Review on human mycoses in South America
José A. Serrano, MD* y Darío Novoa-Montero, MD, MPH, PhD**

Reseña de las micosis humanas en Sudamérica

* Microbiologist-Mycologist (MD). Facultad de Medicina, Departamento de Patología, Universidad de Los Andes, Mérida, Venezuela.

** Internist, Cardiologist, Chronic Diseases Epidemiologist (MD, MHS, PhD). Laboratorio Multidisciplinario de Investigación Clínico-Epidemiológica (Lab-MICE). Unidad de Medicina Interna and Departamento de Medicina, Universidad de Los Andes, Mérida, Venezuela.

Key-words: Human mycoses, histoplasmosis, coccidioidomycosis, AIDS.

Introduction

    This is a comprehensive review on human mycoses in South America. Our aim, according to the main objectives of the I International Symposium on Mycoses in the New Millennium. Challenges and Strategies, is to give an up-dated overview to mycologists on historical and current relevant findings on human mycoses in this western sub-continent. This paper is an updated review of the original Ferst International Symposium on Mycoses in the New Millennium-Challenges & Strategies Society for Indian Human and Animal Mycologists, Chennai (India) 2000. This review is a further and complementary inside on the same subject published by G. de San Blas.

    South America has an overall area of 17,805,200 square kilometers. It is surrounded by the Caribbean Sea at North, by the Atlantic Ocean at East and South, and by the Pacific Ocean at West and South. The geopolitical distribution by countries is in alphabetic order, Argentina, Bolivia, Brazil, Chile, Colombia, Ecuador, Paraguay, Perú, Uruguay and Venezuela (Spanish and Portuguese colonization); and Guiana, Trinidad (British colonization), Surinam (Dutch colonization), and French Guiana. South America is the fourth subcontinent (12% of Earth surface) and is located between 35° and 89° West longitude, and between 12° North, and 55° 30' South latitudes.

    The critical reader of this review should take into account that gathering enough information on this discipline, and summarizing data in the short time we were allowed since Dr. Venugopal choose our names to carry out this task, was compelling and challenging, because possibly many of the relevant existing contributions have been only locally known in dissertations, or sporadic descriptions appeared in relatively 'obscure' publications or 'conferences'. In addition, many articles have not been indexed or included in the new electronic bank of data (Internet). Therefore, the recovering of such kind of information to enlighten this review has some kind of 'serendipity'. This review on mycoses in South America is based on data gathered from national textbooks (Brazil, and Switzerland editors), personal interviews and unpublished data (Brazil).

    The remaining countries data were gathered from North American textbooks, journals, and Med-line and Lilacs banks of data. Recently, G. Cunto de San Blas published relevant historical data on the development of Mycology in South America (1). This amazing paper was a complement to another one published by Briceño-Maaz, Albornoz and San Blas on historical aspects of Mycology in Venezuela (2).

    Our review covers historical aspects, pioneer communications, and relevant published papers on the main cutaneous and deep human mycoses. Emphasis on summary data of papers and other publications on emergent syndromes associated to immunosuppressed people, especially among AIDS patients, are also included.

Review of Case-Reports and Series of Cases in South America, by Countries

    Mycoses frequently reported in South America are paracoccidioidomycosis, histoplasmosis, chromomycosis, eumycetoma, and lobomycosis. Less frequently reported is tinea imbricata. We do not emphasize data on cryptococcosis or sporotrichosis because they are worldwide endemic diseases.

    1. Paracoccidioidomycosis. Paracoccidioidosis is the leader deep human mycosis in South America. Map 1 shows the geographical distribution of paracoccidioidomycosis by Paracoccidioides brasiliensis in South America. It has been found in almost every South American country. The larger number of cases has been reported in Brazil, Venezuela, Argentina, Uruguay, Ecuador, Colombia, Paraguay and Perú. Relatively few cases have been reported in Bolivia, and in French Guiana.

    2. Histoplasmosis. Histoplasmosis (Histoplasma capsulatum) is the second most frequently reported endemic deep human mycosis in South America. Map 2 shows that the higher frequency of cases has been found in Argentina, Brazil, Venezuela and Uruguay. Less frequently it has been found in Northern Chile, Perú, Colombia, Guiana, Bolivia and Paraguay.

Mapa 1. Geographical distribution of paracoccidiomycosis in South America

Mapa 2. Geographical distribution of histoplasmosis in South America

Mapa 3. Geographical distribution of coccidioidomycosis in South America

Mapa 4. Geographical distribution of chromomycosis in South America

Mapa 5. Geographical distribution of mycetoma in South America

Mapa 6. Geographical distribution of lobomycosis in South America

    3. Coccidioidomycosis. Map 3 shows that coccidioidomycosis (Coccidioides immitis) is endemic in Argentina, Paraguay, Venezuela, Bolivia, Colombia, and Northeastern Brazil. It is less frequent in Colombia, Ecuador, Perú, Chile, and Uruguay. The reservaria of C. immitis goes from 34º North latitude to 40º South latitude in ecological areas where mean annual rainfall is below 800 mm.

    4. Chromomycosis (Cladosporium carrionii and Fonsecae pedrosoi) is endemic in Northwestern and Western Venezuela (Falcón, Lara and Zulia states), Northeast and Central Brazil (Amazon Basin). Some cases have been reported in Colombia (Amazon Basin region) and Argentina (see Map 4).

    5. Eumycetoma. Map 5 shows that geographical areas most frequently affected by eumycetomas (Madurella risea, Pyrenochaeta mackinnoni) are Central Venezuela, East and Central Brazil, Northeastern Argentina, and Uruguay. Few cases have been found in Colombia and Ecuador.

Mapa 7. Geographical distribution of Tinea imbricata in South America

    6. Lobomycosis. Lobomycosis (Paracoccidioides loboi or Lacazia loboi) is a rare deep human mycosis. Map 6 shows that in Amazon Basin and Central Brazil, lobomycosis is relatively frequent, mainly among the Caibai indians. Few cases have been reported in French Guiana, Venezuela, Colombia and Argentina.

    7. Tinea imbricata, chimbereê, tokelau, tinea circinata tropicalis, is a contagious dermatophytosis diagnosed in some limited geographical regions in many islands in the Pacific Ocean, Malaysian Archipelago, Southern India, Ceylon, and in the Fiji Islands (Tamana, Lav group). Map 7 shows that tinea imbricata has been found in Amerindian as the purú-borá Indians (Brazil); and some cases have been reported in Colombia.

    Other cutaneous mycoses (dermatophytoses), nail mycoses, ocular mycoses, otomycoses, several opportunistic mycoses, and rhinosporidiosis do not deserve any special map or comments in this paper, since their frequency in South America are similar to that observed worldwide.

The Role f Fungi In Some Authoctonous South American Ethnic Groups

    Fungi have played a significant role in the everyday life, habits and economy within South American native tribes, and in the inbred communities resulting from the early Spanish and Portuguese colonization of South America. An amazing description of the everyday and ritual uses of fungi by South American Indians is found in the San Blas' paper, 'From magic to science…' (1). Since many decades, fungi have been also associated to individual diseases and syndromes among the melting pot ethnic groups resulting from post First and Second World Wars immigrations to South America, from Italy, western and eastern European countries, and some human groups coming from Asia.

    Disregarding the religious use of fungi among pre-Columbian cultures, we only mention data about human pathologic mycoses traced back to Incas (Perú, Bolivia, Northern Argentina and Chile, Ecuador and Southern Colombia); Chibchas (Northern and Central Colombia), Mapuches (Chile), and so forth. For example, facts and information recovered by the Spanish 'cronista' Fray Diego Durán, described the use of several fungi in cosmetic and topical treatments of some skin diseases (3). G. San Blas in Medical Mycology summarized complementary to these data on fungi uses and consumption in the pre-Hispanic world collected by R. G. Wasson and L. Knautt in 2000 (1).

Source: Proceedings of the III Latin American Mycological Congress (1999) (21) (abridged)

Source: Proceedings of the III Latin American Mycological Congress (1999) (21)

    It is worth to emphasize that P. brasiliensis has its exclusive reservoir in South America, and its seems that both lobomycosis and tinea imbricata might have been present among South American indians before Columbus travels.

Teaching, Researching And Training On Mycology In South America

    Teaching, researching and training professionals in mycologic laboratory diagnoses have been led by several University Research Centers within most important high educational level universities in some countries in south America. In 1924, Floriano Paulo de Almeida began his outstanding contribution to study paracoccidioidomycosis in Brazil. Souza Campos and Almeida created the Center of Mycology in the School of Medicine at the University of São Paulo, as described by Lacaz in his manuscript, History of Medical Mycology in Brazil (1999). Floriano de Almeida was the founder of mycologic studies at the University of São Paulo. E. Souza Campos, professor of Microbiology and Immunology. Professor Carlos Da Silva Lacaz succeeded him. Dr. Lacaz undoubtedly represents one of the main leaders of the academic development of Medical Mycology in Brazil and in the Americas. For example, Fava-Netto developed and standardized complement fixation reaction techniques applied to diagnosis and cure control of paracoccidioidomycosis. Lacaz was the master of many relevant foreign students, among whom we dare to mention G. Volcán, E. Belfort, J. A. Serrano, Celina Araujo de Pérez, and S. Urdaneta, García Jover, Nicolle and F. Yegres, M. Pérez de Blanco (from Venezuela), among many other postdoctoral fellows who came from several South American countries (data from Lacaz's unpublished paper, 1999).

    By the early XX century, South American studies on Mycology were strongly influenced and oriented by North American, French, Italian, and German dermatologists and pathologists. Many Venezuelan and Brazilian professionals were postgraduate students in several European Universities by the late XIX and early XX centuries. For example, Pablo Guerra, José G. Hernández, H. Campíns (from Venezuela); A. De Arêa Leão, and O. Fonseca (from Brazil) were trained in European Medical Schools. On the other hand, the American professor S. Taylor Darling, who had discovered the classic histoplasmosis in Panama in 1905, was a visiting professor and lecturer at the School of Hygiene, in São Paulo during the first decades of the XX century. Also the French professor Emile Brumpt, author of 'Précis de Parasitology Medicale', was a lecturer at the School of Medicine (São Paulo) between 1913-1914. He classified the etiologic agent of chromomycosis (Hormodendrum pedrosoi, later assigned to genus Fonsecae, created by P. Negroni, in 1936). Finally, Antonio Carinii, Italian biologist, published pioneer studies on South American blastomycosis in 1910, and in 1912 he discovered the cystic clinical form of a new fungi later identified as Pneumocystis carinii, which in the 1990's became one of the most relevant emergent mycoses associated to AIDS (data from Lacaz's unpublished paper, 1999).

    So far, we have been unable to gather any exhaustive information about Mycology and related studies and research in other South American countries. Excellent summary of contributed papers to international meetings from 1979 are found in the San Blas' paper (1). Below, we will comment some relevant papers and international activities of the Latin American Society of Mycologists .

    In Argentina, P. Negroni and R. Negroni et al published several pioneer papers on mycosis (4), South American and coccidioidomycosis blastomycosis (5-7), Paracoccidioides brasiliensis (8), fungal infections (9), treatment of chronic pulmonary aspergillosis with itraconazole (10), Recently (1999), R. Negroni emphasizes the role of emergent mycoses among HIV positive people (11). Bianchi and Negroni (1992) compared two tests for detecting fungemia in AIDS (12). Other Argentinian mycologists are D.B.M. Zapata, who developed research on mycologic aspects of mycotoxins (13); H. Rubinstein et al, on cryptococcosis (14), and A. Krolewiecki et al on pulmonary nocardiosis among AIDS patients (15).

    In Colombia, a preeminent mycologist is Dr. Ángela Restrepo who has published several papers on paracoccidioidosis, as a reappraisal of its microscopical appearance of mycelia phase (16); estrogens role in the inhibition of mycelium to yeast transformation in P. brasiliensis (17), the 'puzzle' about its 'ecology puzzle' (18, 19). She also summarized data on a general review on paracoccidioidomycosis (20).

    In the last years a great growth on research and teaching medical mycology have been a product of the Asociación Latinoamericana de Micología (ALM). This association is a scientific organization that gathers outstanding specialists in different aspects of the mycological sciences from Latin America and other countries. It was founded when the Fifth Latin American Congress of Botany was held in Havana (Cuba), June 24th to 29th, 1990, under the leadership of Dr. Gastón Guzmán (México). Its by-laws were approved in the Second Latin American Congress of Mycology (October 1996). Currently the ALM gathers about 400 scientists from most Latin America countries. ALM's main subjects of interest cover a variety of fungal topics: taxonomy, ecology, industrial mycology, biotechnology, phytopathology, food mycology, mycorrhiza, biochemistry and molecular biology, physiology, genetics, medical and veterinary mycology, clinical aspects, therapeutics… Mycologists are invited to participate in scientific discussions and exchanges through ALM's electronic list ALM-1@ivic.ve, and to visit the web page http://bragg.ivic.ve/Ivic/ALM/Mycology.html.

    The third Latin American Congress of Mycology was held in August-September 1999 in Caracas (Venezuela). Table 1 summarizes its abstracts by subjects; and Table 2, its abstracts by countries. Table 1 shows that 68 out of 343 papers dealt with medical mycology, which is our subject of interest (21). The San Blas' paper 'from magic to science… (1) describes the modern trends in medical mycological research and milestones in Latin American mycology since 1979. She made praise on the rocketing role of women in the development of Mycology in Latin America (1).

    From the three international congresses and other sources of data, we were able to obtain information on the following areas: (a) cutaneous, nail, ocular, hair and ear mycoses, (b) deep localized mycoses, (c) deep systemic mycoses, and (d) opportunistic emerging mycoses.

    The Latin American Group of Mycologic Research devoted to the study of P. brasiliensis gathered in seven Latin American meetings: four in Brazil and the other three in Antioquia (Colombia), Caracas (Venezuela), and Buenos Aires (Argentina), respectively. The main contributions of this group of mycologists have been on cell and biomolecular biology, clinical diagnosis, pathology, and laboratory diagnoses on paracoccidioidomycosis.

    In 1982, G. Del Negro, C. Da Silva Lacaz, and A. M. Fiorillo published a book on Paracoccidioidomycosis in South America. This book provides an excellent review on the subject including many Brazilian investigators' papers (22).

Papers on Cutaneous Mycoses Published in South America (1985-1999)

    In Argentina G. Davel et al (in 1999) carried out a multicentric study on cutaneous mycoses (23).

    In Brazil, Zaror et al published series of cases of otomycosis in 1990 (24), L. D. Minelli & J. Minelli wrote a review on superficial mycoses (25), H. Gonzalves et al (26) and K. Purim et al reported cases of tinea nigra palmaris (27); B. Trope et al 1992 published a bibliographic review on tinea versicolor (28); A de Brito in 1992 gathered the frequency of new cases of onychomycosis in Pará (1980-1990) (29); J. O. Lopes et al in 1994 reported the first case of human infection by Trychophyton vanbreuseghemi in Brazil (30); O. E. Oliveira Lima et al 1999 gathered frequency of cases of dermatophytoses in Paraíba (31); E. A. Menezes et al described (in 1999) C. neoformans meningitis associated to HIV positive patients in Fortaleza (32); B.C. Zoppas et al, in 1995, conducted a survey for epidemic fungal infectious in Caixas do Sul (33).

    In Colombia, L. Jouffroy, in 1989, wrote a paper on cutaneous mycoses (34), and H. Vélez, in 1990, wrote another one on interdigital non-dermatophytic fungi (35).

    In Chile, MC Díaz et al (36), E. Piontelli-Laforet (37) and L. Zaror, et al (38) published papers on superficial mycosis in several Chilean communities.

    In Perú, V. Bejar et al, in 1991, summarized some aspects of the etiology of dermatomycosis mycoses in Lima (39), Cajavilca et al, in 1999, published a series of 122 cases among dermatology out patients in Lima (40).

    A summary comment on superficial mycoses is that Trichophyton rubrum is the most common etiologic agent of dermatophytoses in South America; Microsporum canis, and some Trichophyton sp. are the most common agents in tinea capitis; Piedra hortai and Piedra blanca are the most frequent agents of hair mycoses. Finally, Candida albicans is the most common agent for cutaneous mycoses (41-43).

Selected Papers on Deep Localized Mycoses in South America (1991-1999)

    In Argentina, A. Luque et al, in 1991(44) presented a case of mycetoma due to Fusarium solani, diagnosis made by study of secretions and biopsies. R. Negroni published two papers on clinical aspects and diagnosis of mycetoma and deep mycoses (45-46).

    In Brazil, A. C. P. Mapurunga et al, in 1990 (47) published a series of 8 cases of deep mycoses in Ceará, and several others on paracoccidioidomycosis, chromomycosis, histoplasmosis, zygomycosis and mycetoma. Also Mapurunga et al, in 1991, reviewed a decade (1979-1989) a series of cases of sporotrichosis, paracoccidioidomycosis, chromomycosis, and lobomycosis (48).

    L. A. Machado et al in 1992, in São Paulo, described two cases of black-grain eumycetoma due to M. grisea (49). Finally, D. Silva et al, in 1990, described a rare case of granulomatous form of lobomycosis (50).

    In Colombia, Cardona-Castro and Agudelo-Flórez developed a chromoblastomycosis model in immunocompetent mice. This model may be suitable for use in experimental studies of chromoblastomycosis (51).

Selected Papers On Opportunistic Mycotic Infections In South America (1990-1999)

    Most opportunistic mycoses in South America are currently related to patients with AIDS or with other pathologies among patients treated with chemotherapy or with immunosuppressant drugs, used to improve cancer or to treat collagen diseases. Mycoses in such groups of patients are emerging infections among immunocompromised patients with or without AIDS. Let's review some indexed reports.

    In Argentina, R. Negroni and P. E. Bonvehi, in 1990, reported the efficacy of itraconazole to treat semi-invasive aspergillosis (52). N. Jacob et al, in 1997, reported cases of phacohypomycosis and mucormycosis among patients who had been recipient of cadaverous kidney transplants (53).

    In Brazil, A. T. Londero and D. V. Pereira, in 1990, stressed the association of opportunistic fungal systemic mycoses to lung diseases (54); and S. A. Marques et al, in 1996, emphasized on opportunistic mycoses and opportunistic behavior within patients from Brazil (55).

    In Chile, M. T. Lobos-M., in 1995, reviewed the emerging pathogen opportunistic fungi among hospital groups (56).

    In French Guiana, in 1999, an abstract by C. Aznar gathered data on opportunist mycoses in that country: Fusarium, Penicillium, Curvularia, and Pecilomyces… The author stressed that the common immunosuppression underlying cause of these emerging syndromes was chemotherapy (57).

    In Perú, A. Urcia et al, in 1999, reported a case of histoplasmosis in a patient with cancer (58); and P. Bengoa, in 1998, reported 3 immunosuppressed patients with deep mycoses, especially on aspergillosis and cryptococcosis meningea (59).

Selected Papers on Systemic Mycoses in South America (1990-1999)

    In Argentina, R. Negroni et al, in 1994 gathered a series of cases of progressive histoplasmosis in a hospital in Buenos Aires, Argentina (60).

    In Brazil, R. Rozembaum et al, in 1992, published a series of 83 patients with cryptococcosis. The authors stressed that those patients with and without AIDS were associated to different strain varieties of C. neoformans (61). O. M. C. Magalhâes et al, in 1995, reported paracoccidioidomycosis in several respiratory patients and contrasted its frequency with the emerging tuberculosis (62). A. T. Londero, et al, in 1997, critically reviewed current frequency of paracoccidioidomycosis in Brazilian children (63).

    In Chile, D. Oddó-B and M. Thompson, in 1991, described pathological and paraclinical diagnosis of pulmonary mycoses (64). S. Sammann-B et al, in 1994, published interesting results of an ecological-epidemiologic study on frequency of C. neoformans in hospital areas in metropolitan Santiago (Chile). The clinical syndromes observed were associated to Cryptococcus neoformans (San Felipe) Vuillemin (65).

     In Colombia, E. Castañeda, in 1993, published data on laboratory methods to diagnose pulmonary mycoses as associated to cryptococcosis (66); M. Rincón-Stella, in 1989 (67) reported 138 cases of paracoccidioidomycosis in Santander (67); A. Tobón et al, in 1996, reported 9 cases of paracoccidioidomycosis and other systemic mycoses in children (68).

    In Perú, J. Casquero et al, in 1999, reported 6 cases of paracoccidioidomycosis in a children hospital in Lima, Perú (69). D. L. Cancio et al found and identified 21 strains of Cryptococcus neoformans in several groups of patients in Lima (70).

Pioneer Milestones of Medical Contributions to Mycology in South America

    Finally, in order to give an overview of pioneer works on mycoses in South America, we built up Table 3. This table epitomizes, in a chronological order, the main milestones on the development of human mycoses knowledge in South America (71-90).

    We expect each reader can follow this summary as a quick guide to have a comprehensive idea of the pioneer works carried out to improve mycologic knowledge in South America (including Venezuela). We apologize the readers for not including the missing data.

    Relevant data on Human Mycoses in Venezuela is the subject of other contribution in Revista de la Sociedad Venezolana de Microbiología.

Acknowledgements

    We acknowledge Dr. P. Venugopal (India) her critical comments to improve editing of this paper. Ana Uzcátegui de Camargo, Secretary of Lab-MICE, carefully typed manuscript several times until this updated manuscript.

Alejandro Posadas	Carlos da Silva Lacaz
(From left to right) Rodo Wanke, Carlos da Silva Lacaz and A.T. Londero.

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