Review on human mycoses in Venezuela

Darío Novoa-Montero, MD, PhD* y José A. Serrano, MD**

* Universidad de Los Andes, Facultad de Medicina, Unidad de Medicina Interna, Sección de Investigación, Laboratorio Multidisciplinario de Investigación Clínico-Epidemiológica (Lab-MICE).
** Universidad de Los Andes, Facultad de Medicina, Departamento de Patología, Unidad de Ultraestructura y de Estudio Multidisciplinario de Actinomicetales Patógenos del Hombre y del Suelo.

Note: This review is an update version of the conference "Human Mycoses in Venezuela". Abstract Book.
I International Symposium on Mycoses in the New Millenium- Challenges & Strategies. Society for Indian Human and Animal Mycologists. February 9th-11th, 2000.

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

Human Cutaneous and Superficial Mycoses in Venezuela

Venezuela is a northern South American country set in the half north of the intertropical zone, in the so-called low latitudes. Its geographical position is between 0°45' and 12°11'46" (North latitude), and between 59°48' and 73°11'49" (West longitude). This country has tropical and subtropical climates. Most cases of human mycoses reported have been found in the States of Lara, Falcón, Zulia, Yaracuy and Carabobo. The State of Lara has been nicknamed the 'Eden of mycoses in Venezuela' (1). Altogether these five states may add up about 70% of the total cases of mycoses reported in Venezuela.

The current importance of the role of cutaneous and superficial mycoses in Venezuela (and in the world) stems on their emergent morbidity among selected groups who are engaged to antibiotic or corticosteroid therapies, women using oral contraceptives or patients using immunosuppressive drugs. In addition, the audiovisual (TV) adds suggesting a 'liberal' not medically prescribed use of antimycotic ointments, sprays, vaginal suppositories or tablets have notably contributed to increase the recurrence of human dermatophytoses and candidiasis infections, specially among patients with diabetes, hormonal disorders or obesity. Other risk factors for incidence and prevalence of human cutaneous mycoses infections in communities are the professional use of rubber and leader shoes, boots and thick clothes. According Albornoz (2), the public health impact of dermatomycoses has been the appearance of outbreaks in schools, platoons of soldiers, sport teams, and so forth.

Albornoz emphasizes the following facts: (a) the statistical data gathered by the Venezuela Ministry of Health are an overestimation of the 'true' prevalence of clinical mycoses (morbidity) since the final mycological laboratory diagnosis has usually been missing; (b) therefore, diagnoses as a whole have been clinically based, and only partially confirmed by mycological tests. In addition, not reported cases and groups of people with mycoses who do not ask for medical assistance, may produce an underestimation of the actual frequency of superficial mycoses in Venezuela (2).

Table 1, summarizes data on reported cases of cutaneous mycoses in Venezuela from 1984 to 1997. This table abridges a sequential series of tables published in the Boletín Informativo- Micosis en Venezuela, numbers 1 to 32(3). Between 1984 and 1997, Mycology Groups led by Albornoz pointed out that they had only confirmed about 57.7% (range 51.4% to 66.5%) mycological diagnoses out of the total reported clinical diagnoses. It might mean that about 6 out of 10 clinically suspected cases of cutaneous my coses among general Venezuelan population might suffer 'true' mycotic infections. Up to now the following eight cutaneous or superficial mycoses have been reported in Venezuela: dermatophytoses, candidiasis, pityriasis, otomy cosis, onichomycosis, ocular mycosis, tinea nigra, and piedra.

Source: Boletín Informativo- Las Micosis en Venezuela (3).
Table 1. Percent of mycologically confirmed diagnoses of clinically diagnosed cutaneous mycoses in Venezuela (1984-1997).

A summary of reported cases by the main groups of mycologists in Venezuela between 1984 and 1997 are displayed on Table 2. Fifty seven percent were dermatomycoses; 25 percent, pityriasis; 19 percent, candidiasis; and only about 2 percent gather otomycosis, onychomycosis, tinea and piedra.

Der: Dermatophytosis; Can: Candidiasis; Pit: Pityriasis; Oto: Otomycosis; Ony: Onycomycosis; Tin: Tinea nigra; Pie: Piedra.
Source: Working Groups on Medical Mycology. Boletín Informativo- Las Micosis en Venezuela, 1-32 (3). ]]> Table 2. Number of reported cases of human cutaneous mycotic infections by groups of work by geographical areas and type of mycoses. All Venezuela (1984-1997).

Relevant Papers on Human Systemic and Localized Deep Mycoses in Venezuela

Introduction

Table 3 displays a summary of reported cases of the fourteen human types of deep and localized mycoses published by several groups of researchers in Venezuela (1984-1997). We categorize these mycoses in four groups:

(1) Relatively common endemic mycotic diseases: paracoccidioidosis, histoplasmosis, chromomycosis, candidiasis and sporotrichosis, which add up 89.5%.

(2) Endemic mycotic infections but clinically less common diseases: cryptococcosis, coccidioidomycosis and eumycetomas, which add up 6.2%.

(3) Opportunistic mycotic diseases, which appear in patients suffering diabetes, cancer, or being treated with immunossuppressors, receiving long lasting venous perfusions (specially in intensive care units or organ transplants centers). Also opportunistic mycoses are associated to AIDS. Most common opportunistic mycoses are: aspergillosis, hypomycosis, zygomycosis, fusarium, and torulopsis, systemic candidiasis (not included in Table 2), wich add up about 4.3%.

(4) Very rare reported deep mycoses infections are rhinosporidiosis, and lobomycosis (not included in Table 3).

The above categorized human mycoses can be regrouped as follows:

(1) Systemic deep mycoses as shown in Map 1 are: (a) histoplasmosis, (b) paracoccidioidomycosis, (c) aspergillosis, (d) cryptococcosis, and (e) coccidioidomycosis (2).

(3) Opportunistic mycoses: (a) aspergillosis, (b) candidiasis, (c) torulosis, (d) hypomycosis, (e) zygomycosis, (f) mucormycosis, and (g) fusarium. These opportunistic mycoses can produce either localized or deep mycoses, and they have eventually been published as case reports (2).

The etiologic agent of chromomycosis, Cladosporium carrionii, is found in the dry regions with xerophytic vegetation (States of Falcón, Lara and Zulia). Histoplasmosis (Histoplasma capsulatum), paracoccidioidosis (Paracoccidioides brasiliensis) and cryptococcosis (Cryptococcus neoformans) are found in the subtropical and templates Venezuelan regions as the Andes mountain system (States of Táchira, Mérida and Trujillo), Sierra de San Luis (States of Falcón and Lara), Cordillera de la Costa (States of Carabobo, Aragua, Miranda, Distrito Federal, Anzoátegui, Sucre, and Monagas), and Macizo Guayanés (State of Bolívar).

Par: Paracocidioidomycosis; His: Histoplasmosis; Cry: Cryptococcosis; Coc: Coccidioidomycosis;Asp: Aspergillosis; Muc: Mucormycosis; Eum: Eumycetoma; Zyg: Zygomycosis: Chr: Chromomycosis; ]]> Spo: Sporotrichosis; Can: Candidiasis; Hyp: Hypomycosis; Tor: Torulopsis; Fus: Fusarium. Source: Working Groups on Medical Mycology. Boletín Informativo- Las Micosis en Venezuela, 1-32 (3).
Table 3. Summary of reported cases of deep human mycotic infections by working F research, geographical area and type of mycoses. All Venezuela (1984-1997).

Paracoccidioidomycosis (ICD-9 116.1; ICD-10 B41)

The control of Communicable Diseases Manual (CCDM) defines paracoccidioidomycosis as "a serious and at times fatal chronic (also known as adult type) mycosis characterized by patchy pulmonary infiltrates and/or ulcerative lesions of the mucosa (oral, nasal, GI) and of the skin. Lymphadenopathy is frequent. In disseminated cases all viscera may be affected; adrenal glands are especially susceptible. The juvenile (acute form), which is less common, is characterized by reticuloendothelial system involvement and bone marrow dysfunction" (4).

Pioneer studies on paracoccidioidomycosis (South American blastomicosis, paracoccidioidal granuloma) in Venezuela were carried by O'Daly (5). Reports of cases were published by D. R. Iriarte & C. Rodríguez (6), D. R. Iriarte (7), D. Guerra (8), A. Celis-Pé rez (9), A. Angulo-Ortega (10), J. Barros-Saint Pasteur (11), H. Benaím-Pinto (12), J. Baldó (13), F. Moncada-Reyes et al (14), and R. Avendaño-Monzón (15). Studies on pathology of paracoccidioidomycosis have been published by Mendelovici et al on ecology (16), Salfelder et al focused on animal model (17) and on reviews or chapters in books (18-20).

From 1993 to 2000 the following papers were indexed:

o G. San Blas, in 1993, published a review on Paracoccidioides brasiliensis, as the causal agent of a systemic mycosis highly prevalent in Latin America (Brazil, Colombia, Venezuela and Argentina). She summarizes the known clinical syndromes, pathological methods of diagnosis, immunology aspects (serological, humoral and cellular immunity and HLA antigen). Also agent virulence, antibiotic therapy, laboratory methods, and biochemical aspects of this fungus were included (21).

o Due to the endemic character of paracoccidioidosis in South America, multidisciplinary teams of researchers have gathered seven international meetings (three in Brazil, and the remaining in Colombia, Venezuela, Argentina, and Uruguay) (22).

o M. B. de Albornoz & R. Albornoz carried out an epidemiologic survey on paracoccocidioidosis tests looking for sensitivity of intradermo reaction results among groups of people from endemic area in Venezuela (23).

Histoplasmosis (American histoplasmosis) (ICD-9 115.0; ICD-10 B39.4)

Let's refer only to the American histoplasmosis in this paper. In Venezuela, H. Campíns wrote two papers on histoplasmosis in 1953 (24, 25). The pioneer investigator on ecology of histoplasmosis, C. Capretti et al in 1963 isolated H. capsulatum (26). Salfelder continued the ecologic search of H. capsulatum in Mérida 1966 (27). Clinical and histopathologic descriptions of histoplasmosis were published by Salfelder et al between 1960 and 1967 (28-48). Experimental models were carried out by Salfelder et al in chickens (49), in mice (50-52), in hamsters (53-57), and dogs (58, 59). Books and chapters in books by Salfelder et al were published on clinical and histopathologic aspects (60, 61), and in atlas textbooks (62, 63) about histoplasmosis.

D. Borelli isolated H. capsulatum in Caracas (1957)(64), and Montemayor et al isolated it from 'Cavernas del Peñón' (Miranda State) in 1958(65), and Ajello et al, from Cueva del Guácharo (State of Monagas) also in 1960(66). Finally, M. Albornoz gathered data on specific skin sensitivity (intradermo reaction) in Paracotos (State of Miranda in 1971) (23). Among others, Angulo & Pollak published data on biopsies and autopsies on deep mycoses in 1990(67) and H Vargas-Montiel, on quantitative immunodiffusion techniques for monitoring deep mycoses in 1985 (68).

Coccidioidomycosis (Valley fever, San Joaquín fever, Desert fever, Desert rheumatism, Coccidioidal granuloma, Posadas disease) (ICD-9 114; ICD-10 B38).

The CCD Manual defines coccidioidomycosis as, "A deep mycosis that generally begins as a respiratory infection. The primary infection may be entirely asymptomatic or resemble an acute influenzal illness with fever, chills, cough and (rarely) pleuritic pain. About one fifth of clinically recognized cases (an estimated 5% of all primary infections) develop erythema nodosum, most frequently in Caucasian females and rarest in African-American males. Primary infection may heal completely without detectable residuals; may leave fibrosis, a pulmonary nodule that may or may not have calcified areas; leave a persistent thin-walled cavity or most rarely may progress to the disseminated form of the disease" (4).

In Venezuela, H. Campíns et al pub lished the first cases of coccidioidomycosis in 1949(69-70). Campins recognized coccidioidomycosis to be a public health problem in geographical areas where Coccidioides immitis is prevalent in the xerophytic and dry ecologic system in Western Venezuela (23). Zirit et al described an outbreak of coccidioidomycosis in Falcón State in 1959(72). G. Tapia isolated C. immitis from Venezuelan soils (Caracas) in 1969 (73). M. A. Quintero et al, in 1987, carried out a descriptive epidemiologic study in Pueblo Nuevo, Falcón State (74).

M. B. de Albornoz published a comprehensive review including definition, epidemiology (ecology), pathogenesis, clinical forms, laboratory diagnosis, pathology, and treatment updated up to 1996 (2).

The potential importance of coccidioidomycosis associated to several emergent syndromes was emphasized by M. Dolande et al in 1999, based on a series of cases (1994-1998). Looking for immunodiagnosis of deep mycoses among AIDS patients, they found that 64% were positive for histoplasmosis, but only 27% were HIV-positive for coccidioidomycosis (75). Further comments on AIDS associated mycologic syndromes will be made below.

Sporotrichosis (ICD-9 117.1; ICD-10 B14)

The CCD Manual defines sporotrichosis as: "A fungal disease, usually of the skin, often of an extremity, which begins as a nodule. As the nodule grows, lymphatics draining the area become firm and cord-like and form a series of nodules, which in turn may soften and ulcerate. Osteoarticular, pulmonary and disseminated multifocal infections are rare. Fatalities are uncommon. Laboratory confirmation is made by culture of a biopsy, pus or exudate. Organisms are rarely visualized by direct smear. Biopsies tissue should be examined with fungal stains" (4).

In addition, L. Aristimuño and Y. López described the geographical distribution of S. schenckii and suggested that its mycelial form is able to be adapted to different ecological conditions, being the most important requirement for its growth the high environmental humidity (83). Also L. Aristimuño and Y. López surveyed a rural population applying the sporotrichina intradermal reaction and found 8.5% seropositive prevalence of infection among asymptomatic to clinical sporotrichosis. Among seropositive people, two-third have had some kind of clinical syndromes (83). The authors emphasize that one of the main risk factors to become positive to sporotrichosis infection is the agricultural occupation (83). M. Mendoza et al in 1992, using acrilamide gel and immunoblot techniques further characterized the metabolic antigen of filamentose form of S. schenckii (84). M. B. C. de Albornoz reported 87 cases of sporotrichosis in children (1956-1996) stressing that 37/87 (43.5%) appears like the cutaneous limphangitic form; 33/87 (38%) were localized nodules, and the other 17/87 (19.5%) were lymphatic form (cordon-like form)(84). M. B. de Albornoz concludes that sporotrichosis is the most frequent localized deep mycoses infection in Venezuelan childrens (85).

Chromomycosis (Chromoblastomycosis, Dermatitis verrucosa) (ICD-9 117.2; ICD-10 B43)

The CCCD Manual defines chromomycosis as: "A chronic spreading mycosis of the skin and subcutaneous tissues, usually of a lower extremity. Progression to contiguous tissues is slow, over a period of years, with eventual large verrucous or even cauliflower-like masses and lymphatic stasis. Rarely a cause of death. Microscopic examination of scrapings or biopsies from lesions reveals characteristic large, brown, thick walled, rounded cells that divide by fission in two planes. Confirmation of the diagnosis should be made by biopsy and attempted cultures of the fungus" (4).

O'Daly was the pioneer pathologist who observed the first cases of chromomycosis in Venezuela in 1937 and 1938, published in 1943 (86). He isolated a not yet classified etiologic agent from soils of dry geographic zones in 1943. Lately this agent was classified by Trejos as Cladosporium carrionii in 1954 (87). Fonsecaea pedrosoi is the etiologic agent of chromycosis in other climatic areas. Richard Yegres et al, until 1992, had diagnosed 397 cases of chromomycosis in the Mycology Unit of Falcón State(88). The 'prevalence' of infection was 16/1000 persons in endemic areas (more frequent in adults and clustered in families) (88). In 1996, Pérez-Blanco et al published the first case of chromomycosis due to Rhinocladiella aquaspersa in Venezuela (89). Yegres et al's main contribution to improve the knowledge on endemic chromomycosis in Venezuela may be the search for epidemiologic aspects, which include occupational infection in goat shepherds (90), and the isolation of strains from xerophytic environments (91-93).

Mycetomas (ICD-9 039; ICD-10 B47)

The CCD Manual defines mycetoma as: "A clinical syndrome caused by a variety of aerobic actinomycetes (bacteria) and eumycetes (fungi), characterized by swelling and suppuration of subcutaneous tissues and formation of sinus tracts with visible granules in the pus draining from the sinus tracts. Lesions are usually on the foot or lower leg, sometimes on the hand, shoulder and back, and rarely at other sites. Mycetoma may be difficult to distinguish from chronic osteomyelitis and botryomycosis, the latter been a clinically and pathologically similar entity caused by a variety of bacteria, including staphylococci and gram-negative bacteria. Specific diagnosis depend on visualizing the granules in fresh preparation or histologic slides and isolation fungus in culture" (4).

Eumycetoma (Maduromycosis, Madura foot) (ICD-9 117.4; ICD-10 B47.0)

Eumycetoma is caused by Madurella mycetomatis, M. grisea, Pseudoallescheria (Petriellidium) boydii, Scedosporium (Monosporium) apiospermum, Exophiala (Philalophora) jeanselmei, Acremonium (Cephalosporium) recifei, Acremonium falciforme, Leptosphaeria senegalensis. Neotestudina rosatii, Pyrenochaeta romeroi, or several other species (4).

In Venezuela, mycetomas are either produced by 'true' fungi (eumycetomas) or by bacteriae actinomycetes (actinomycetomas). The most frequent etiologic eumycetoma agents in Venezuela are Madurella grisea, Pyrenochaeta mackinonnii, and P. romeroi (94-96). A summary of etiologic agents of eumycetoma in the State of Lara is displayed in Table 4 (95).

Actinomadura madurae is the most common agent of actinomycetoma in Venezuela, followed by Nocardia brasiliensis, and N. asteroides. Table 5 displays the geographical distribution of reported cases of actinomycetoma by states in Venezuela, by main etiologic agents In the State of Lara were reported 35/59 (59%) and Actinomadura 17/59 (37%) of the reported cases in Venezuela (94). Novoa-Montero and Serrano inference is that either eu or actinomycetomas are not a public health problem in Venezuela (97). This fungi human mycoses (eumycetomas) produce endemic infection, but prevalence of clinical cases appears to be very low. Mycetomas are associated to low and very low socioeconomic conditions, especially among agriculture and field workers in Falcón, Lara and Zulia states, where xerophytic and dry regions are extensive (98). The ratio between prevalence of infection and prevalence of clinical cases should be a matter of further research in order to also define how (pathogenic) and why (other risk factors as covariates) only quite a few people became clinically sick in rural communities where prevalence of seropositivity is high (97).

Source: Serrano, J. A. (95) (updated 2000).
Table 5. Distribution of clinical cases of Actinomicetoma reported in Venezuela, by States of (1976-1998).

Candidiasis (ICD-9 112; ICD-10 B37)

The CCD Manual defines candidiasis as: "A mycosis usually confined to the superficial layers of skin or mucous membranes, that present clinically as oral thrush, intertrigo, vulvovaginitis, paronychia or onychomycosis. Ulcers or pseudo-membranes may be formed in the esophagus, stomach or intestine. Candidemia most commonly arises from intravascular catheters and may produce lesions in many organs, such as kidney, spleen, lung, liver, eye, meninges, brain and native cardiac valves or around prosthetic cardiac valves" (4).

In Venezuela, candidiasis, candidosis, candidomycosis, previously known an moniliasis, was firstly reported in 1921 by E. González associated to bronchial moniliasis (99). P. Guerra, in 1935, wrote his pioneer dissertation on the rol of pathogenic yeast on dermatology (100). He and M. Langeron published a description on C. stellatoidea in 1938 (101), and P. Guerra described "erosio interdigitalis" by Monilia albicans and clinically associated to eritrasma (102).

M. Feo carried out comprehensive studies on non-pathogenic and pathogenic yeasts in Venezuela (103, 104). S. Rodulfo and M. Mendoza clarified that C.albicans most common infection is associated to serotype A candidiasis (69%), while serotype B represents (31%) of infections confirmed by biopsy. Candidiasis serotype A is frequent as an emergent infection in patients with AIDS (105).

Lobo's Disease (Lobomycosis) (ICD-9; ICD-10 B48.0)

The CCD-Manual describes "Keloidal blastomycosis (Lobo disease), a disease with only skin involvement formerly confused with paracoccidioido mycosis, is caused by Loboi loboi, a fungus known only in its tissue form and not yet grown in culture" (4). Taborda et al renamed Lobo's Disease agent as Lacazia loboi to pay tribute to Carlos Da Silva Lacaz.

Rhinosporidiosis (ICD-9 117.0; ICD-10 B48.1)

Rhinosporidiosis (Rhinosporidium seeberii) (112,113) is a granulomatous chronic infection, not transmissible man-to-man, characterized by polipoid lesions in man and some quadruped animals, chicks and gees (114). Local infections are mainly oral, nasopharinx, rectal and genital mycoses. Rarely, skin, bronchi and bones (114).

Rhinosporidiosis is endemic in Venezuela. It is mainly acquired when people are working in rice fields in Portuguesa and Barinas States. L. Potenza and A. Celis-Pérez described the first case in 1947 (115). Other case reports stressing conjuntival infection were published R. Sánchez-B. & M. Schargy, in 1947(116) and in 1953 (117). V. Alizo & F. Wenger in 1953 (118), F. Gómez et al in 1962 (119), and F. Gómez in 1966 (120).

E. G. Vogelsang described R. seeberi in an equine infection in Venezuela, in 1955 (121). Sauerteig published a series of 16 cases of rhinosporidiosis in children and young adults in 1985 (122). J. Montarroso observed 20 cases of ocular rhinosporidiosis, K. Brass observed other 10 cases of rhinosporidiosis along of 30 years activity in Carabobo State. Cases described by K.Brass came from Barinas and Portuguesa States in Venezuela (cited by E. Sauerteig, 122).

Oportunistic and Emergent Mycoses Infections in Venezuela

Main mycoses agents usually found worldwide.

Opportunist fungi currently are cosmopolitan infections within which etiologic species differ according to each geographical region. Table 3 displays that opportunistic mycoses infections described in Venezuela have been associated to Zygomycetes sp. (ICD-10 B46.0) and mucormycosis (ICD-10 B46.0; B46.5); Candida sp. (ICD-9 112; ICD-10 B37) which is the most frequently reported; less frequently reported are Aspergillum sp. (ICD-9 117.3; ICD-10 B44), and Fusarium sp.

The following opportunistic infection agents are mainly associated to the so called emergent mycotic syndromes: Cryptococcus neoformans (ICD-9 117.5; ICD-10 B43), Histoplasma capsulatum (ICD-9 115.0; ICD-10 B39.4), Coccidioides immitis (ICD-9 114; ICD-10 B38), Paracoccidioides brasiliensis (ICD-9 116.1; ICD-10 B41), and Pneumocystis carinii (ICD-9 136.3; ICD-10 B59) (4).

Mycotic emergent syndromes are associated to specific underlying diseases, specially to diabetes mellitus, leukosis, lymphomas, drug additions, AIDS, and to whatever other immunosuppressed individuals.

Venezuela is not the exception with respect to epidemics of deep and systemic mycoses associated with the increasing number of AIDS groups of patients, which is rocketing since 1989, when AIDS clearly showed to be a relatively common syndrome in this country.

Fernández and M. Mandells, in 1990, in a series of 490 patients (1988-1989) found 64 patients with emergent mycoses syndromes, among which 43 suffered deep mycoses (histoplasmosis, cryptococcosis, paracoccidioidosis), systemic candidiasis, and doubled infected by cryptococcosis and histoplasmosis (123).

M. Dolande et al, in 1999, checked up 740 immunologic samples analyses confirmed that 265 came from AIDS patients within whom 66 showed to be positive for the following systemic mycoses: 42 for histoplasmosis, 98 for cryptococcosis, 5 for paracoccidioidomycosis, and 1 for coccidioidomyco sis. The 475 samples taken from asymptomatic HIV positive patients appeared to be negative to systemic mycoses (124). Merheb-Guillot et al revised 404 autopsy protocols of immunosuppressed persons (1985-1989) (338 without HIV and, 66 HIV positive). Candida albicans was found in 49.2%, H. capsulatum in 41.3%, and Cryptococcus neoformans in 12.7% among free AIDS-free dead individuals. When AIDS dead individuals were checked up, histoplasmosis proportion was 18.4% (lower than among AIDS free dead), cryptococcosis proportion was 33.3% (higher than among AIDS free ones), meanwhile candidiasis was present in 23.2% (also lower than among AIDS free dead) (125).

I. Peña et al reported a patient biopsy of some Kaposi-like lesions, truly due to Cryptococcus neoformans (126). Santiago et al, in 1998, examined 346 AIDS patients (Central Venezuela); 124 samples (38.8%) had some kind of deep mycoses (C. neoformans, H. capsulatum, P. brasiliensis and C. albicans) (127).

A. Río-Fabra observed that the most frequent opportunist agent worldwide associated to AIDS is Pneumocystis carinii, meanwhile H. capsulatum, which mainly produces pulmonary acute infections in AIDS patients, is most frequent in Venezuela. C. neoformans, P. brasiliensis and C. immitis have been rarely seen among AIDS patients in Venezuela (128).

Relevant Venezuelan Contribution to Drug Treatment of Human Mycoses

The original relevant drug developed in Venezuela aimed to treat mycoses was patented by Apitz-Castro et al in 1987(129), after careful assays following his pioneer communication in 1963(130). This drug has been named 'ajoene' (E,Z,4,5,9 trithiadodeca-1,6,11-thriene 9-oxides) (131). It is an organosulphurate compound, originally obtained from the alcoholic extracts of garlic (130). This drug has both in vivo and in vitro antifungal activity for pathogenic fungi, say cutane ous (131) deep localized human mycoses, chromomycosis (132); paracoccidioidosis (133). Antimycotic effect of ajoene seems to be due to a selective inhibition of phosphatidylcholine biosynthesis in inferior eucaryotes (131).

Historical and Major Contribution of Venezuelan Physicians, Pathologists and Mycologists to Improve Mycology Knowledge.

Table 6 epitomizes the historical and major contributions of Venezuelan physicians, early pathologists and mycologists to consolidate mycology as a scientific discipline in Venezuela. This summary includes data from 1882 to 1999 (134-217).

Table 6. Historical and major contributions of Venezuelan physicians, pathologists and mycologists (1882-1999).

In 1882, D. de-Armas described the first case of tinea tonsurans in Venezuela (134). Turning the XIX century appeared the so called 'Renaissance of the Venezuelan Medicine' The medical leaders of that 'renaissance' were F. A. Rísquez (1856-1941), L. Razetti (1862-1932), José Gregorio Hernández (1864-1919), and J. Santos-Dominici (1869-1954). As a matter of fact, Razetti and Dominici, while being trained in France, conceived a specific proposal to carry out a new approach to develop medical sciences in Venezuela during the beginning of XX Century. This 'renaissance' included, among other objectives which were reached indeed: (a) Foundation of the Hospital Vargas (Caracas, 1891); (b) foundation of the Department of Histology, Pathology Experimental, Physiology and Bacteriology (1891); (c) creation of the Journal Gaceta Médica de Caracas (1893); (d) foundation of the Pasteur Institute of Caracas (1895); and (e) foundation of the Laboratory of the Hospital Vargas (1902) (162).

Based on the activity of the above mentioned institutions, several Venezuelan professionals published reports of clinical cases of mycoses. They were S. Montiel-Pulgar in 1908 (135), M. A. Fonseca (136), R. Rangel in 1909 (137), R. Medina-Jiménez in 1913 (138), R. Pino-Pou in 1917 (139), E. González in 1921(99). B. Jiménez and M. Cuenca in 1923 (140), and E.P. De Bellard in 1924 (141).

J. R. Rísquez (1883-1947) succeeded J. Gregorio Hernández (died in 1919) in the Cátedra de Bacteriología y Parasitología (162). In addition to important investigations on parasitology and bacteriology, he wrote a paper on pie de Madura in 1927 (142). J. R. Rísquez excited his students to carry on research on Venezuelan infectious diseases. Among his undergraduate medical students, L. Briceño-Iragorry and H. Villalobos wrote a paper on Actinomycetoma in 1927 (142).

Del Corral in 1934 (143), and M. Vegas in 1935 (76) reported cases of hair and cutaneous mycoses. Also J. A. O'Daly in 1937 (5) and D. R. Iriarte Rodríguez in 1939 (6) reported cases on deep mycoses.

By 1937, a new medical pioneer, P. Guerra (1903-1944), went back to Venezuela after having been trained as post graduate fellow by Paul Ravaut and M. Langeron in Paris. Guerra and Langeron published the description and identification of Candida guilliermondii (100). They also carried out studies on Candida stellatoidea (101). Guerra was chairman of the Unit of Dermatology and Pathology of the Hospital Vargas in Caracas. His relevant contribution to the study of mycoses in Venezuela is related to pathogenic yeasts (100). He was the founder of the first Venezuelan Laboratory for diagnosis of human mycoses (162). Potenza and Pérez-Celis described the first case of rhinosporidiosis in Venezuela in 1947 (115).

In 1943, Lorenzo de Montemayor assumed as assistant technician of Dr. Guerra. He evolved to become a technologist at the Universidad Central de Venezuela in 1963, and was a post graduate student of J. Mackinnon, in Montevideo (Uruguay) (164). Lately he went to California (USA) to continue his training in mycology. Thereafter, he was named Professor of the Escuela de Bioanálisis (Universidad Central de Venezuela) where he trained many laboratory medical technologists (164). One of Montemayor's paper on mycology was his description of Favus aviari in 1946 (163). Montemayor's main contribution to mycologic studies was to maintain and increase a pathogenic fungi collection in Caracas as well as to improve training and teaching on mycology in Venezuelan Universities (164).

Potenza and Benaím-Pinto described the first case of central nervous system infection by Cryptococcus neoformans (144).

In central western Venezuela, Dr. H. Campíns, dermatologist and mycologist, founded in 1953 the Department of Dermatology at the Hospital Central Antonio María Pineda in Barquisimeto, Lara State. He is a pioneer investigator on deep mycoses, specifically on coccidioidomycosis (69). Campíns trained the first group of dermatologist-mycologists in central western Venezuela, (Segundo Barroeta, María Antonieta Mejía, Ramón Zamora, among others). The Department of Dermatology in Barquisimeto was named after H. Campíns, as a tribute to his memory and acknowledgment to his outstanding activity. Nowadays, the unique Master Degree in Dermatopathology held in Venezuela is sponsored by this department.

By the fifties of the XX Century, the following pioneer mycologists published sound papers. L. Pollak in 1953 on histoplasmosis (145), K. Brass et al, in 1954, on blastomicosis (146), D. Borelli on new pathogenic fungi species 1955 (147-150); and G. Maekelt who developed seroepidemiologyc tests to be applied to diagnose clinical patients and to validate descriptive epidemiologic studies (151, 152).

In Zulia State, J. Hómez-Chacín founded the Department of Dermatology and the Unit of Parasitology and Tropical Medicine at the School of Medicine, Universidad del Zulia, in 1954. In addition, G. Casas-Rincón and J. Hómez-Chacín founded the Section of Medical Mycology in the Department of Microbiology at the same University in 1971. By 1957, a Venezuela Governmental Steering Committee, named Comisión Coordinadora del Estudio Nacional de las Micosis was led by J. I. Baldó. Its objectives were aimed to increase the state of the re search and cumulative knowledge on human mycoses in Venezuela. This committee made a review on the contemporary Venezuelan knowledge on mycoses. A synthesis of this group of mycologists' papers was presented on the IV Congreso Venezolano de Tisiología y Neumonología, Valencia (Ven.) Oct 9-12, 1959. In 1961, Mycopathologia et Mycologia Applicatada (T. Benedek, editor) published its Proceedings (167). Fruits of that Comisión were the First Venezuelan Workshop in Mycology (168), and a monograph, 'Cartilla Micológica' (169). In the sixties of XX Century, in Venezuela, the known cases of mycoses were on histoplasmosis, paracoccidioidomycosis, coccidioidomycosis, blastomicosis, mycetomas, candidasis, cryptococcosis, chromomycosis, sporotrichosis, nocardiosis, actinomycosis, rhinosporidiosis, and cutaneous mycoses (162). This Comisión ceased its activities by 1979 (170).

Other important investigations on mycoses in Venezuela are the papers from the Venezuelan pathologists I. Campo de Aasem on blastomycosis queloidiana (Lobomycosis) in 1957 (107), L. Carbonell on ultrastructure and cytochemistry of deep mycoses agents (153-154, 171), G. de San Blas and F. San made sound contributions on molecular biology of P.brasiliensis and other deep mycoses (21, 133).

M. B. de Albornoz, after her training as a fellow in Mycology at London School of Hygiene and Tropical Medicine, became the leader of a group of mycologists now-a-days spread along Venezuela (Caracas, and the States of Bolívar, Falcón, Monagas, Táchira, Zulia, Barinas, Carabobo, Lara y Sucre) (2). This mycology group of research on mycoses main achievements have been: (a) Standardization of methods for serological, immunological, skin tests…; (b) validation of such methods; (c) application of validated tests for developing community surveys, and to carry out clinical and laboratory tests; (d) promotion and development of multidisciplinary and interdisciplinary groups for diagnosis, research and teaching in Mycology; (e) application of research on Mycology pointing out to solve specific problems or to promote a better public health applications in selected Venezuelan communities (3).

Doctor M. B. de Albornoz's and her group of mycologists have published 32 issues of the Boletín Informativo: Micosis in Venezuela between 1985 and 1998, and it will continue to be published. This 'boletín' has included many aspects of several Venezuelan human mycoses: (a) reports of important cases or several series of cases; (b) laboratory methods on Mycology; (c) descriptive epidemiologic data; (d) therapeutic trials; (e) biographical sketches of relevant Venezuelan mycologists, etc. (3). Dr. Albornoz's team work on editing, publishing and keep-on-going this boletín, supported by their own financial resources and sporadic private pharmaceutical companies subsides, are worth to be though over as the best contemporary academic effort to improve Mycology in Venezuela as a new scientific discipline among the Biology Sciences.

Recently, in 1996, M. B. Albornoz edited a handbook entitled, 'Temas de Micología Médica' (2). This handbook includes the most recent concepts and advances on Medical Mycology. It is an updated handbook, which is very useful to introduce Spanish speaking students and professionals interested on the field of human medical mycology (2). Dr. Albornoz and her team activities on mycology in Venezuela was worth enough to deserve the creation of the Mycologic Section at the Annual Meeting of the Venezuelan Association for the Advancement of Sciences (AsoVAC).

New advances on mycology research sero/and immunodiagnosis of eumycetoma and chromomycosis were the outstanding contributions on immunology and serodiagnoses of eumycetoma and chromoblastomycosis published by H. Romero (1989-1999) (155-157).

In the field of teaching Mycology as an advanced discipline, J. A. Serrano published two papers on ultrastructural and cytochemical aspects of actino of eumycetes and mycetoma (95, 173). In addition, F. Yegres and N. Richard-Yegres have sponsored four post graduate courses on Medical Mycology in the School of Experimental Medicine at the University 'Francisco de Miranda', Coro, Falcón State, between 1994 and 1999. These post graduate courses have been cosponsored by the Venezuelan National Institute of Hygiene. This course involved to be a Master Degree in Medical Mycology in 1999.

Since 1994 D. Novoa-Montero, chronic diseases epidemiologist, has been inviting mycologists to follow a new approach to evolve their researches on deep mycoses. His proposal has been called "multidisciplinary family-case comparison epidemiologic model", which is a practical and effective application of the clinical epidemiology discipline, based on the so called empirical epidemiology. Figure 1 displays Novoa-Montero proposal as a flow chart to carry out productive research on man-to-man transmitted mycoses (and, for extension, some bacterial chronic infections and diseases). This submodel of case-control epidemiologic design has been proposed at several international symposia on Mycology, as in Moscow (Russia), in 1994 (1), in Jabalpur (India) in 1996 (158), in Beijing (China) in 1997 (159), and in Davis (California) at SILCIBIO 2000 (174). Related papers resulting from these symposia have been published in Biotechnology, Russia (1), and in the Journal of Medical Mycology, France (97), and in the Boletín de la Sociedad Venezolana de Microbiología (161).

Textbooks and Monographs on Mycoses or Mycology in Venezuela

We could trace the following books:

(1) Cartilla Micológica. This monograph was edited by Fundación Eugenio Mendoza. It was the first com prehensive review on mycologic published researches in Venezuela up to 1959 (169). It represents one of the most pragmatic work carried out by the 'Comisión Coordinadora del Estudio Nacional de la Mycosis' steered and supervised by J. Baldó (169),

(2) Bibliografía Dermatológica Venezolana. This monograph was edited by the Venezuelan protodermatologist Francisco Kerdel-Vegas. It represents the most comprehensive review on dermatology and superficial and deep localized mycoses in Venezuela, which includes papers, monographs, pamphlets, books and chapters in books, updated by 1996 (175).

(3) Micosis Profundas-Datos Generales y Observaciones en Mérida. This manual, edited by K. Salfelder and T. R. Liscano in 1979, is a guide for undergraduate medical students, and eventually for interested specialists. The book covers diagnosis methods, and histopatologic characteristics of cryptococcosis, blastomycosis, paracoccidioidosis, aspergillosis, basidioidomycosis, etc. (176).

(4) Traité de Mycologie Médicale. This is a classical international textbook on medical mycology, where Dante Borelli is a coauthor with J. Delacrétaz and D. Grigouriu. D. Borelli main contribution in this textbook is related with deep localized and systemic mycoses, some therapeutic aspects to treat several mycoses, and techniques to perform laboratory techniques useful to validate clinical and epidemiologic diagnoses on human mycoses (150).

(5) Micología General. This is a textbook written by C. Casas-Rincón. This book covers general aspects of mycology, and specific aspects on human, animal, vegetal mycotic diseases, or practical and industrial applications of fungi. Moreover, it describes environmental fungi contaminants and laboratory techniques to characterize and diagnose fungi (177).

Contribution of Venezuelan General Physicians, Dermatologists and Pathologists to Mycology

Venezuelan pioneer studies on mycoses without pathologic confirmation.

In 1882, D. de Armas published what appears to be the first report on tinea tonsurans treated with salicylic acid and crushed ice (134). Twenty six-years later, in 1908, S. Montiel-Pulgar reported the first case of actinomycetoma (135). Thereafter, many series of cases of several mycoses were published: M.A. Fonseca in 1909 (136), R. Rangel in 1909 (137), Medina-Jiménez (138), R. Pino-Pou in 1917 (139), E. González in 1921 (99), De Bellard in 1924(141), L. Briceño-Iragorry, R. Rísquez in 1929 (179), and P. del Corral in 1934 (143). Details on each author contribution can be seen in Table 6. The above mentioned professionals were general practitioners, medical doctors, medical technologists… One of the Venezuelan protodermatologists, M. Vegas, in 1935, described the first case of sporotrichosis (76). It is worth emphasizing that none of the above reports of cases were confirmed by pathological methods.

Pioneer studies on human mycoses including both dermatologic and pathologic descriptions.

In 1936, R. Jaffé, the pioneer German Venezuelan pathologist, arrived in Venezuela. Jaffé was the master of the new generation of contemporary Venezuelan pathologists. From then on, the join activities of Venezuelan dermatologists and German pathologists, associated or not with medical practitioners, internists, surgeons, otorrhinolaringolo gists… on one hand; laboratory technicians and technologists, on the other hand, published many relevant contributions which consolidate what we dare to call 'the preconstitutional stage of Mycology in Venezuela'.

The relevant pioneer contributions works of dermatologists on human mycoses were initiated by P. Guerra in 1935 (100-102). His trainee, and later technologist, L. de Montemayor (163) and other dermatologists published several papers, say by H. Campíns in 1949-1956 (24, 25, 69-71), D. Borelli in 1957 (64) and Campo de Aasen in 1959 (107).

D. Borelli, through his tenacious work enhanced and internationally put on the spot the mycologic studies in Venezuela. We consider Borelli to be the founder of Mycology as a new scientific discipline in Venezuela. D. Borelli published highly specialized research (64, 80, 147-149), meanwhile he was teaching and training a lot of new professionals on mycology. He is without question the most outstanding Venezuelan mycologist.

Brief review on the German Pathologists' contributions to mycology knowledge, teaching and training in Venezuela.

The following review on relevant data on German pathologists contributions to Mycology in Venezuela were mainly excerpted from the book 'Patólogos Alemanes en Venezuela' (German Pathologists in Venezuela) 1936-1981(180), and from Dr. Salfelder's personal curriculum, other personal communications, and some indexed papers published after 1981. Lets follow this relevant German pathologists 'pathway'. A summary of their main contributions to Venezuela Mycology is displayed on Table 7

Table 7

R. Jaffé. Although he did not directly published any contribution on mycoses, he was the master of the most relevant Venezuelan new pathologists trained from the late thirties to the fifties in the twenty Century (180).

K. H. Salfelder. If R. Jaffé was the master of Venezuelan new generation of pathologists in Caracas and Northern Central Venezuela, K. Salfelder has been the mentor and the leader of the new generation of pathologists in Western Venezuela. He is a worldwide recognized scientist not only as pathologist but also as a prominent protozoologist and mycologist. K. H. Salfelder engaged the University of the Andes Medical School in 1951 and retired in 1979. Since then, he established the 'Laboratorio de Investigación en Patología'. This laboratory has been maintained by Salfelder, Teresa Reyes de Liscano and others pathologists, who have co-authored most of the 217 papers and contributions up to 2001, among which 112 papers are related to mycoses. Their papers on mycoses can be summarized as follows: (1) Paracoccidioidomycosis: which includes aspects on ecology (16), experimental studies (17), clinical aspects (18-20). (2) Histoplasmosis: which includes aspects on ecology (20), clinical and histologic aspects (29-48), experimental findings (49-59), chapters in books (60-63). (3) Chromomycosis: which includes case reports of acute infection (181-182), and cases of chromomycosis simultaneously developed with other deep mycoses (200). (4) Opportunistic mycoses: which includes papers on aspergillosis (183); on pneumocystosis (184-186, 199); adiasporomycosis (187, 188). (5) North American blastomycosis: which includes aspects on clinical features (200); experimental (190); reviews (191). (6) Cryptococcosis: which includes papers on experimental (192); on ecology (193), (7) Several mycosis: which includes chromomycosis, cryptococcosis, Nocardia, eumycetoma (181); reviews (195). (8) Sporotrichosis: (196, 197), among others (180).

E. Sauerteig. He was coworker and co-author with Salfelder not only on topics of mycoses, but also in other papers on pathology (180). Sauerteig's papers on rhinosporidiosis may be considered his more original contribution (122). He also wrote cryptococcosis (193), candidiosis (193, 198), histoplasmosis (34, 35), sporotrichosis (196, 197), torulopsis (199), and cryptosporidiosis and blastomicosis (201), and aspergillosis (206).

K. Brass. His research, carried out in Valencia (Central Venezuela), was mainly addressed to Chagas' disease (180). His contributions on mycoses were related to cryptococcosis (202), deep mycoses (203), paracoccidioidomycosis (204), histoplasmosis (205), and aspergillosis (206).

G. Doehnert. Son of H. R. Doehnert, graduated at the Universidad de Los Andes (Mérida, Venezuela) and trained in pathology by Dr. K. Salfelder (180). He was co-author of papers on histoplasmosis (34-36), paracoccidioidomycosis (209), several infections (209).

G. Franz. He published a paper on pathologic finding on human systemic mycoses (162). and other on rhyzopus (212).

F. Wenger. German pathologist who, after residing in Ecuador, worked in Maracaibo (Universidad del Zulia) (180) with respect to mycology, he published a paper on rhinosporidiosis (213). Other, on lymphatic paracoccid ioidomycosis (214), deep mycoses (215), actinomycetoma (216), and chromomycosis (217).

Final Remark

Table 7 epitomizes the special contributions of German pathologists to built-up the 'constitutional stage' of mycology studies in Venezuela. The main achievement of German pathologists in Venezuela was to introduce histopathologic characterization, laboratory techniques and demonstration of mycotic agents in patients which final diagnoses were unknown then and there. Their contributions allowed completing final diagnoses of clinical organic pathologies, and to make differential pathological diagnoses among fungi themselves, fungi and bacteria, and fungi and protozoa.

The section 'Development of teaching diagnostic laboratory mycoses Techniques through institutional working groups in Venezuela' described most relevant data on the history of Venezuelan mycologists up to 1998.

In 1981, K. Salfelder and D. Novoa-Montero edited a monograph entitled "Patólogos Alemanes en Venezuela. 1936-1981". (German pathologist in Venezuela. 1936-1981) (180), which is the main source of data for this section of the paper.

Ultimately, Mycology in Venezuela has received the contributions of chemists and biologists G. de San-Blas and F. San-Blas (21, 22); ultrastructural aspects (J. A. Serrano (96), Serrano also published a biomedical-social aspects of eumycetoma (218); biological and mycological aspects (Yegres and Richard-Yegres, 90-93); and serological and immunological studies (H. Romero, 155-157), among other outstanding researchers, some of them included in previous comments (Table 6).

A recent review on historical aspects on the development of the Mycology in Venezuela was published by Briceño-Maaz et al as a 'Breve historia de la micología médica en Venezuela' (219). Finally, on amazing review was wrote down by G. de San Blas, 'A journey through Latin American Medical mycology', where the Venezuelan historical development and relevant papers on mycologic aspects up to 2000 are included (22).

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

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24. Campíns, H. y Shary, M.: Comprobación de las histoplasmosis en Venezuela. Gaceta Médica de Caracas; 61:67-75, 1953.        [ Links ]

25. Campíns, H.; Zubillaga, Z.; Gómez-López, L. and Dorante, M.: An epidemic of histoplasmosis in Venezuela. Am J Trop Med & Hyg.; 5:690-695, 1956.        [ Links ]

26. Capretti, C.; Salfelder, K. y Romero, A.: Histoplasma capsulatum en el suelo de nuestro ambiente. Exámenes micológicos. Mycopath. et Mycol.; 17:55-70, 1963.        [ Links ]

27. Salfelder, K.: Búsqueda de Histoplasma capsulatum en una cueva de La Azulita, Estado. Mérida,. Ediciones de la Corporación de Los Andes, Mérida, Venezuela, 1966.         [ Links ]

28. Salfelder K. Zur Differential diagnose der Histoplasmose. Z. Tropenmed. Parasit.; 11: 453-469, 1960.        [ Links ]

29. Salfelder, K. y Capretti, C.: Primoinfección pulmonar de histoplasmosis en un lactante. Mycopath. 1961; 15:251-257, 1961.        [ Links ]

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31. Salfelder, K.; Romanovich, J.; Liscano, T. R. de und Moncada, F.: Ueber einen fall von Lungenhistoplasmom mi moeglicher infection in italien. Mykosen.; 6:29-34, 1963.        [ Links ]

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