Non-Zoonotic Transmission of Sporotrichosis: A Translational Study of Forty-Three Cases in a Zoonotic Hyperendemic Area
Abstract
:1. Introduction
2. Materials and Methods
2.1. Ethical Approval
2.2. Elaboration of the Database and Clinical Strains
2.3. Molecular Identification
2.4. Antifungal Susceptibility Testing
2.5. Statistical Analyses
3. Results
3.1. Analysis of Socio-Demographic, Epidemiological and Clinical Data of Patients
3.2. Sporothrix spp. Identification
3.3. Antifungal Susceptibility Profile
3.4. Description of Clinical Data of Patients According to the Type of Fungal Species Identified
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Maria, R.; De, R.; De Oliveira, M.M.E.; Saraiva Freitas, D.F.; Gutierrez Galhardo, M.C. New Diagnostic Applications in Sporotrichosis. In Skin Biopsy—Perspectives; Khopkar, U., Ed.; InTech: Houston TX, USA, 2011; ISBN 978-953-307-290-6. Available online: http://www.intechopen.com/books/skin-biopsy-perspectives/new-diagnostic-applications-in-sporotrichosis (accessed on 23 May 2024).
- Orofino-Costa, R.; de Macedo, P.M.; Rodrigues, A.M.; Bernardes-Engemann, A.R. Sporotrichosis: An update on epidemiology, etiopathogenesis, laboratory and clinical therapeutics. An. Bras. Dermatol. 2017, 92, 606–620. [Google Scholar] [CrossRef] [PubMed]
- Falcão, E.M.M.; Pires, M.C.d.S.; Andrade, H.B.; Gonçalves, M.L.C.; Almeida-Paes, R.; do Valle, A.C.F.; Bastos, F.I.; Gutierrez-Galhardo, M.C.; Freitas, D.F.S. Zoonotic sporotrichosis with greater severity in Rio de Janeiro, Brazil: 118 hospitalizations and 11 deaths in the last 2 decades in a reference institution. Med. Mycol. 2020, 58, 141–143. [Google Scholar] [CrossRef] [PubMed]
- Schubach, A.; Schubach, T.M.P.; Barros, M.B.d.L.; Wanke, B. Cat-transmitted sporotrichosis, Rio de Janeiro, Brazil. Emerg. Infect. Dis. 2005, 11, 1952–1954. [Google Scholar] [CrossRef]
- Freitas, D.F.S.; do Valle, A.C.F.; de Almeida Paes, R.; Bastos, F.I.; Galhardo, M.C.G. Zoonotic Sporotrichosis in Rio de Janeiro, Brazil: A protracted epidemic yet to be curbed. Clin. Infect. Dis. 2010, 50, 453. [Google Scholar] [CrossRef]
- Arrillaga-Moncrieff, I.; Capilla, J.; Mayayo, E.; Marimon, R.; Mariné, M.; Gené, J.; Cano, J.; Guarro, J. Different virulence levels of the species of Sporothrix in a murine model. Clin. Microbiol. Infect. 2009, 15, 651–655. [Google Scholar] [CrossRef] [PubMed]
- Della Terra, P.P.; Rodrigues, A.M.; Fernandes, G.F.; Nishikaku, A.S.; Burger, E.; de Camargo, Z.P. Exploring virulence and immunogenicity in the emerging pathogen Sporothrix brasiliensis. PLoS Negl. Trop. Dis. 2017, 11, e0005903. [Google Scholar] [CrossRef] [PubMed]
- Rodrigues, A.M.; de Hoog, G.S.; de Camargo, Z.P. Sporothrix Species Causing Outbreaks in Animals and Humans Driven by Animal-Animal Transmission. PLoS Pathog. 2016, 12, e1005638. [Google Scholar] [CrossRef]
- Gremião, I.D.F.; Oliveira, M.M.E.; Monteiro de Miranda, L.H.; Saraiva Freitas, D.F.; Pereira, S.A. Geographic Expansion of Sporotrichosis, Brazil. Emerg. Infect. Dis. 2020, 26, 621–624. [Google Scholar] [CrossRef]
- Silva, M.B.T.D.; Costa, M.M.D.M.; Torres, C.C.D.S.; Galhardo, M.C.G.; Valle, A.C.F.D.; Magalhães, M.D.A.F.M.; Sabroza, P.C.; Oliveira, R.M.D. Esporotricose urbana: Epidemia negligenciada no Rio de Janeiro, Brasil. Cad. Saúde Pública 2012, 28, 1867–1880. [Google Scholar] [CrossRef]
- Fichman, V.; Freitas, D.F.S.; de Macedo, P.M.; do Valle, A.C.F.; Almeida-Silva, F.; Zancopé-Oliveira, R.M.; Almeida-Paes, R.; Gutierrez-Galhardo, M.C. Sporotrichosis After Tattooing Caused by Sporothrix brasiliensis. Mycopathologia 2022, 187, 137–139. [Google Scholar] [CrossRef]
- Ferrer, C.; Colom, F.; Frasés, S.; Mulet, E.; Abad, J.L.; Alió, J.L. Detection and identification of fungal pathogens by PCR and by ITS2 and 5.8S ribosomal DNA typing in ocular infections. J. Clin. Microbiol. 2001, 39, 2873–2879. [Google Scholar] [CrossRef]
- Marimon, R.; Gené, J.; Cano, J.; Trilles, L.; Dos Santos Lazéra, M.; Guarro, J. Molecular phylogeny of Sporothrix schenckii. J. Clin. Microbiol. 2006, 44, 3251–3256. [Google Scholar] [CrossRef] [PubMed]
- Tamura, K.; Nei, M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 1993, 10, 512–526. [Google Scholar] [PubMed]
- CLSI—Clinical and Laboratory Standars Institute. Reference Method for Broth Dilution Antifungal Susceptibility Testing of Filamentous Fungi; CLSI document M38-A2; Approved Standard-Second Edition; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2008; Volume 28, ISBN 978-1-56238-668-9. [Google Scholar]
- Espinel-Ingroff, A.; Abreu, D.P.B.; Almeida-Paes, R.; Brilhante, R.S.N.; Chakrabarti, A.; Chowdhary, A.; Hagen, F.; Córdoba, S.; Gonzalez, G.M.; Govender, N.P.; et al. Multicenter, International Study of MIC/MEC Distributions for Definition of Epidemiological Cutoff Values for Sporothrix Species Identified by Molecular Methods. Antimicrob. Agents Chemother. 2017, 61, e01057-17. [Google Scholar] [CrossRef]
- Chakrabarti, A.; Bonifaz, A.; Gutierrez-Galhardo, M.C.; Mochizuki, T.; Li, S. Global epidemiology of sporotrichosis. Med. Mycol. 2015, 53, 3–14. [Google Scholar] [CrossRef] [PubMed]
- da Rosa, A.C.M.; Scroferneker, M.L.; Vettorato, R.; Gervini, R.L.; Vettorato, G.; Weber, A. Epidemiology of sporotrichosis: A study of 304 cases in Brazil. J. Am. Acad. Dermatol. 2005, 52, 451–459. [Google Scholar] [CrossRef]
- de Oliveira, M.M.E.; de Almeida-Paes, R.; de Medeiros Muniz, M.; de Lima Barros, M.B.; Galhardo, M.C.G.; Zancope-Oliveira, R.M. Sporotrichosis caused by Sporothrix globosa in Rio De Janeiro, brazil: Case report. Mycopathologia 2010, 169, 359–363. [Google Scholar] [CrossRef]
- Schubach, T.M.P.; Schubach, A.; Okamoto, T.; Barros, M.B.L.; Figueiredo, F.B.; Cuzzi, T.; Fialho-Monteiro, P.C.; Reis, R.S.; Perez, M.A.; Wanke, B. Evaluation of an epidemic of sporotrichosis in cats: 347 cases (1998–2001). J. Am. Vet. Med. Assoc. 2004, 224, 1623–1629. [Google Scholar] [CrossRef]
- Rabello, V.B.S.; Almeida-Silva, F.; Scramignon-Costa, B.d.S.; Motta, B.d.S.; de Macedo, P.M.; Teixeira, M.d.M.; Almeida-Paes, R.; Irinyi, L.; Meyer, W.; Zancopé-Oliveira, R.M. Environmental Isolation of Sporothrix brasiliensis in an Area With Recurrent Feline Sporotrichosis Cases. Front. Cell Infect. Microbiol. 2022, 12, 894297. [Google Scholar] [CrossRef]
- Almeida-Silva, F.; Rabello, V.B.d.S.; Scramignon-Costa, B.d.S.; Zancopé-Oliveira, R.M.; de Macedo, P.M.; Almeida-Paes, R. Beyond Domestic Cats: Environmental Detection of Sporothrix brasiliensis DNA in a Hyperendemic Area of Sporotrichosis in Rio de Janeiro State, Brazil. J. Fungi 2022, 8, 604. [Google Scholar] [CrossRef]
- Montenegro, H.; Rodrigues, A.M.; Dias, M.A.G.; da Silva, E.A.; Bernardi, F.; de Camargo, Z.P. Feline sporotrichosis due to Sporothrix brasiliensis: An emerging animal infection in São Paulo, Brazil. BMC Vet. Res. 2014, 10, 269. [Google Scholar] [CrossRef]
- Chaves, A.R.; de Campos, M.P.; Barros, M.B.L.; do Carmo, C.N.; Gremião, I.D.F.; Pereira, S.A.; Schubach, T.M.P. Treatment abandonment in feline sporotrichosis—Study of 147 cases. Zoonoses Public Health 2013, 60, 149–153. [Google Scholar] [CrossRef] [PubMed]
- Miller, S.D.; Keeling, J.H. Ant sting sporotrichosis. Cutis 2002, 69, 439–442. [Google Scholar] [PubMed]
- Haddad, V.J.; Miot, H.A.; Bartoli, L.D.; Cardoso, A.d.C.; de Camargo, R.M.P. Localized lymphatic sporotrichosis after fish-induced injury (Tilapia sp.). Med. Mycol. 2002, 40, 425–427. [Google Scholar] [CrossRef]
- Rodrigues, A.M.; de Hoog, G.S.; de Camargo, Z.P. Molecular Diagnosis of Pathogenic Sporothrix Species. PLoS Negl. Trop. Dis. 2015, 9, e0004190. [Google Scholar] [CrossRef]
- Teixeira, M.M.; de Almeida, L.G.P.; Kubitschek-Barreira, P.; Alves, F.L.; Kioshima, E.S.; Abadio, A.K.R.; Fernandes, L.; Derengowski, L.S.; Ferreira, K.S.; Souza, R.C.; et al. Comparative genomics of the major fungal agents of human and animal Sporotrichosis: Sporothrix schenckii and Sporothrix brasiliensis. BMC Genom. 2014, 15, 943. [Google Scholar] [CrossRef]
- Almeida-Paes, R.; de Oliveira, M.M.E.; Freitas, D.F.S.; do Valle, A.C.F.; Zancopé-Oliveira, R.M.; Gutierrez-Galhardo, M.C. Sporotrichosis in Rio de Janeiro, Brazil: Sporothrix brasiliensis is associated with atypical clinical presentations. PLoS Negl. Trop. Dis. 2014, 8, e3094. [Google Scholar] [CrossRef]
- Bittencourt, A.A.; Oyafuso, L.K.M.; Cavalin, R.F.; Palhares, R.B.; Benard, G.; Gimenes, V.M.F.; Del Negro, G.M.B.; Siqueira, L.P.M.; de Freitas Xavier, R.S.; Lopes-Bezerra, L.M.; et al. A neglected disease. Human sporotrichosis in a densely populated urban area in São Paulo, Brazil: Clinical-epidemiological and therapeutic aspects. Braz. J. Microbiol. 2022, 53, 739–748. [Google Scholar] [CrossRef]
- Bernardes-Engemann, A.R.; Tomki, G.F.; Rabello, V.B.d.S.; Almeida-Silva, F.; Freitas, D.F.S.; Gutierrez-Galhardo, M.C.; Almeida-Paes, R.; Zancopé-Oliveira, R.M. Sporotrichosis Caused by Non-Wild Type Sporothrix brasiliensis Strains. Front. Cell Infect. Microbiol. 2022, 12, 893501. [Google Scholar] [CrossRef] [PubMed]
- Teixeira, M.M.; Almeida-Paes, R.; Bernardes-Engemann, A.R.; Nicola, A.M.; de Macedo, P.M.; Valle, A.C.F.; Gutierrez-Galhardo, M.C.; Freitas, D.F.S.; Barker, B.M.; Matute, D.R.; et al. Single nucleotide polymorphisms and chromosomal copy number variation may impact the Sporothrix brasiliensis antifungal susceptibility and sporotrichosis clinical outcomes. Fungal Genet. Biol. 2022, 163, 103743. [Google Scholar] [CrossRef]
- Almeida-Silva, F.; Coelho, R.A.; Bernardes-Engemann, A.R.; Fichman, V.; Freitas, D.F.; Galhardo, M.C.; Corrêa, D., Jr.; Frases, S.; Zancopé-Oliveira, R.M.; Almeida-Paes, R. In vitro isavuconazole activity against Sporothrix brasiliensis suggests its efficacy in some severe sporotrichosis cases. Future Microbiol. 2023, 18, 1041–1048. [Google Scholar] [CrossRef]
Variable | Description | N (%) |
---|---|---|
Epidemiology | Plants and/or soil manipulation | 21 (48.8%) |
Unknown | 12 (27.9%) | |
Insect bites | 4 (9.4%) | |
Previous trauma * | 2 (4.7%) | |
Human aggression | 1 (2.3%) | |
Human bite | 1 (2.3%) | |
Trauma with iron gate | 1 (2.3%) | |
Trauma with fishbone | 1 (2.3%) | |
Clinical form | Lymphocutaneous | 28 (65%) |
Fixed cutaneous | 10 (23.3%) | |
Cutaneous disseminated | 2 (4.7%) | |
Unifocal extracutaneous ** | 2 (4.7%) | |
Disseminated | 1 (2.3%) | |
Treatment | Itraconazole | 27 (62.9%) |
Terbinafine | 3 (7%) | |
Change in treatment | Itraconazole to terbinafine Itraconazole to amphotericin B Itraconazole to terbinafine to amphotericin B Itraconazole to posaconazole | 4 (9.3%) |
1 (2.3%) | ||
1 (2.3%) | ||
1 (2.3%) | ||
Adjuvant treatment | Cryosurgery associated with itraconazole Cryosurgery associated with itraconazole and terbinafine Cryosurgery associated with terbinafine Cryosurgery Warm water compress | 2 (4.7%) |
1 (2.3%) | ||
1 (2.3%) | ||
1 (2.3%) | ||
1 (2.3%) | ||
Outcome | Clinical cure | 35 (81.4%) |
Lost to follow-up | 6 (13.9%) | |
Still under treatment | 2 (4.7%) |
Clinical Form (Total) (%) | Lesion Topography (Number of Patients) (%) |
---|---|
Lymphocutaneous (28) (65%) | Upper limbs (17) (39.5%) |
Lower limbs (6) (13.9%) | |
Trunk (4) (9.3%) | |
Face (1) (2.3%) | |
Fixed cutaneous (10) (23.3%) | Upper limbs (5) (11.6%) |
Lower limbs (4) (9.3%) | |
Trunk (1) (2.3%) | |
Cutaneous disseminated (2) (4.7%) | Skin (2) (4.7%) |
Disseminated (1) (2.3%) | Skin/Eye/Upper airways/Multifocal bones (1) (2.3%) |
Unifocal extracutaneous (2) (4.7%) | Eye (1) (2.3%) |
Lung (1) (2.3%) |
Age Group | Clinical Form (N) | Occupation |
---|---|---|
0–18 | Lymphocutaneous (5) | Students |
Fixed cutaneous (1) | ||
19–59 | Lymphocutaneous (18) | Housewives; service workers and trade sellers; mid-level technicians; painting workers; service workers in general; teachers; masonry structure workers; bus drivers; auto mechanics; structural assembly workers in civil works; members of the armed forces, police and fire service; commerce operators in stores and markets; economists; and people outside the labor market. |
Fixed cutaneous (4) | ||
Disseminated (1) | ||
Cutaneous disseminated (1) | ||
Unifocal extracutaneous (ocular) (1) | ||
≥60 | Lymphocutaneous (5) | Retired; housewives; service workers and trade sellers, auto mechanics and painting workers |
Fixed cutaneous (5) | ||
Cutaneous disseminated (1) | ||
Unifocal extracutaneous (pulmonary) (1) |
Treatment (Total) | Clinical Outcome (N) |
---|---|
Itraconazole (27) | Cure (22) |
Lost to follow-up (4) | |
Still under treatment (1) | |
Terbinafine (3) | Cure (3) |
Itraconazole to terbinafine (4) | Cure (4) |
Itraconazole to amphotericin B (1) | Lost to follow-up (1) |
Itraconazole to terbinafine to amphotericin B (1) | Lost to follow-up (1) |
Itraconazole to posaconazole (1) | Still under treatment (1) |
Cryosurgery (1) | Cure (1) |
Cryosurgery associated with itraconazole (2) | Cure (2) |
Cryosurgery associated with itraconazole and terbinafine (1) | Cure (1) |
Cryosurgery associated with terbinafine (1) | Cure (1) |
Warm water compress (1) | Cure (1) |
MIC (µg/mL) | ECV Interpretation Number of Isolates | |||||
---|---|---|---|---|---|---|
Species (N) | Antifungal | Range | MIC50/MIC90 | GM | WT | non-WT |
AMB | 0.5–8 | 4/4 | 2.31 | 38 | 1 | |
S. brasiliensis | TRB | 0.03–0.12 | 0.06/0.12 | 0.06 | 39 | 0 |
(39) | ITR | 0.5–8 | 1/2 | 1.11 | 38 | 1 |
POS | 0.25–2 | 1/2 | 1.11 | 39 | 0 | |
ISA | 0.5–4 | 2/4 | 2.43 | - | - | |
S. globosa | AMB | 1–4 | 1/4 | 2.52 | - | - |
(3) | TRB | 0.06–0.12 | 0.06/0.12 | 0.08 | - | - |
ITR | 1–2 | 1/2 | 1.26 | - | - | |
POS | 1–2 | 1/2 | 1.59 | - | - | |
ISA | 2–4 | 2/4 | 2.52 | - | - | |
S. schenckii | AMB | 8 | - | - | 0 | 1 |
(1) | TRB | 0.25 | - | - | 0 | 1 |
ITR | 4 | - | - | 0 | 1 | |
POS | 4 | - | - | 0 | 1 | |
ISA | 4 | - | - | - | - |
Strain | Sex/ Age | Occupation | Transmission | Clinical Form | Comorbidities | Treatment/Outcome |
---|---|---|---|---|---|---|
S. globosa 27135 | F/77 | Housewife | Contact with plants | Lymphocutaneous | - | ITR/Cure |
S. globosa 34540 | M/62 | Auto mechanic | Previous trauma * | Fixed cutaneous | High blood pressure | ITR/TRB Cure |
S. globosa 43391 | F/71 | Teacher | Previous trauma * | Lymphocutaneous | High blood pressure and diabetes mellitus | ITR/Cure |
S. schenckii 43461 | F/71 | Retired | Contact with plants | Lymphocutaneous | Hyperthyroidism | ITR/Cure |
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Nahal, J.; Coelho, R.A.; Almeida-Silva, F.; Bernardes-Engemann, A.R.; Procópio-Azevedo, A.C.; Rabello, V.B.d.S.; Loureiro, R.G.; Freitas, D.F.S.; do Valle, A.C.F.; de Macedo, P.M.; et al. Non-Zoonotic Transmission of Sporotrichosis: A Translational Study of Forty-Three Cases in a Zoonotic Hyperendemic Area. J. Fungi 2024, 10, 610. https://doi.org/10.3390/jof10090610
Nahal J, Coelho RA, Almeida-Silva F, Bernardes-Engemann AR, Procópio-Azevedo AC, Rabello VBdS, Loureiro RG, Freitas DFS, do Valle ACF, de Macedo PM, et al. Non-Zoonotic Transmission of Sporotrichosis: A Translational Study of Forty-Three Cases in a Zoonotic Hyperendemic Area. Journal of Fungi. 2024; 10(9):610. https://doi.org/10.3390/jof10090610
Chicago/Turabian StyleNahal, Juliana, Rowena Alves Coelho, Fernando Almeida-Silva, Andréa Reis Bernardes-Engemann, Anna Carolina Procópio-Azevedo, Vanessa Brito de Souza Rabello, Rayanne Gonçalves Loureiro, Dayvison Francis Saraiva Freitas, Antonio Carlos Francesconi do Valle, Priscila Marques de Macedo, and et al. 2024. "Non-Zoonotic Transmission of Sporotrichosis: A Translational Study of Forty-Three Cases in a Zoonotic Hyperendemic Area" Journal of Fungi 10, no. 9: 610. https://doi.org/10.3390/jof10090610