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Table of Contents
CASE REPORT
Year : 2021  |  Volume : 14  |  Issue : 6  |  Page : 281-284

Disseminated cutaneous leishmaniasis due to Leishmania (Leishmania) amazonensis in human immunodeficiency virus (HIV)-infected patients: A report of two cases


1 Hospital de Doenças Tropicais Doutor Anuar Auad; Laboratório de Imunidade Natural (LIN), Instituto de Patologia Tropical e Saúde Pública, Universidade Federal de Goiás, Goiânia, Goiás, Brazil
2 Laboratório de Imunidade Natural (LIN), Instituto de Patologia Tropical e Saúde Pública, Universidade Federal de Goiás, Goiânia, Goiás, Brazil

Date of Submission07-Oct-2020
Date of Decision22-Jan-2021
Date of Acceptance10-Mar-2021
Date of Web Publication25-Jun-2021

Correspondence Address:
Fátima Ribeiro-Dias
Laboratório de Imunidade Natural (LIN), Instituto de Patologia Tropical e Saúde Pública, Universidade Federal de Goiás, Goiânia, Goiás
Brazil
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Source of Support: This study is supported by Research Program for Sistema Único de Saúde (SUS)/Brazilian Ministry of Healthy/Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG) grant No. 201.710.267.001.235, Conflict of Interest: None


DOI: 10.4103/1995-7645.315891

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  Abstract 


Rationale: Co-infection of human immunodeficiency virus (HIV) and Leishmania spp. has impact on clinical and therapeutic outcomes of leishmaniases. Most studies do not present the identification of Leishmania species causing American tegumentary leishmaniasis in co-infections. In the Americas, Leishmania (L.) Viannia (V.) braziliensis and L. (V.) guyanensis have been identified.
Patient concerns: In this study, two cases of American tegumentary leishmaniasis in patients infected with HIV are described. Patients presented several lesions with rapid dissemination and mucosal involvement.
Diagnosis: Disseminated cutaneous leishmaniasis caused by L. amazonensis was identified by molecular test.
Interventions: The patients were treated with conventional therapies for HIV infection and American tegumentary leishmaniasis.
Outcomes: In co-infection, the clinical manifestations are atypical and the treatment response can be impaired.
Lessons: These cases show that HIV infection impacts L. amazonensis infection and point to the relevance of identifying Leishmania species, which can lead to a better patient management.

Keywords: Leishmania amazonensis; HIV; Disseminated cutaneous leishmaniasis; Case report


How to cite this article:
Araujo CF, N Oliveira IB, Silveira MB, Ribeiro-Dias F. Disseminated cutaneous leishmaniasis due to Leishmania (Leishmania) amazonensis in human immunodeficiency virus (HIV)-infected patients: A report of two cases. Asian Pac J Trop Med 2021;14:281-4

How to cite this URL:
Araujo CF, N Oliveira IB, Silveira MB, Ribeiro-Dias F. Disseminated cutaneous leishmaniasis due to Leishmania (Leishmania) amazonensis in human immunodeficiency virus (HIV)-infected patients: A report of two cases. Asian Pac J Trop Med [serial online] 2021 [cited 2022 Jul 2];14:281-4. Available from: https://www.apjtm.org/text.asp?2021/14/6/281/315891


  1. Introduction Top


Leishmania (L.) amazonensis protozoan is associated with localized cutaneous leishmaniasis, disseminated cutaneous leishmaniasis (DL), and diffuse cutaneous leishmaniasis (DCL). Whereas DL patients present cellular immunity and therapeutic response, DCL represents an anergic pole of immune response and there is no effective treatment[1]. The co-infection with Leishmania/human immunodeficiency virus (HIV) is a public health problem and represents 8.5% of all patients with American tegumentary leishmaniasis in Brazil. These two infectious agents act synergistically, facilitating their own replication and survival[2].

Co-infection with HIV/Leishmania has increased in Latin America. Most of the studies do not present the identification of Leishmania species causing American tegumentary leishmaniasis. In the Americas, few studies of co-infection reported L. braziliensis[3],[4] and L. guyanensis[5] as causal agents in co-infections. Recently, L. amazonensis was reported causing DCL[6]. Here, we described two cases of DL in patients infected with HIV caused by L. amazonensis.

This study was approved by the local Ethics Committee (CAAE82524717.1.0000.5078), and patients signed the consent to participate in the research and publication.


  2. Case reports Top


2.1. Case 1

In February 2019, an ulcerated lesion appeared on the scrotal region of a Brazilian 50-year-old male patient from Goiás, Midwestern region. After one month, ulcerated lesions spread for the trunk, face, nasal mucosa, and upper limbs. Lower limbs were affected presenting bleeding and papular lesions. Histopathological analysis suggested Leishmania infection and the patient was tested HIV positive by enzymatic immune assay (ELISA) and polymerase chain reaction (PCR). In [Figure 1], the inflammatory process showed several macrophages with large vacuoles containing rounded structures, which were confirmed as Leishmania by immunohistochemistry. High number of CD68+ macrophages as well as CD3+ T lymphocytes was presented [Figure 1]. The isolated parasite was characterized as L. amazonensis by PCR[7]. Reactive serology and computed tomography of the chest suggested paracoccidioidomycosis. The indirect immunofluorescence test (IFT) for American tegumentary leishmaniasis was positive (1/40), CD4+ T lymphocyte count was 69 cells/mm3, and the viral load was 143 993.
Figure 1: An ulcerated lesion appeared on the scrotal region of a Brazilian 50-year-old male patient from Goiás, Midwestern region. After one month, ulcerated lesions spread to the trunk, face, nasal mucosa, and upper limbs. Lower limbs were affected presenting bleeding and papular lesions. Histopathological analysis suggested Leishmania infection and the patient was tested HIV positive. Biopsy fragment from one cutaneous lesion was used to perform H&E and immunohistochemistry (IHC) stainings. (A) Panoramic view of the lesion, showing severe inflammatory process with mononuclear cells in upper and lower layers of the dermis (H&E, 200×). (B) Parasitophorous vacuoles in macrophages with rounded structures, suggestive of amastigotes, adhered to the membranes (H&E, 200×). (C) IHC detection of CD68+ macrophages (IHC, 200×). (D) CD3+ T lymphocytes (IHC, 40×). (E) CD20+ B lymphocytes (IHC, 40×). (F) Amastigotes (IHC, 400×). The inset presents amastigote in detail showing nucleus and kinetoplast (1 000×).

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The antiretroviral tenofovir + lamivudine + dolutegravir and prophylactic antibiotic (sulfamethoxazole-trimethoprim) treatments were started for HIV infection. The meglumine antimoniate (Glucantime®) was used for American tegumentary leishmaniasis, but it was suspended on the 9th day due to alterations in the electrocardiogram. Then, liposomal amphotericin B was used for 12 days. The schedules are presented in [Table 1]. The patient has ended American tegumentary leishmaniasis treatment when itraconazole was prescribed for paracoccidioidomycosis. All American tegumentary leishmaniasis lesions were healed. His viral load became undetectable, CD4+ T lymphocyte count was still low (77 cells/mm3), but American tegumentary leishmaniasis lesions remained healed. He is still under follow up [Table 1].
Table 1: Clinical evolution of Leishmania (Leishmania) amazonensis/HIV co-infected patients.

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2.2. Case 2

In Mato Grosso (Midwestern region), in June 2017, a Brazilian 52-year-old male patient was diagnosed with HIV (ELISA/PCR) and started the treatment with tenofovir + lamivudine + dolutegravir. In November, he finished the treatment for tuberculosis. In December, he presented several cutaneous papular and ulcerated lesions on the lower limbs and feet, besides mucosal lesion when he arrived at Hospital de Doenças Tropicais (HDT, in Goiás). From a lesion fragment, L. amazonensis was identified by PCR[7] confirming American tegumentary leishmaniasis. Initially, he was treated with liposomal amphotericin for 7 days, but the lesions relapsed. He underwent amphotericin B deoxycholate for 10 days and subsequently, a second cycle of liposomal amphotericin for 8 days, with partial improvement. At the beginning of American tegumentary leishmaniasis treatment, CD4+ T lymphocyte count was 278 cells/mm3 and the viral load was undetectable. In April 2018, he was treated again with liposomal amphotericin for 10 days, followed by weekly prophylactic Glucantime®, ending in July 2018. The tuberculosis relapsed and treatment was changed [Table 1]. In November, the lesions were partially healed, presented pruritus, and some of them showed serous secretion due to secondary skin infection. The patient received cephalothin for seven days with clinical improvement. In March 2019, the IFT for American tegumentary leishmaniasis was positive (1/160), with active lesions on the lower limbs and nasal mucosa. Then, fluconazole was prescribed for 30 days. In June 2019, the cutaneous lesions were fully healed, there were no active lesions on the nasal mucosa, IFT was negative, and tuberculosis was cured. Although the patient did not continue under follow up in Goiás, his viral load was required in Mato Grosso in October 2019, and it was undetectable. He was considered clinically cured for American tegumentary leishmaniasis [Table 1].


  3. Discussion Top


The current co-infected patients presented several atypical, papular and inflammatory cutaneous lesions with ulceration, besides nasal mucosa involvement; the histophatological findings showed low amounts of amastigote forms and predominance of macrophages, but also B lymphocytes and high numbers of T lymphocytes. Both patients presented clinical cure with regular treatments for American tegumentary leishmaniasis and were infected with L. amazonensis. Although the cellular immune response was not evaluated, all the aspects above, in accordance with previous studies on American tegumentary leishmaniasis[8],[9], suggested the diagnosis of DL instead of DCL caused by L. amazonensis[6].

In case 1, the pleomorphic and fast disseminated lesions outlined an aggressive DL. This outcome was expected due to the immunodeficiency caused by the reduced CD4+ T lymphocyte count, which can lead to a deficiency in containing the parasite. Although case 2 presented a better immune status compared to case 1, he also had multiple papular and ulcerative cutaneous lesions. In both patients, the treatment was difficult, requiring different drugs to obtain success. As in this study, different schedules of treatments have been described for HIV-infected patients with American tegumentary leishmaniasis, which lead to an increase in side effects of the drugs[2],[3].

The two cases here indicate that HIV infection can impact L. amazonensis infection leading to the spread of the parasite and make the American tegumentary leishmaniasis therapy difficult. Differences in response to American tegumentary leishmaniasis treatments have been described when comparing patients infected with different Leishmania spp[10]. Moreover, pentavalent antimonial fails to treat most of co-infected patients and causes increased side effects[3],[5] as shown here. Remarkably, studies comparing the therapeutic outcome of American tegumentary leishmaniasis caused by different Leishmania spp. in HIV-infected patients are missing.

Our study described two cases of co-infected patients with L. amazonensis and HIV and indicates the necessity of Leishmania species identification to improve the management of co-infected patients.

Conflict of interest statement

The authors declare that there are no conflicts of interest.

Acknowledgements

We thank the financial support by the Research Program for Sistema Único de Saúde (SUS)/Brazilian Ministry of Healthy/Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG; grant to F.R-D). This study was supported in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil(CAPES)-Finance Code 001. IBNO is FAPEG/CAPES’s fellow and FR-D is research’s fellow of Brazilian National Council for Scientific and Technological Development (CNPq). The authors are grateful to the contribution of Dr. Sebastião Alves Pinto for histopathological analyses (Faculty of Medicine, Universidade Federal de Goiás and Instituto Goiano de Oncolologia e Hematologia) and Dr. Miriam Leandro Dorta by technical support in Leishmania species identification.

Funding

This study is supported by Research Program for Sistema Único de Saúde (SUS)/Brazilian Ministry of Healthy/Fundação de Amparo à Pesquisa do Estado de Goiás (FAPEG) grant No. 201.710.267.001.235.

Authors’ contributions

C.F.A. contributed to data acquisition and manuscript preparation. I.B.N.O. contributed to data acquisition and manuscript preparation as well as edition and revision. M.B.S. performed the Leishmania species identification. F.R-D. revised and edited the manuscript. Both I.B.N.O and F.R-D contributed equally to the final version of the manuscript. F.R-D. was responsible for conception and supervision of the research project and the manuscript.

 
  References Top

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Goto H, Lindoso JAL. Cutaneous and mucocutaneous leishmaniasis. Infect Dis Clin North Am 2012; 26: 293-307.  Back to cited text no. 1
    
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Sampaio R, Salaro C, Resende P, De Paula C. American cutaneous leishmaniasis associated with HIV/AIDS: Report of four clinical cases. Rev Soc Bras Med Trop 2002; 35: 651-654.  Back to cited text no. 3
    
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Silva G, Sugui D, Nunes R, Azevedo K, Azevedo M, Marques A, et al. Mucocutaneous leishmaniasis/HIV coinfection presented as a diffuse desquamative rash. Case Rep Infect Dis 2014; 2014: 293761. doi: 10.1155/2014/293761.  Back to cited text no. 4
    
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Corrêa Soares GH, Silva ABSD, Ferreira LSS, Ithamar JS, Medeiros GA, Pereira SRF, et al. Case report: Coinfection by Leishmania amazonensis and HIV in a Brazilian diffuse dutaneous leishmaniasis patient. Am J Trop Med Hyg 2020; 103(3): 1076-1080.  Back to cited text no. 6
    
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Volpini A, Passos V, Oliveira G, Romanha A. PCR-RFLP to identify Leishmania(Viannia) braziliensis and L. (Leishmania) amazonensis causing American cutaneous leishmaniasis. Acta Trop 2004; 90: 31-37.  Back to cited text no. 7
    
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Pereira LIA, Dorta ML, Pereira AJCS, Bastos RP, Oliveira MAP, Pinto, AS, et al. Case report: Increase of NK cells and proinflammatory monocytes are associated with the clinical improvement of diffuse cutaneous leishmaniasis after immunochemotherapy with BCG/ Leishmania antigens. Am J Trop Med Hyg 2009; 81: 378-383.  Back to cited text no. 8
    
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Machado GU, Prates FV, Machado PRL. Disseminated leishmaniasis: Clinical, pathogenic, and therapeutic aspects. An Bras Dermatol 2019; 94: 9-16.  Back to cited text no. 9
    
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Romero GAS, Guerra MVF, 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: 456-465.  Back to cited text no. 10
    


    Figures

  [Figure 1]
 
 
    Tables

  [Table 1]


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