagenosis, elastosis perforans serpiginosa, perforating folliculitis and conditions resulting from chronic kidney failure and diabetes mellitus. 13,14 Transepidermal elimination may be found sporadically in conditions as diverse as non-infectious granulomas, lichenoid skin reactions, extracellular deposition of substances, neoplasias and infections. With respect to the latter group, a growing number of microorganisms are being cited within the context of the transepidermal elimination of parasites, including fungi, bacteria, protozoa and even chlamydiae. 15 Parasites clustered in a hyperplastic epidermis and associated with inflammatory cells, particularly neutrophiles forming microabscesses and/or histiocytes, suggesting transepidermal elimination of parasites, are predominantly found in granulomatous and suppurative mycotic infections such as chromomycosis and paracoccidioidomycosis,16,17 the most prevalent forms of deep mycoses in Brazil. Nevertheless, this condition does not correspond exactly to the microscopic findings in lobomycosis, which are characterized by an inflammatory, granulomatous infiltrate rich in histiocytes in which neutrophils are only seen in the superficial dermis of ulcerated lesions.6,7 The occurrence of the transepidermal elimination of parasites in lobomycosis was first reported by Gadelha and Bandeira in 1983,10. Subsequent communications followed this initial report.6-8 Pradinaud referred to the presence of clinically observable "tiny black dots" on the surface of lesions in lobomycosis, similar to those seen in chromomycosis, which would correspond to parasites being eliminated together with necrotic residue.8 To the best of our knowledge, no detailed study had yet been carried out on the microscopic characteristics of the transepidermal elimination of parasites in lobomycosis.
In the present study, the authors were able to demonstrate at least three features associated with the phenomenon of transepidermal elimination of parasites in lobomycosis: 1) the presence of an exudative reaction of neutrophils, histiocytes and/or lymphocytes together with parasites in the epidermis; 2) in other cases, only parasitic bodies were found; and 3) in both situations, the alterations were processed in hyperplastic infundibula, at times with a pseudocarcinomatous pattern, avoiding the inter-infundibular epidermis. This last feature is in accordance with the current concept that pseudocarcinomatous hyperplasia represents a proliferation of the infundibular epithelium and/or eccrine duct that is found in any chronic suppurative infundibulitis such as halogenoderma, fungal infections and atypical mycobacterioses. 18 In conclusion, histopathological features consistent with the transepidermal elimination of parasites, although found in a statistically nonsignificant number of cases in this sample, suggest that in lobomycosis this phenomenon invariably occurs through the infundibular epithelium. Future studies are required to evaluate the possible importance of this finding in the epidemiology of this mycosis.
1. Lobo J. Um caso de blastomicose produzido por uma espécie nova encontrada em Recife. Rev Med Pernamb. 1931;1:763-75. [ Links ]
2. De Vries GA, Laarman JJ. A case of Lobo's disease in the dolphin Sotalia guianensis. Aquatic Mammals. 1973;1:26-33. [ Links ]
3. Migaki G, Valério MG, Irvine B, Gardner FM. Lobo's disease in am Atlantic bottle-nosed dolphin. J Am Vet Med Assoc. 1971;159:578-82. [ Links ]
4. Symmers WSTC. A possible case of Lobo's disease acquired in Europe from a bottle-nosed dolphin (Tursiops truncatus). Bull Soc Pathol Exot Filiales 1983;76:777-84. [ Links ]
5. Lopes PCS, Paula GS, Both MC, Xavier FM, Scaramello AC. First case of lobomycosis in a bottle-nose dolphin from Southern Brazil. Marine Mammal Sci. 1993;9:329-31. [ Links ]
6. Brito AC. Lobomycosis. In: Tyring SK, Lupi O, Hengge UR, eds. Tropical dermatology. São Paulo: Elsevier; 2006. p.207-9. [ Links ]
7. Brito AC, Quaresma JAS. Lacaziose (doença de Jorge Lobo): revisão e atualização. An Bras Dermatol. 2007;82:461-74. [ Links ]
8. Pradinaud R, Talhari S. Lobomycose. Encycl Méd Chir (Elsevier, Paris): Maladies infectieuses; 1996. p.1-6. [ Links ]
9. Bhawan J, Bain RW, Purtilo DT, Gomez N, Dewan C, Whelan CF, et al. Lobomycosis: an electronmicroscopic, histochemical and immunologic study. J Cutan Pathol. 1976;3:5-16. [ Links ]
10. Gadelha AR, Bandeira V. Micoses profundas. In: da Silva IM, ed. Dermatopatologia. Rio de Janeiro: Atheneu; 1983. p.125-34. [ Links ]
11. Miranda MFR, Silva AJG. Vinyl adhesive tape also effective for direct microscopy diagnosis of chromomycosis, lobomycosis, and paracoccidioidomycosis. Diagn Microbiol Infect Dis. 2005;52:39-43. [ Links ]
12. Mehregan AH. Transepidermal elimination. Curr Probl Dermatol. 1970; 3:124-47. [ Links ]
13. Woo TY, Rasmussen JE. Disorders of transepidermal elimination. Part 1. Int J Dermatol. 1985;24:267-79. [ Links ]
14. Woo TY, Rasmussen JE. Disorders of transepidermal elimination. Part 2. Int J Dermatol. 1985;24:337-48. [ Links ]
15. Ramdial PK, Kharsany AB, Reddy R, Chetty R. Transepidermal elimination of cutaneous vulval granuloma inguinale. J Cutan Pathol. 2000;27:493-9. [ Links ]
16. Uribe F, Zuluaga AI, León W, Restrepo A. Histopathology of chromoblastomycosis. Mycopathologia. 1989;105:1-6. [ Links ]
17. Uribe F, Zuluaga AI, León W, Restrepo A. Histopathology of cutanoeus and mucosal lesions in human paracoccidioidomycosis. Rev Inst Med Trop Sao Paulo. 1987; 29:90-6. [ Links ]
18. Ackerman AB, Chongchitnant N, Sanchez J, Guo Y, Bennin B, Reichel M, et al. Histologic diagnosis of inflammatory skin diseases. An algorithmic method based on pattern analysis. 2 ed. Baltimore: Williams & Wilkins; 1997. p.79-80. [ Links ]
Mailing Address: Recebido em 22.04.2009. * Study carried out at the Department of Dermatology, Health Sciences Institute, Federal University of Pará (UFPA), Belém, Pará, Brazil as part of Project # 3CCS010403C: "Basic and Professional Integration in Medical Training", coordinated by Réia Sílvia Lemos, Professor, PhD. Belém, PA, Brazil.
Mario Fernando Ribeiro de Miranda
Av. Nazaré, 1.033 / 701 - Nazaré
66035-170 Belém - PA
Aprovado pelo Conselho Consultivo e aceito para publicação em 07.11.09.
Conflict of interest: None.
Financial support: Support from Project 3CCS010403C of the Health Sciences Institute (formerly the Health Sciences Center), Federal University of Pará (UFPA), exclusively in the form of reimbursement of material used to perform histological exams.
Recebido em 22.04.2009.
* Study carried out at the Department of Dermatology, Health Sciences Institute, Federal University of Pará (UFPA), Belém, Pará, Brazil as part of Project # 3CCS010403C: "Basic and Professional Integration in Medical Training", coordinated by Réia Sílvia Lemos, Professor, PhD. Belém, PA, Brazil.