Sporotrichoid leishmaniasis: a cross-sectional clinical, epidemiological and laboratory study in Rio de Janeiro State, Brazil

Livia Martins Veloso de Carvalho Maria Inês Fernandes Pimentel Fátima Conceição-Silva Érica de Camargo Ferreira e Vasconcellos Cláudia Maria Valete-Rosalino Marcelo Rosandiski Lyra Mariza de Matos Salgueiro Maurício Naoto Saheki Maria de Fátima Madeira Eliame Mouta-Confort Liliane de Fátima Antonio Aline Fagundes da Silva Leonardo Pereira Quintella Sandro Javier Bedoya-Pacheco Armando de Oliveira Schubach About the authors

ABSTRACT

Background

Atypical presentations of cutaneous leishmaniasis include sporotrichoid leishmaniasis (SL), which is clinically described as a primary ulcer combined with lymphangitis and nodules and/or ulcerated lesions along its pathway.

Aims

To assess the differences between patients with sporotrichoid leishmaniasis and typical cutaneous leishmaniasis (CL).

Methods

From January 2004 to December 2010, 23 cases of SL (4.7%) were detected among 494 CL patients diagnosed at a reference center for the disease in Rio de Janeiro State, Brazil. These 23 cases were compared with the remaining 471 patients presenting CL.

Results

SL predominated in female patients (60.9%, p = 0.024), with older age (p = 0.032) and with lesions in upper limbs (52.2%, p = 0.028). CL affected more men (64.5%), at younger age, and with a higher number of lesions exclusively in lower limbs (34.8%).

Conclusions

Differences in clinical and epidemiological presentation were found between SL patients as compared to CL ones, in a region with a known predominance of Leishmania (Viannia) braziliensis. The results are similar to the features of most of the sporotrichosis patients as described in literature, making the differential diagnosis between ATL and sporotrichosis more important in overlapping areas for both diseases, like in Rio de Janeiro State.

Sporotrichoid leishmaniasis; American tegumentary leishmaniasis; Cutaneous leishmaniasis; Sporotrichosis

INTRODUCTION

The most characteristic presentation of cutaneous leishmaniasis is: one or a few painless ulcers with infiltrated borders in exposed body areas11. Brasil. Ministério da Saúde. Manual de vigilância da leishmaniose Tegumentar Americana. 2ª ed. Brasília: Ministério da Saúde, 2010.. However, several other forms are also described22. Bari AU, Rahman SB. Many faces of cutaneous leishmaniasis. Indian J Dermatol Venereol Leprol. 2008;74:23-7.,33. Guerra JA, Talhari S, Paes MG, Garrido M, Talhari JM. Aspectos clínicos e diagnósticos da leishmaniose tegumentar americana em militares simultaneamente expostos à infecção na Amazônia. Rev Soc Bras Med Trop. 2003;36:587-90.. This diversity could be related to the host immune response, skin area, and species of Leishmania44. Azeredo-Coutinho RB, Conceição-Silva F, Schubach A, Cupolillo E, Quintella LP, Madeira MF, et al. First report of diffuse cutaneous leishmaniasis and Leishmania amazonensis infection in Rio de Janeiro State, Brazil. Trans R Soc Trop Med Hyg. 2007;101:735-7.,55. Iftikhar N, Bari I, Ejaz A. Rare variants of cutaneous leishmaniasis: whitlow, paronychia and sporotrichoid. Int J Dermatol. 2003;42:807-9.. In Rio de Janeiro State, Leishmania (Viannia) braziliensis is the almost exclusively prevalent species44. Azeredo-Coutinho RB, Conceição-Silva F, Schubach A, Cupolillo E, Quintella LP, Madeira MF, et al. First report of diffuse cutaneous leishmaniasis and Leishmania amazonensis infection in Rio de Janeiro State, Brazil. Trans R Soc Trop Med Hyg. 2007;101:735-7., and different genotypes were not associated with the clinical variability66. Baptista C, Schubach AO, Madeira MF, Leal CA, Pires MQ, Oliveira FS, et al. Leishmania (Viannia) braziliensis genotypes identified in lesions of patients with atypical or typical manifestations of tegumentary leishmaniasis: evaluation by two molecular markers. Exp Parasitol. 2009;42:317-2..

Sporotrichoid leishmaniasis (SL) presents itself as an ulcer, lymphangitis, and nodules or ulcerated lesions along its pathway; it resembles the typical presentation of sporotrichosis22. Bari AU, Rahman SB. Many faces of cutaneous leishmaniasis. Indian J Dermatol Venereol Leprol. 2008;74:23-7.,55. Iftikhar N, Bari I, Ejaz A. Rare variants of cutaneous leishmaniasis: whitlow, paronychia and sporotrichoid. Int J Dermatol. 2003;42:807-9.,77. López-Escobar M, Drake-Monfort M, Salesa-Gutiérrez de Rozas R, Hermana-Ramírez S. Leishmaniose cutanea esporotricoide. Actas Dermosifiliogr. 2007;98:444-5.. This study aimed to access the differences between SL and typical cutaneous leishmaniasis.

MATERIALS AND METHODS

Cross-sectional study with comparison of epidemiological and clinical parameters, laboratory findings at the time of diagnosis, as well as post-treatment follow-up, between sporotrichoid forms of leishmaniasis (SL) and typical forms of cutaneous leishmaniasis (CL).

We studied patients diagnosed with American tegumentary leishmaniasis (ATL) at a reference center for the disease in Rio de Janeiro, Brazil, between January 2004 and December 2010.

Patients who were included followed systematic research protocols, including epidemiological history, clinical examination and laboratory tests. Patients with concomitant involvement of skin and mucous membranes of the upper aerodigestive tract and those with diffuse anergic leishmaniasis were excluded.

Patients were evaluated by experienced dermatologists in the diagnosis and treatment of cutaneous leishmaniasis. Clinical diagnosis of SL was performed when there were ulcerated lesions accompanied by lymphangitis and gummas/nodes along the lymphatic path. Typical leishmaniasis lesions (CL) were not accompanied by this lymphatic pattern, and were generally comprised of ulcerated lesions with infiltrated borders, in most cases one lesion or a few; occasionally, an infiltrated plaque or, more rarely, verrucous lesions. Patients with ten or more lesions were also exceptions. Cases presenting with short lymphatic path around the lesion without gummas or nodules were not clinically classified as SL.

Diagnosis of leishmaniasis was confirmed by visualization and/or isolation of parasites by at least one of the following methods: Leishmania spp culture in NNN+ Schneider media88. Almeida AB, Souza VR, Sorte EC, Figueiredo FB, Paula DA, Pimentel MF, et al. Use of parasitological culture to detect Leishmania (Leishmania) chagasi in naturally infected dogs. Vector Borne Zoonotic Dis. 2011;11:1555-60., or conventional histopathology and/or immunohistochemical examination99. Quintella L, Cuzzi T, Madeira M, Okamoto T, Schubach AO. Immunoperoxidase technique using an anti-Leishmania (L.) chagasi hyperimmune serum in the diagnosis of culture-confirmed American tegumentary leishmaniasis. Rev Inst Med Trop Sao Paulo. 2009;51:83-6. of a skin lesion fragment collected through a biopsy procedure. Immunological tests included Montenegro skin test (MST)1010. Fagundes A, Marzochi MC, Perez M, Schubach A, Ferreira A, Silva JP, et al. Skin reactivity to thimerosal and phenol-preserved Montenegro antigen in Brazil. Acta Trop. 2007;101:25-30. and serological tests such as the indirect immunofluorescence assay (IFA), and/or the enzyme-linked immunosorbent assay (ELISA)1111. Barroso-Freitas AP, Passos SR, Mouta-Confort E, Madeira MF, Schubach AO, Santos GP, et al. Accuracy of an ELISA and indirect immunofluorescence for the laboratory diagnosis of American tegumentary leishmaniasis. Trans R Soc Trop Med Hyg. 2009;103:383-9..

The analysis considered clinical characteristics (gender, age, time of disease progression before diagnosis, affected area of the body, and response to treatment - cure or relapse of the disease), besides the results to the diagnostic exams listed above.

A database was constructed (SPSS16 software for Windows - SPSS Inc, Chicago, Illinois, USA), and kept under the responsibility of the authors, based on the records of the patients. Clinical features and the results of the laboratory exams of SL patients were compared with the same parameters of CL patients treated in the same period at this reference center. Measurements of central tendency and dispersion for quantitative variables (age in years, MST in millimeters, time of disease progression before diagnosis in months) were calculated and subsequently these parameters were transformed into categorical variables as follows:

Age: < 25 years, 25 to 44 years, > 44 years.

MST in millimeters: negative (0 to 4 mm); and positive (≥ 5 mm).

Time of disease progression before diagnosis: ≤ 3 months; and > 3 months.

Affected area of the body: lesions exclusively located in upper limbs; exclusively located in lower limbs; and in other or multiple locations.

The variables were analyzed using the Pearson Chi Squared and Fisher’s exact tests, as well as by logistic regression (SPSS16.0).

The species of Leishmania was determined in SL patients, whenever possible.

Missing data were not considered in the analysis, but they were made explicit in Table 1.

Table 1
- Clinical-epidemiological and laboratory characteristics, besides post-treatment follow-up- of patients with sporotrichoid leishmaniasis (SL) and typical cutaneous leishmaniasis (CL), 2004 - 2010

Ethical considerations

Patients signed an informed consent at diagnosis. This study is a subproject of a larger research project approved by the Institutional Ethics in Research Committee under the Nº 0016.0.009-02, and it was re-submitted to the same Board and revalidated under the Nº 0056.0.009.000-10.

RESULTS

During the analyzed period, among 579 patients with ATL, 84 patients had mucosal involvement and one patient had diffuse anergic leishmaniasis and were therefore excluded, since they had a particular immunological behaviour; 494 patients with cutaneous leishmaniasis were studied, among them 23 (4.7%) presented SL. Figure 1 shows lesions of patients with SL in upper limbs (upside) and typical CL lesions in lower limbs (bottom).

Figure 1
- Sporotrichoid leishmaniasis in upper limbs (upside) and typical cutaneous leishmaniasis in lower limbs (bottom)

Twenty patients (86.9%) with SL had positive cultures for Leishmania spp, and 18 were characterized as L. (V.) braziliensis. From the three remaining patients, one had parasitologically confirmed SL through visualization of amastigotes in histopathology; the other two had SL diagnosis made through a compatible clinical and epidemiological history, aside from positive immunological tests (MST, IFA and/or ELISA), as well as a good response to treatment with meglumine antimoniate.

The results of the clinical and epidemiological features, laboratory tests performed for diagnosis, and follow-up after treatment for both groups of patients (SL and CL) are presented in Table 1.

DISCUSSION

There were significant differences when clinical and epidemiological characteristics of patients with SL and CL were compared, with more females and older age in SL. Patients with CL were predominantly males, in agreement with data from the Ministry of Health of Brazil, which reported 74% of cases of cutaneous leishmaniasis in men11. Brasil. Ministério da Saúde. Manual de vigilância da leishmaniose Tegumentar Americana. 2ª ed. Brasília: Ministério da Saúde, 2010.. Although in both groups the lesions were mainly detected in exposed areas, we observed a predominance of lesions in the upper limbs in the SL group, as compared to the CL group, which presented a higher number of lower limb lesions, as classically described in the literature33. Guerra JA, Talhari S, Paes MG, Garrido M, Talhari JM. Aspectos clínicos e diagnósticos da leishmaniose tegumentar americana em militares simultaneamente expostos à infecção na Amazônia. Rev Soc Bras Med Trop. 2003;36:587-90.,1212. Furtado T. Critérios para o diagnóstico da leishmaniose tegumentar americana. An Bras Dermatol. 1980;55:81-6.. Interestingly, those features were are also present in sporotrichosis in Rio de Janeiro, with a predominance of older females and lesions in the upper limbs1313. Barros MB, Paes RA, Schubach AO. Sporothrix schenckii and sporotrichosis. Clin Microbiol Rev. 2011;24:633-54.. They are different pathogens showing similar clinical-epidemiological characteristics. Despite diverse explanations for their occurrence, in the case of sporotrichosis transmitted by cats, older women are more likely to care for and feed infected animals, which could also explain why lesions are presented mostly in the hands and forearms/arms due to the manipulation of cats1313. Barros MB, Paes RA, Schubach AO. Sporothrix schenckii and sporotrichosis. Clin Microbiol Rev. 2011;24:633-54.. Leishmaniasis, however, is transmitted by sand flies and this explanation does not elucidate the results obtained in SL.

We have generally observed that SL patients behaved similarly to CL patients in terms of laboratory exams, and did not present different post-treatment prognosis either.

MST is a tool for evaluating the delayed hypersensitivity cell response to Leishmania antigens inoculated intradermally, and it is widely used for diagnosis and in epidemiological surveys1010. Fagundes A, Marzochi MC, Perez M, Schubach A, Ferreira A, Silva JP, et al. Skin reactivity to thimerosal and phenol-preserved Montenegro antigen in Brazil. Acta Trop. 2007;101:25-30.,1414. Cuba-Cuba CA, Marsden PD, Barretto AC, Jones TC, Richards F. The use of different concentrations of leishmanial antigen in skin testing to evaluate delayed hypersensitivity in American cutaneous leishmaniasis. Rev Soc Bras Med Trop. 1985;18:231-6.. Despite the fact that it does not constitute a confirmatory parasitological test, it is usually the only available diagnostic test for cutaneous leishmaniasis in most primary health care facilities in Brazil. The test may be negative in the first four to six weeks from the onset of skin lesions11. Brasil. Ministério da Saúde. Manual de vigilância da leishmaniose Tegumentar Americana. 2ª ed. Brasília: Ministério da Saúde, 2010.. Additionally, positivity to MST is independent of gender or age of patients1515. Manzur A, Bari A. Sensitivity of leishmanin skin test in patients of acute cutaneous leishmaniasis. Dermatol Online J. 2006;12:2., and it is reported to have a high sensitivity: positivity close to 100% in confirmed ATL cases1616. Sadeghian G, Momeni A, Siadat AH, Yousefi P. Evaluation of leishmanin skin test and its relationship with the clinical form and duration of cutaneous leishmaniasis. Dermatol Online J. 2006;12:3.. However, in individuals who do not have active leishmaniasis, lesions or scars suggestive of prior disease, or in those who reside in non-endemic areas for the disease, its positivity may vary between 20 and 30%11. Brasil. Ministério da Saúde. Manual de vigilância da leishmaniose Tegumentar Americana. 2ª ed. Brasília: Ministério da Saúde, 2010.,1010. Fagundes A, Marzochi MC, Perez M, Schubach A, Ferreira A, Silva JP, et al. Skin reactivity to thimerosal and phenol-preserved Montenegro antigen in Brazil. Acta Trop. 2007;101:25-30.. The occurrence of positive MST in confirmed cases of sporotrichosis was previously detected in Rio de Janeiro1717. De Lima Barros MB, Schubach A, Francesconi-do-Valle AC, Gutierrez-Galhardo MC, Schubach TM, Conceição-Silva F, et al. Positive Montenegro skin test among patients with sporotrichosis in Rio de Janeiro. Acta Trop. 2005;93:41-7.. Since endemic areas for sporotrichosis and leishmaniasis overlap extensively in Rio de Janeiro State, the presence of both agents could partly explain the positivity of MST in patients who do not have leishmaniasis, adding some difficulty to the differential diagnosis. However, in our study, the strong reactions found in almost all the patients with SL lead us to suggest that this test can be valuable in conditions of scarcity of exams for the parasitological diagnosis of leishmaniasis. There was a trend to higher values of MST in patients with SL than in patients with CL.

In patients with CL, there are also generally low to moderate levels of specific antibodies detected by both IFA and ELISA, when compared to the levels found in patients with the mucosal forms of the disease. However, there are individual variations1111. Barroso-Freitas AP, Passos SR, Mouta-Confort E, Madeira MF, Schubach AO, Santos GP, et al. Accuracy of an ELISA and indirect immunofluorescence for the laboratory diagnosis of American tegumentary leishmaniasis. Trans R Soc Trop Med Hyg. 2009;103:383-9.,1818. Cataldo JI, Mello FC, Mouta-Confort E, Madeira MF, Schubach AO, Genestra MS, et al. Immunoenzymatic assay for the diagnosis of American tegumentary leishmaniasis using soluble and membrane-enriched fractions from infectious Leishmania (Viannia) braziliensis. J Clin Lab Anal. 2010;24:289-94.. In our study, both groups (SL and CL) showed moderate to high percentages of positivity in leishmaniasis serology by those methods.

Regarding parasite detection by culture of fragments of lesions collected through biopsy, considered as the gold standard for ATL diagnosis, the majority of our patients were diagnosed based on the parasite isolation (85% in both SL and CL groups). This positivity is higher than usually described1212. Furtado T. Critérios para o diagnóstico da leishmaniose tegumentar americana. An Bras Dermatol. 1980;55:81-6.,1919. Romero GA, Guerra MV, Paes MG, Macedo VO. Comparison of cutaneous leishmaniasis due to Leishmania (Viannia) braziliensis and L. (V.) guyanensis in Brazil: therapeutic response to meglumine antimoniate. Am J Trop Med Hyg. 2001;65:456-65.. In addition, both studied groups showed moderate sensitivity of parasite detection in histopathology. Sensitivity indices of histopathology in the literature show wide variation11. Brasil. Ministério da Saúde. Manual de vigilância da leishmaniose Tegumentar Americana. 2ª ed. Brasília: Ministério da Saúde, 2010.,1212. Furtado T. Critérios para o diagnóstico da leishmaniose tegumentar americana. An Bras Dermatol. 1980;55:81-6.; however, immunohistochemistry showed higher sensitivities than hematoxylin-eosin staining for the parasite detection99. Quintella L, Cuzzi T, Madeira M, Okamoto T, Schubach AO. Immunoperoxidase technique using an anti-Leishmania (L.) chagasi hyperimmune serum in the diagnosis of culture-confirmed American tegumentary leishmaniasis. Rev Inst Med Trop Sao Paulo. 2009;51:83-6..

The analyzed patients in the present study came from a geographical area with a large predominance of Leishmania (V.) braziliensis, like most of Brazilian regions. This can be considered a limitation of the study. In the Amazon region, for example, the coexistence of different species of Leishmania could lead to other findings. Additional studies to verify clinical and epidemiological features of SL patients under conditions of greater diversity of the parasite population can add information to the SL characterization. However, as SL is reported in other countries2020. Cozzani E, Satta R, Fausti V, Cottoni F, Parodi A. Cutaneous sporotrichoid leishmaniasis resistant to pentavalent antimonial therapy: complete resolution with itraconazole. Clin Exp Dermatol. 2011;36:49-51.

21. Masmoudi A, Ayadi N, Khabir A, Bouzid L, Bouassida S, Meziou T J, et al. Forme sporotrichoide de leishmaniose cutanée em Tunisie: étude clinique et histologique. Ann Dermatol Venereol. 2008;135:63-7.
-2222. Talari S A, Talaei R, Shajari G, Vakili Z, Taghaviardakani A. Childhood cutaneous leishmaniasis: report of 117 cases from Iran. Korean J Parasitol. 2006;44:355-60. where L. (V.) braziliensis has not been reported, it seems that this clinical presentation is mostly due to the characteristics of the patients. In addition, as sporotrichosis has been described in different regions all over the world2323. de Oliveira MM, Veríssimo C, Sabino R, Aranha J, Zancopé-Oliveira RM, Sampaio P, et al. First autochthone case of sporotrichosis by Sporothrix globosa in Portugal. Diagn Microbiol Infect Dis. 2014;78:388-90.

24. Mata-Essayag S, Delgado A, Colella MT, Landaeta-Nezer ME, Rosello A, Perez de Salazar C, et al. Epidemiology of sporotrichosis in Venezuela. Int J Dermatol. 2013;52:974-80.

25. Subedi S, Kidd SE, Baird RW, Coatsworth N, Ralph AP. Sporotrichosis from the northern territory of Australia. Am J Trop Med Hyg. 2014;91:1263-8.
-2626. Tobin EH, Jih WW. Sporotrichoid lymphocutaneous infections: etiology, diagnosis and therapy. Am Fam Physician. 2001;63:326-32., differential diagnosis may become a real challenge elsewhere.

The results of the present study suggest that SL and CL patients have different characteristics, and they reflect mainly clinical and epidemiological variations between the groups. Since these differences could be produced by distinct immunological profiles, studies are now been performed in order to clarify in situ immunological distinctions between SL and CL.

ACKNOWLEDGEMENTS

The authors would like to thank the Instituto Nacional de Infectologia/Fundação Oswaldo Cruz; CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico); CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior); PROEP-CNPq (402557/2011-5) and FAPERJ (Fundação Carlos Chagas Filho de Amparo à Pesquisa no Estado do Rio de Janeiro, process Nº E26/111.230/2014) for their financial support. The funders had no role in the study design, data collection and analysis, decision to publish or preparing the manuscript.

REFERENCES

  • 1
    Brasil. Ministério da Saúde. Manual de vigilância da leishmaniose Tegumentar Americana. 2ª ed. Brasília: Ministério da Saúde, 2010.
  • 2
    Bari AU, Rahman SB. Many faces of cutaneous leishmaniasis. Indian J Dermatol Venereol Leprol. 2008;74:23-7.
  • 3
    Guerra JA, Talhari S, Paes MG, Garrido M, Talhari JM. Aspectos clínicos e diagnósticos da leishmaniose tegumentar americana em militares simultaneamente expostos à infecção na Amazônia. Rev Soc Bras Med Trop. 2003;36:587-90.
  • 4
    Azeredo-Coutinho RB, Conceição-Silva F, Schubach A, Cupolillo E, Quintella LP, Madeira MF, et al. First report of diffuse cutaneous leishmaniasis and Leishmania amazonensis infection in Rio de Janeiro State, Brazil. Trans R Soc Trop Med Hyg. 2007;101:735-7.
  • 5
    Iftikhar N, Bari I, Ejaz A. Rare variants of cutaneous leishmaniasis: whitlow, paronychia and sporotrichoid. Int J Dermatol. 2003;42:807-9.
  • 6
    Baptista C, Schubach AO, Madeira MF, Leal CA, Pires MQ, Oliveira FS, et al. Leishmania (Viannia) braziliensis genotypes identified in lesions of patients with atypical or typical manifestations of tegumentary leishmaniasis: evaluation by two molecular markers. Exp Parasitol. 2009;42:317-2.
  • 7
    López-Escobar M, Drake-Monfort M, Salesa-Gutiérrez de Rozas R, Hermana-Ramírez S. Leishmaniose cutanea esporotricoide. Actas Dermosifiliogr. 2007;98:444-5.
  • 8
    Almeida AB, Souza VR, Sorte EC, Figueiredo FB, Paula DA, Pimentel MF, et al. Use of parasitological culture to detect Leishmania (Leishmania) chagasi in naturally infected dogs. Vector Borne Zoonotic Dis. 2011;11:1555-60.
  • 9
    Quintella L, Cuzzi T, Madeira M, Okamoto T, Schubach AO. Immunoperoxidase technique using an anti-Leishmania (L.) chagasi hyperimmune serum in the diagnosis of culture-confirmed American tegumentary leishmaniasis. Rev Inst Med Trop Sao Paulo. 2009;51:83-6.
  • 10
    Fagundes A, Marzochi MC, Perez M, Schubach A, Ferreira A, Silva JP, et al. Skin reactivity to thimerosal and phenol-preserved Montenegro antigen in Brazil. Acta Trop. 2007;101:25-30.
  • 11
    Barroso-Freitas AP, Passos SR, Mouta-Confort E, Madeira MF, Schubach AO, Santos GP, et al. Accuracy of an ELISA and indirect immunofluorescence for the laboratory diagnosis of American tegumentary leishmaniasis. Trans R Soc Trop Med Hyg. 2009;103:383-9.
  • 12
    Furtado T. Critérios para o diagnóstico da leishmaniose tegumentar americana. An Bras Dermatol. 1980;55:81-6.
  • 13
    Barros MB, Paes RA, Schubach AO. Sporothrix schenckii and sporotrichosis. Clin Microbiol Rev. 2011;24:633-54.
  • 14
    Cuba-Cuba CA, Marsden PD, Barretto AC, Jones TC, Richards F. The use of different concentrations of leishmanial antigen in skin testing to evaluate delayed hypersensitivity in American cutaneous leishmaniasis. Rev Soc Bras Med Trop. 1985;18:231-6.
  • 15
    Manzur A, Bari A. Sensitivity of leishmanin skin test in patients of acute cutaneous leishmaniasis. Dermatol Online J. 2006;12:2.
  • 16
    Sadeghian G, Momeni A, Siadat AH, Yousefi P. Evaluation of leishmanin skin test and its relationship with the clinical form and duration of cutaneous leishmaniasis. Dermatol Online J. 2006;12:3.
  • 17
    De Lima Barros MB, Schubach A, Francesconi-do-Valle AC, Gutierrez-Galhardo MC, Schubach TM, Conceição-Silva F, et al. Positive Montenegro skin test among patients with sporotrichosis in Rio de Janeiro. Acta Trop. 2005;93:41-7.
  • 18
    Cataldo JI, Mello FC, Mouta-Confort E, Madeira MF, Schubach AO, Genestra MS, et al. Immunoenzymatic assay for the diagnosis of American tegumentary leishmaniasis using soluble and membrane-enriched fractions from infectious Leishmania (Viannia) braziliensis J Clin Lab Anal. 2010;24:289-94.
  • 19
    Romero GA, Guerra MV, Paes MG, Macedo VO. Comparison of cutaneous leishmaniasis due to Leishmania (Viannia) braziliensis and L. (V.) guyanensis in Brazil: therapeutic response to meglumine antimoniate. Am J Trop Med Hyg. 2001;65:456-65.
  • 20
    Cozzani E, Satta R, Fausti V, Cottoni F, Parodi A. Cutaneous sporotrichoid leishmaniasis resistant to pentavalent antimonial therapy: complete resolution with itraconazole. Clin Exp Dermatol. 2011;36:49-51.
  • 21
    Masmoudi A, Ayadi N, Khabir A, Bouzid L, Bouassida S, Meziou T J, et al. Forme sporotrichoide de leishmaniose cutanée em Tunisie: étude clinique et histologique. Ann Dermatol Venereol. 2008;135:63-7.
  • 22
    Talari S A, Talaei R, Shajari G, Vakili Z, Taghaviardakani A. Childhood cutaneous leishmaniasis: report of 117 cases from Iran. Korean J Parasitol. 2006;44:355-60.
  • 23
    de Oliveira MM, Veríssimo C, Sabino R, Aranha J, Zancopé-Oliveira RM, Sampaio P, et al. First autochthone case of sporotrichosis by Sporothrix globosa in Portugal. Diagn Microbiol Infect Dis. 2014;78:388-90.
  • 24
    Mata-Essayag S, Delgado A, Colella MT, Landaeta-Nezer ME, Rosello A, Perez de Salazar C, et al. Epidemiology of sporotrichosis in Venezuela. Int J Dermatol. 2013;52:974-80.
  • 25
    Subedi S, Kidd SE, Baird RW, Coatsworth N, Ralph AP. Sporotrichosis from the northern territory of Australia. Am J Trop Med Hyg. 2014;91:1263-8.
  • 26
    Tobin EH, Jih WW. Sporotrichoid lymphocutaneous infections: etiology, diagnosis and therapy. Am Fam Physician. 2001;63:326-32.

Publication Dates

  • Publication in this collection
    2017

History

  • Received
    18 Aug 2016
  • Accepted
    22 Feb 2017
Instituto de Medicina Tropical de São Paulo Av. Dr. Enéas de Carvalho Aguiar, 470, 05403-000 - São Paulo - SP - Brazil, Tel. +55 11 3061-7005 - São Paulo - SP - Brazil
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