Hostname: page-component-74656f9884-j7cmm Total loading time: 0 Render date: 2026-11-06T22:30:52.576Z Has data issue: false hasContentIssue false
  • English
  • Français

Epidemiological aspects of strongyloidiasis in Brazil

Published online by Cambridge University Press:  03 August 2011

F. M. PAULA  and
J. M. COSTA-CRUZ
F. M. PAULA
Affiliation:
Laboratório de Investigação Médica – LIM/06, Instituto de Medicina Tropical de São Paulo, Universidade de São Paulo, São Paulo, Brazil
J. M. COSTA-CRUZ*
Affiliation:
Laboratório de Diagnóstico de Parasitoses, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Uberlândia, Minas Gerais, Brazil
*
*Corresponding author: Laboratório de Diagnóstico de Parasitoses, Instituto de Ciências Biomédicas, Universidade Federal de Uberlândia, Uberlândia, MG, Brasil. Av. Pará, 1720, 38400-902, Uberlândia, MG, Brazil. Tel: +55 34 3218 2187. Fax. +55 34 3218 2333. E-mail: costacruz@ufu.br
Rights & Permissions [Opens in a new window]

Summary

The objective of this review was to outline an epidemiological profile of Strongyloides stercoralis by parasitological and serological diagnosis in inhabitants, and to associate this profile with different immunosupression situations, in Brazil, over 20 years (1990–2009). The occurrence of S. stercoralis using parasitological methods was 5·5%, being 4·8% in rural and 5·0% in urban areas, characterizing the country as hyperendemic. There was a diversity of techniques used as a diagnostic tool and only 39·1% of the studies presented results based on at least 1 specific method. The occurrence increased with age, being 12·1%, for those over 60 that suggests an epidemiological condition of concern for the elderly population. Of the seroepidemiological studies in the general population the mean positivity in serum samples was 21·7% and 29·2%, using an immunofluorescence antibody test and enzyme-linked immunosorbent assay (ELISA), respectively. The occurrence of strongyloidiasis in immunosuppressed individuals was 11·8% by parasitological methods and 19·5% using immunological methods. Considering that Brazil is a tropical country and that the character of chronicity and autoinfection of the parasite that can result in severe forms of hyperinfection or dissemination makes strongyloidiasis an important medically and socially neglected problem.

Keywords

strongyloidiasisepidemiologyprevalenceBrazil

Information

Type
Review Article
Information
Parasitology , Volume 138 , Issue 11 , September 2011 , pp. 1331 - 1340
Copyright
Copyright © Cambridge University Press 2011

INTRODUCTION

Strongyloides stercoralis (Bavay, 1876) is an intestinal nematode, which causes strongyloidiasis, helminthiasis usually responsible for chronic asymptomatic infections of the gastrointestinal tract in immunocompetent human hosts and may remain undetected for decades. In immunocompromised patients due to immunosuppressive therapy (particularly steroids) (Genta, Reference Genta1992; Keiser and Nutman, Reference Keiser and Nutman2004; Lam et al. Reference Lam, Tong, Chan and Siu2006), infection with human immunodeficiency virus (HIV) (Ferreira, Reference Ferreira2003; Keiser and Nutman, Reference Keiser and Nutman2004; Silva et al. Reference Silva, Ferreira, Borges and Costa-Cruz2005), infection with human T-lymphotropic virus 1 (HTLV- 1) (Porto et al. Reference Porto, Muniz, Oliveira Júnior and Carvalho2002; Keiser and Nutman, Reference Keiser and Nutman2004), solid organ transplantation (Keiser and Nutman, Reference Keiser and Nutman2004; Concha et al. Reference Concha, Harrington and Rogers2005), haematological malignancies (Graeff-Teixeira et al. Reference Graeff-Teixeira, Leite, Sperhacke, Fassina, Petry, Mucenic, Pandolfi, Barcelos and Job1997; Keiser and Nutman, Reference Keiser and Nutman2004), solid-organ malignancies (Safdar et al. Reference Safdar, Malathum, Rodriguez, Husni and Rolston2004), hypogammaglobulinaemia (Keiser and Nutman, Reference Keiser and Nutman2004), chronic alcoholism (Oliveira et al. Reference Oliveira, Ribeiro, Mendes, Oliveira and Costa-Cruz2002; Silva et al. Reference Silva, Ferreira, Borges and Costa-Cruz2005; Marques et al. Reference Marques, Zago-Gomes, Gonçalves and Pereira2010) severe malnutrition (Keiser and Nutman, Reference Keiser and Nutman2004) or diabetes mellitus (Mendonça et al. Reference Mendonça, Gonçalves-Pires, Rodrigues, Ferreira and Costa-Cruz2006), this infection may develop into a hyperinfection syndrome or disseminated disease (Keiser and Nutman, Reference Keiser and Nutman2004; Marcos et al. Reference Marcos, Terashima, DuPont and Gotuzzo2008).

This parasite infects humans through skin penetration, and has a complex life cycle involving 2 stages of development: a phase of free-living that occurs in the environment, good conditions of temperature and humidity, and the other stage as a parasite, which occurs within the host. The parthenogenetic female of S. stercoralis lays few eggs per day, which are deposited in the intestinal epithelium, the rhabditiform mature larvae exit in the feces of the patients, and constitute in the diagnostic stage viewed in optical microscopy. By a process of autoinfection, there may be a rapid increase in the number of infective larvae; strongyloidiasis consequently persists for decades (Grove, Reference Grove1996; Costa-Cruz, Reference Costa-Cruz, Neves, Melo, Linardi and Vitor2005). The fact that the free-living forms of the parasite in the soil depend on favourable environmental conditions such as humidity and high temperature, makes conditions in many regions of Brazil ideal for the development and maintenance of intestinal parasites (Carmo et al. Reference Carmo, Perez, Gerolomo, Silva and Alves2005).

Definitive diagnosis of strongyloidiasis is performed mainly by the identification of larvae in fecal specimens, through concentration techniques or culture methods. Nevertheless, these larvae are excreted in low numbers and not daily, making the parasitological methods unreliable in most cases, requiring the analysis of 7 stool samples to increase the positivity (Dreyer et al. Reference Dreyer, Fernandes-Silva, Alves, Rocha, Albuquerque and Addiss1996; Uparanukraw et al. Reference Uparanukraw, Phongsri and Morakote1999). Several techniques are described for the parasitological diagnosis of strongyloidiasis, including the modified Baermann method by Moraes (BM) (Baermann, Reference Baermann1917; Moraes, Reference Moraes1948), the method of Rugai (R) (Rugai et al. Reference Rugai, Mattos and Brisola1954), Harada-Mori (HM) (Harada and Mori, Reference Harada and Mori1955) and culture method on agar plates (AP) (Arakaki et al. Reference Arakaki, Hasegawa, Asato, Ikeshiro, Kinjo, Saito and Iwanaga1988). However, the increased number of stool samples and the inconvenience of fresh stool specimens, make these parasitological diagnostic methods unusable in routine laboratory practice. Larvae can also be found in other body fluids (sputum, broncho-alveolar lavage, among others), through endoscopy, colonoscopy, or intestinal biopsy (Costa-Cruz, Reference Costa-Cruz, Neves, Melo, Linardi and Vitor2005; Minematsu et al. Reference Minematsu, Hokama, Makishi, Arakaki, Kinjo and Fujita2011). The failure to diagnose this parasitosis is reflected in the frequent reports of fatal cases associated with hyperinfections, brought on by corticosteroid therapy. The similarity between corticosteroids and an ecdyses hormone of the parasite, which promotes maturation of infective larvae in the intestine of the patient, is a possible explanation for this association (Hernandez-Chavarria, Reference Hernandez-Chavarria2001). Thus, the serological methods present a good alternative for early diagnosis and for evaluating the effectiveness of treatment (Sato et al. Reference Kobayashi, Hasegawa, Forli, Nishimura, Yamana, Shimabukuro and Sato1995; Paula et al. Reference Paula, Castro, Gonçalves-Pires, Marçal, Campos and Costa-Cruz2000; Siddiqui and Berk, Reference Siddiqui and Berk2003; Costa-Cruz, Reference Costa-Cruz, Neves, Melo, Linardi and Vitor2005; Page et al. Reference Page, Dempsey and McCarthy2006; Sudré et al. Reference Sudré, Macedo, Peralta and Peralta2006; Varatharajalu et al. Reference Varatharajalu, Parandaman, Ndao, Andersen and Neva2011).

Many epidemiological aspects of Strongyloides infection are not well known, such as prevalence rates that can be expected in different sectors of the population, environmental and zoonotic aspects, geographical variations, besides transmission and clinical presentation, host immunity and the risk factors for dissemination. The prevalence of S. stercoralis is underestimated, especially by the low sensitivity of parasitological diagnostic methods employed in routine procedures that do not include specific methods to search for larvae, and also the shortage of parasitological surveys. Thus, S. stercoralis infections in many areas remain without information (Hernandez-Chavarria, Reference Hernandez-Chavarria2001; Olsen et al. Reference Olsen, van Lieshout, Marti, Polderman, Polman, Steinmann, Stothard, Thybo, Verweij and Magnussen2009). Strongyloidiasis has a heterogeneous worldwide distribution, and prevalence has been divided into 3 categories: sporadic (<1%), endemic (1–5%) and hyperendemic (>5%) (Pires and Dreyer, Reference Pires and Dreyer1993). It is estimated that strongyloidiasis affects 30–100 million individuals around the world. All hyperendemic areas are located in the tropics, the endemic areas in the subtropics, but the parasite is also present, sporadically, in the United States, Europe and Asia (Olsen et al. Reference Olsen, van Lieshout, Marti, Polderman, Polman, Steinmann, Stothard, Thybo, Verweij and Magnussen2009).

The World Health Organization (2005) recommended that the Strongyloides infection could be included in the ‘Parasite Control Program’ in areas where the infection is endemic. However, now the infection is only a possible target and presumably, not effectively integrated in helminth control programmes. Recognizing that intestinal parasites are still prevailing in the country, the Brazilian government created the National Surveillance and Control of Enteroparasitoses in 2005 (Carmo et al. Reference Carmo, Perez, Gerolomo, Silva and Alves2005) and in 2007, the Growth Acceleration Program (PAC) (Ministério da Fazenda, 2007) providing for actions in sanitation, targeting the reduction of infectious and parasitic diseases, including intestinal parasitosis.

Despite scientific knowledge and technological advances available for its treatment and prevention, strongyloidiasis is still a parasitic disease of great importance to public health in Brazil, but information on strongyloidiasis is based on studies that show local epidemiological data. The objective of this review is to outline an epidemiological profile of this intestinal helminth in Brazil by parasitological and serological diagnosis in inhabitants of rural and urban areas, and associate this profile with different immunosuppression situations.

METHODOLOGY

We conducted a review of the literature on epidemiological aspects of strongyloidiasis in Brazil, using the keywords ‘Strongyloides stercoralis’, ‘strongyloidiasis’, ‘intestinal parasites’ and ‘Brazil’ in different combinations. We searched in the Scientific Eletronic Library Online (SciELO) and the U.S. National Library of Medicine (PubMed) over 20 years (1990–2009). There have been many studies regarding intestinal parasites from which the specific results for S. stercoralis were extracted. We used as inclusion criteria any study that gave values of the occurrence of S. stercoralis in Brazil in accordance with the region, location by state, rural and urban areas, considering the population by age, immunity, the method of diagnosis, or parasitological and serological association with other diseases (alcoholism, diabetes, cancer, infection with AIDS/HIV and HTLV-1, among others). As exclusion criteria: any study published before 1990 and after 2009, and papers that did not show the occurrence of S. stercoralis, when we used the keyword ‘intestinal parasite’. To analyse the information the value of the mean (X) frequencies reported was chosen.

RESULTS AND DISCUSSION

Epidemiological profile of S. stercoralis by parasitological methods

In the period from 1990 to 2009 it was found that the occurrence of infection by S. stercoralis in Brazil, using parasitological methods of diagnosis was 5·5%, characterizing the country as a hyperendemic area for strongyloidiasis. There was a variation of 3·9% to 7·9% among the 5 regions of Brazil, but there was no variation between the rural (4·8%) and urban (5·0%) areas. It is known that the marked socio-economic inequalities observed in Brazil, combined with the disorderly urbanization process, cause portions of the population to live in precarious living conditions. The occupation of the peripheral areas of cities where sanitary conditions make the quality of life style not different from rural areas, and often in worse conditions that favour the transmission of intestinal parasites (De Carli et al. Reference De Carli, Mentz, Rott, Silva, Wendorff, Tasca, Castilhos, De Carli, Montenegro and Mylius1997).

Changes in the prevalence of Strongyloides stercoralis in Brazil in the period 1990–2009 as assessed by parasitological methods of diagnosis are shown in Fig. 1. The variation was from 1·1 to 10·8% during the period studied. The occurrence of S. stercoralis infection in humans, using parasitological methods, distributed by region, state of the federation and the population studied is shown in Table 1. The diversity of parasitological diagnostic methods used in parasitological survey, make epidemiological knowledge of this parasite irregular. Of the 64 studies analysed and shown in Table 1, the diversity of techniques used as a diagnostic tool can be observed, in which 39 of the studies (60·9%) used non-specific methods for the detection of S. stercoralis larvae. We included as non-specific parasitological methods the parasitological techniques used in the routine of clinical laboratories, for example: the Direct (Amato Neto and Correa, Reference Amato Neto and Correa1991), Faust (Faust et al. Reference Faust, D'Antoni, Odom, Miller, Peres, Sawitz, Thomen, Tobie and Walker1938), Lutz (Lutz, Reference Lutz1919), or Ritchie/Blagg/MIFC (Ritchie, Reference Ritchie1948) methods that are not suitable or specific for the detection of nematode larvae. Only 25 (39·1%) of the studies present results based on at least 1 specific method (BM, R, HM or AP) for the detection of these helminth larvae.

Fig. 1.

Changes in the prevalence of Strongyloides stercoralis in Brazil in the period 1990–2009 as assessed by parasitological methods of diagnosis.

Table 1.

Occurrence of Strongyloides stercoralis infection in humans, considering the parasitological diagnosis, region, state and population in Brazil from 1990 to 2009

(% Positive parasitological methods, without discrimination of rural and urban general, All (studies without discrimination of age).)

The concept that children are a group largely involved in parasite infections (Moura et al. Reference Moura, Bragazza, Coelho and Aun1997; Carvalho et al. Reference Carvalho, Carvalho and Mascarini2006; Silva et al. Reference Silva, Silva, Almeida, Sousa and Freitas2009) was not observed for this parasite in this period. When we analysed the articles that were available to characterize the age group studied, it was noted that the occurrence of S. stercoralis increased with age (Fig. 2). The mean occurrence of 12·1% for S. stercoralis, for age 60 and over (Hurtado-Guerrero et al. Reference Hurtado-Guerrero, Alencar and Hurtado-Guerrero2005; Aguiar et al. Reference Aguiar, Gonçalves, Sodré, Pereira, Bóia, Lemos and Daher2007; Miné and Rosa, Reference Miné and Rosa2008), suggests epidemiological conditions of concern for the elderly population in Brazil since, in this group, the immune system is weakened, particularly for those with poor health. In a parasitological study in the Amazon region, Hurtado-Guerrero et al. (Reference Hurtado-Guerrero, Alencar and Hurtado-Guerrero2005) drew attention to the effect that intestinal parasites have on the nutritional status and health of the elderly population, and, moreover, mentioned an occurrence of 9·1% for S. stercoralis in this age group. The greater occurrence of S. stercoralis in the elderly was obtained from the study of Miné and Rosa (Reference Miné and Rosa2008) in São Paulo state, which detected 20·4% infection in the elderly, considering both sexes, but 40% in elderly males of >80 years of age.

Fig. 2.

Changes in the prevalence of Strongyloides stercoralis, by the age of the Brazilian population, in the period 1990–2009 as assessed by parasitological methods of diagnosis. * The population was not weighted by the age distribution of the sampled members.

Epidemiological profile of S. stercoralis by serological methods

Owing to the limited sensitivity of parasitological methods for diagnosis of infection by S. stercoralis, serological methods have been resorted to, which have high sensitivity and specificity. Immunological tests such as enzyme-linked immunosorbent assay (ELISA), immunofluorescence antibody test (IFAT) and Western-blotting, have been described for the diagnosis of strongyloidiasis (Costa-Cruz et al. Reference Costa-Cruz, Bullamah, Gonçalves-Pires, Campos and Vieira1997; Sudré et al. Reference Sudré, Siqueira, Barreto, Peralta, Macedo and Peralta2007; Machado et al. Reference Machado, Faccioli, Costa-Cruz, Lourenço, Roque-Barreira, Gonçalves-Pires and Ueta2008c; Feliciano et al. Reference Feliciano, Gonzaga, Gonçalves-Pires, Gonçalves, Rodrigues, Ueta and Costa-Cruz2010). Among the various techniques used in immunodiagnosis of strongyloidiasis, the ELISA test has been shown to be superior with respect to practicality, safety and the availability of reagents (Liu and Weller, Reference Liu and Weller1993), in addition to high sensitivity and specificity (Schaffel et al. Reference Schaffel, Nucci, Carvalho, Braga, Almeida, Portugal and Pulcheri2001). The ELISA was the test of choice for most of the articles analysed as a single technique for serological diagnosis (Rossi et al. Reference Rossi, Partel, Teixeira, Takahashi, De Barros-Mazon and Da Silva1993; Costa-Cruz et al. Reference Costa-Cruz, Madalena, Silva, Sopelete, Campos and Taketomi2003; Machado et al. Reference Machado, Ueta, Gonçalves-Pires, Oliveira, Faccioli and Costa-Cruz2003; Rodrigues et al. Reference Rodrigues, Oliveira, Sopelete, Silva, Campos, Taketomi and Costa-Cruz2007), or in association with the IFAT and/or Western blot (Silva et al. Reference Silva, Barcelos, Passos-Lima, Espindola, Campos and Costa-Cruz2003; Rodrigues et al. Reference Rodrigues, Sopelete, Silva, Cunha-Junior, Taketomi and Costa-Cruz2004; Mota-Ferreira et al. Reference Mota-Ferreira, Gonçalves-Pires, Ferreira, Sopelete, Adballah and Costa-Cruz2009). The difficulty in obtaining S. stercoralis larvae and thus obtaining a sufficient amount of antigenic material has been a limiting factor for the immunodiagnosis of strongyloidiasis (Rossi et al. Reference Rossi, Partel, Teixeira, Takahashi, De Barros-Mazon and Da Silva1993). This is why many researchers have been using heterologous antigens, Strongyloides ratti or Strongyloides venezuelensis, in the diagnosis of strongyloidiasis, since they are easy to obtain and are a safe source without risk to their handlers, besides having high sensitivity and specificity (Costa-Cruz et al. Reference Costa-Cruz, Bullamah, Gonçalves-Pires, Campos and Vieira1997; Machado et al. Reference Machado, Ueta, Gonçalves-Pires, Oliveira, Faccioli and Costa-Cruz2001, Reference Machado, Ueta, Gonçalves-Pires, Oliveira, Faccioli and Costa-Cruz2003; Silva et al. Reference Silva, Barcelos, Passos-Lima, Espindola, Campos and Costa-Cruz2003; Rodrigues et al. Reference Rodrigues, Sopelete, Silva, Cunha-Junior, Taketomi and Costa-Cruz2004, Reference Rodrigues, Oliveira, Sopelete, Silva, Campos, Taketomi and Costa-Cruz2007; Feliciano et al. Reference Feliciano, Gonzaga, Gonçalves-Pires, Gonçalves, Rodrigues, Ueta and Costa-Cruz2010).

Of the 3 seroepidemiological studies conducted in the general population in Brazil, the mean positivity in serum samples of S. stercoralis infection was 21·7% and 29·2%, using serological testing by IFAT-IgG and ELISA-IgG, respectively, studies were concentrated in the Southeast region (Costa-Cruz et al. Reference Costa-Cruz, Machado and Campos1998; Machado et al. Reference Machado, Teixeira, Paula, Gonçalves-Pires, Ueta and Costa-Cruz2007; Mota-Ferreira et al. Reference Mota-Ferreira, Gonçalves-Pires, Ferreira, Sopelete, Adballah and Costa-Cruz2009).

Occurrence of S. stercoralis infection associated with different types of immunosuppression

The occurrence of S. stercoralis infection associated with different types of immunosuppression compared to parasitological diagnosis and/or serology, is shown in Table 2. The variety of techniques may be noted, but most studies have used techniques suitable for the detection of larval helminths since the suspicion of infection by S. stercoralis could be mentioned in the population studied. The average occurrence was 11·8% using parasitological diagnostic methods. In 4 studies of immunosuppression using parasitological and immunological diagnosis it was found that the mean occurrence increased from 7·1% to 19·5% respectively (Paula et al. Reference Paula, Castro, Gonçalves-Pires, Marçal, Campos and Costa-Cruz2000; Schaffel et al. Reference Schaffel, Nucci, Carvalho, Braga, Almeida, Portugal and Pulcheri2001; Mendonça et al. Reference Mendonça, Gonçalves-Pires, Rodrigues, Ferreira and Costa-Cruz2006; Machado et al. Reference Machado, Teixeira, Gonçalves-Pires, Loureiro, Araújo and Costa-Cruz2008d), emphasizing the usefulness of serological methods as a tool for diagnosis of strongyloidiasis, especially when the question involved is immunosuppression.

Table 2.

Occurrence of Strongyloides stercoralis infection in humans using parasitological methods and/or serological diagnosis, distributed according to the type of immunosuppression (1990–2009)

* Positive by serological methods (ELISA – enzyme-linked immunosorbent assay; IFAT, indirect fluorescent antibody test); parasitological methods (BM, Baermann-Moraes; D, direct; F, Faust/flotation; HM, Harada-Mori; L, Lutz; MIFC, Ritchie/Blagg; AP, culture agar plate, R, Rugai) and staining (AR, acid fast; ZN, Ziehl-Neelsen; AS, Blue metilen Safranin; CW, Chromotropic Weber's).

Although the association of strongyloidiasis and immunosuppression are important, case reports are scarce. In Brazil, the occurrence of strongyloidiasis in transplant patients (Dulley et al. Reference Dulley, Costa, Cosentino, Gamba and Saboya2009; Villela et al. Reference Vilela, Clemente, Mira, Torres, Veloso, Fonseca, Fonseca, França and Lima2009), the use of corticosteroids and/or with neoplasias (Godoy et al. Reference Godoy, Campos, Costa and Castro1998; Rodrigues et al. Reference Rodrigues, Fróes, Anefalos and Kobayasi2001; Lambertucci et al. Reference Lambertucci, Leão and Barbosa2003; Porto et al. Reference Porto, Alcântara, Leal, Castro and Carvalho2005; Salluh et al. Reference Salluh, Bozza, Pinto, Toscano, Wellers and Soares2005; Giavina-Bianchi et al. Reference Giavina-Bianchi, Silva, Toledo-Barros, Birolini, Kalil and Rizzo2006; Benincasa et al. Reference Benincasa, Azevedo, Canabarro, Valentim, Silva, Superti and Dias2007; Ben-Horin et al. Reference Ben-Horin, Barshack, Chowers and Mouallem2008; Veloso et al. Reference Veloso, Porto and Moraes2008), and haemolytic anaemia (Ferreira et al. Reference Ferreira, Barbosa, Ferreira, Souza, Neves, Carvalho and Barbosa2008) have been emphasized. Many of these reports show that the late diagnosis of infection may be associated with the severity of infection, causing patient death (Rodrigues et al. Reference Rodrigues, Fróes, Anefalos and Kobayasi2001; Salluh et al. Reference Salluh, Bozza, Pinto, Toscano, Wellers and Soares2005; Benincasa et al. Reference Benincasa, Azevedo, Canabarro, Valentim, Silva, Superti and Dias2007; Ferreira et al. Reference Ferreira, Barbosa, Ferreira, Souza, Neves, Carvalho and Barbosa2008; Veloso et al. Reference Veloso, Porto and Moraes2008; Villela et al. Reference Vilela, Clemente, Mira, Torres, Veloso, Fonseca, Fonseca, França and Lima2009). In a study of prevalence of symptomatic parasitosis in adult renal transplant recipients, in Porto Alegre, Brazil, from 2001 to 2005, Valar et al. (Reference Valar, Keitel, Dal Prá, Gnatta, Santos, Bianco, Sukienni, Pegas, Bittar, Oliveira and Garcia2007) showed that out of 657 transplants, 11 (1·67%) had symptoms and confirmed S. stercoralis diagnosis by the finding of larvae in feces (8 cases), by broncho-alveolar lavage fluid (in 2 cases), duodenal biopsy and sputum (in 1 case), and from these, 3 cases developed hyperinfection, and 1 died. The diagnosis of strongyloidiasis in these reported cases occurred through the finding of larvae in feces (Dulley et al. Reference Dulley, Costa, Cosentino, Gamba and Saboya2009), in other fluids (Porto et al. Reference Porto, Alcântara, Leal, Castro and Carvalho2005; Salluh et al. Reference Salluh, Bozza, Pinto, Toscano, Wellers and Soares2005; Ferreira et al. Reference Ferreira, Barbosa, Ferreira, Souza, Neves, Carvalho and Barbosa2008; Villela et al. Reference Vilela, Clemente, Mira, Torres, Veloso, Fonseca, Fonseca, França and Lima2009), at biopsy (Rodrigues et al. Reference Rodrigues, Fróes, Anefalos and Kobayasi2001; Lambertucci et al. Reference Lambertucci, Leão and Barbosa2003; Salluh et al. Reference Salluh, Bozza, Pinto, Toscano, Wellers and Soares2005; Giavina-Bianchi et al. Reference Giavina-Bianchi, Silva, Toledo-Barros, Birolini, Kalil and Rizzo2006; Ben-Horin et al. Reference Ben-Horin, Barshack, Chowers and Mouallem2008) and at autopsy (Godoy et al. Reference Godoy, Campos, Costa and Castro1998; Benincasa et al. Reference Benincasa, Azevedo, Canabarro, Valentim, Silva, Superti and Dias2007; Veloso et al. Reference Veloso, Porto and Moraes2008).

Co-infection by S. stercoralis and HTLV-1 has been reported to decrease in response to anti-helmintic treatment and increased severity of viral infection in these patients (Porto et al. Reference Porto, Oliveira Filho, Neva, Orge, Alcântara, Gam and Carvalho2001, Reference Porto, Muniz, Oliveira Júnior and Carvalho2002). In a coproparasitological survey, Chieffi et al. (Reference Chieffi, Chiattone, Feltrim, Alves and Paschoalotti2000) called attention to the higher prevalence of S. stercoralis among HTLV-1 positive blood donors in relation to the negative HTLV-1.

HIV/AIDS infection associated with S. stercoralis has been reported in some studies (Dias et al. Reference Dias, Mangini, Torres, Vellosa, Silva, Silva, Corrêa and Coletti1992; Feitosa et al. Reference Feitosa, Bandeira, Sampaio, Badaró and Brites2001; Blatt and Cantos, Reference Blatt and Cantos2003; Silva et al. Reference Silva, Ferreira, Borges and Costa-Cruz2005) using parasitological methods and/or serological diagnosis. However, only 3 reports demonstrated the seriousness of helminthiasis when associated with HIV/AIDS, previously considered an opportunistic parasite (Takayanagui et al. Reference Takayanagui, Lofrano, Araújo and Chimelli1995; Ferreira et al. Reference Ferreira, Nishioka, Borges, Costa-Cruz, Rossin, Rocha, Silvestre and Nunes-Araújo1999; Bachur et al. Reference Bachur, Vale, Coêlho, Queiroz and Chaves2008).

The association of chronic alcoholics with strongyloidiasis is an interesting aspect, since this group of patients may be suffering from severe forms of strongyloidiasis, probably due to dulled mental function, breakdown of local protective barriers, aspiration, exposure to pathogens and malnutrition caused by alcoholism (Oliveira et al. Reference Oliveira, Ribeiro, Mendes, Oliveira and Costa-Cruz2002; Zago-Gomes et al. Reference Zago-Gomes, Aikawa, Perazzio, Gonçalves and Pereira2002). The corticosteroid metabolites in alcoholics may increase the fecundity of the females, and thus the number of rhabditiform larvae coming out in the feces (Zago-Gomes et al. Reference Zago-Gomes, Aikawa, Perazzio, Gonçalves and Pereira2002). However, Genta (Reference Genta1992) suggested that the ecdysoid-like action of the steroids would increase the developmental rate and moulting of the larvae in the intestine causing autoinfection. The increase in autoinfection would lead to an increased number of adult female worms, leading to an increase in the number of larvae (L1) in the feces.

Complementary aspects

Domestic animals such as dogs infected with Strongyloides, particularly in areas where sanitary conditions are unsatisfactory, can become reservoirs for this helminth and sources of human infection (Ferreira-Junior et al. Reference Ferreira-Junior, Gonçalves-Pires, Silva, Gonçalves and Costa-Cruz2006; Gonçalves et al. Reference Gonçalves, Machado, Gonçalves-Pires, Ferreira, Silva and Costa-Cruz2007; Campos-Filho et al. Reference Campos-Filho, Barros, Campos, Braga, Cazorla, Albuquerque and Carvalho2008). Thus, the presence of feces from infected humans or animals contaminating the soil are epidemiological factors that may influence the onset, maintenance and propagation of human strongyloidiasis as well as favourable conditions of temperature and humidity, and inadequate hygienic habits (Costa-Cruz, Reference Costa-Cruz, Neves, Melo, Linardi and Vitor2005).

We would like to emphasize that one drawback of immunological assays for antibody demonstration is that it reflects the history of infection and not necessarily the current on-going infection. It is difficult in many cases to know whether or not low-level autoinfection is continuing. This occurs mainly because antibody levels remain detectable for years after antihelmintic treatment. (Liu and Weller, Reference Liu and Weller1993; Grove, Reference Grove1996).

Currently, the detection of coproantigen by ELISA, standardized in experimental models (Nageswaran et al. Reference Nageswaran, Craig and Devaney1994; Gonçalves et al. Reference Gonçalves, Silva, Ueta and Costa-Cruz2010), and for human strongyloidiasis (El-Badry, Reference El-Badry2009) allows the identification of cases of active infection. The development of Polymerase Chain Reaction (PCR) in faecal samples of animals with low experimental infection by S. venezuelensis (Marra et al. Reference Marra, Chiuso-Minicucci, Machado, Zorzella-Pezavento, França, Ishikawa, Amarante, Sartori and Amarante2010) and also in human faecal samples (Verweij et al. Reference Verweij, Canales, Polman, Ziem, Brienen, Polderman and van Lishout2009) are promising as an alternative for the diagnosis of strongyloidiasis.

CONCLUSIONS

The non-application of techniques for the accurate diagnosis of this helminthiasis, either parasitological or immunological and molecular biology in the large centres, contributes to the underestimation of the prevalence of strongyloidiasis. Thus, many epidemiological aspects of infection by S. stercoralis are unknown or only poorly understood, such as national endemic areas, in which prevalence rates and intensities can typically be expected in different settings and populations, the zoonotic aspects, and geographical variations involved in infection. Therefore, we recommend what we consider to be the way forward and the priorities to reducing the prevalence of strongyloidiasis. (1) Health education campaigns on the disease. (2) Parasitological diagnosis including specific methods for analysing the nematode larvae. (3) Need to screen patients from endemic areas of strongyloidiasis prior to receiving corticosteroid therapy or organ transplantation. (4) Follow-up of patients with immunosuppression. (5) Development of novel diagnostic assays, and finally (6) the notification of positive cases.

Considering that Brazil is a tropical country and the character of chronicity and auto-infection of this parasite which can result in severe forms of hyper-infection or dissemination makes strongyloidiasis an important medical and social problem that unfortunately is neglected by health authorities.

References

REFERENCES

Aguiar, J. I. A., Gonçalves, A. Q., Sodré, F. C., Pereira, S. R., Bóia, M. N., Lemos, E. R. S. and Daher, R. R. (2007). Intestinal protozoa and helminths among Terena Indians in the State of Mato Grosso do Sul: high prevalence of Blastocystis hominis. Revista da Sociedade Brasileira de Medicina Tropical 40, 631–63410.1590/S0037-86822007000600006.CrossRefGoogle Scholar
Amato Neto, V. and Correa, L. L. (1991). Exame Parasitológico de Fezes. Sarvier, São Paulo, Brazil.Google Scholar
Arakaki, T., Hasegawa, H., Asato, R., Ikeshiro, T., Kinjo, F., Saito, A. and Iwanaga, M. (1988). A new method to detect Strongyloides stercoralis from human stool. Japannese Journal of Tropical Medicine Hygiene 16, 11–17.Google Scholar
Araujo, C. F. and Fernández, C. L. (2005). Prevalência de parasitas intestinais na cidade de Eirunepé, Amazonas. Revista da Sociedade Brasileira de Medicina Tropical 38, 69. doi: 10.1590/S0037-86822005000100016.CrossRefGoogle Scholar
Bachur, T. P. R., Vale, J. M., Coêlho, I. C. B., Queiroz, T. R. B. S. and Chaves, C. S. (2008). Enteric parasitic infections in HIV/AIDS patients before and after the highly active antiretroviral therapy. Brazilian Journal of Infectious Diseases 12, 115–122. doi: 10.1590/S1413-86702008000200004.Google ScholarPubMed
Baermann, G. (1917). Eine einfache Methode zur Auffindung von Ankylostomum (Nematoden) Larven in Erdproben. Mededeel mith. H. Geneesk. Batavia, Lab Weltevreden Feestbundel. pp. 41–47.Google Scholar
Barbosa, F. C., Ribeiro, M. C. M. and Marçal Júnior, O. (2005). Comparação da prevalência de parasitoses intestinais em escolares da zona rural de Uberlândia (MG). Revista de Patologia Tropical 34, 151–154.Google Scholar
Basso, R. M. C., Silva-Ribeiro, R. T., Soligo, D. S., Ribacki, S. I., Callegari-Jacques, S. M. and Zoppas, B. C. A. (2008). Evolução da prevalência de parasitoses intestinais em escolares em Caxias do Sul, RS. Revista da Sociedade Brasileira de Medicina Tropical 41, 263–268. doi: 10.1590/S0037-86822008000300008.CrossRefGoogle ScholarPubMed
Bencke, A., Artuso, G. L., Reis, R. S., Barbieri, N. L. and Rott, M. B. (2006). Enteroparasitoses em escolares residentes na periferia de Porto Alegre, RS, Brasil. Revista de Patologia Tropical 35, 31–36.Google Scholar
Ben-Horin, S., Barshack, I., Chowers, Y. and Mouallem, M. (2008). Flare-up of ulcerative colitis after systemic corticosteroids: a strong case for Strongyloides. World Journal of Gastroenterology 14, 4413–4415. doi: 10.3748/wjg.14.4413.CrossRefGoogle Scholar
Benincasa, C. C., Azevedo, F. O., Canabarro, M. S., Valentim, H. M., Silva, V. D., Superti, S. V. and Dias, F. S. (2007). Hiper-infecção por Strongyloides stercoralis. Relato de caso. Revista Brasileira de Terapia Intensiva 19, 128–131. doi: 10.1590/S0103-507×2007000100018.CrossRefGoogle Scholar
Blatt, J. M. and Cantos, G. A. (2003). Evaluation of techniques for the diagnosis of Strongyloides stercoralis in human immunodeficiency virus (HIV) positive and HIV negative individuals in the city of Itajaí, Brazil. Brazilian Journal of Infectious Diseases 7, 402–408. doi: 10.1590/S1413-86702003000600008.Google Scholar
Boia, M. N., Motta, L. P., Salazar, M. S. P., Mutis, M. P. S., Coutinho, R. B. A. and Coura, J. R. (1999). Estudo das parasitoses intestinais e da infecção chagásica no município Novo Airão, Estado do Amazonas, Brasil. Caderno de Saúde Pública 15, 497–504. doi: 10.1590/S0102-311X1999000300006.CrossRefGoogle Scholar
Buschini, M. L. T., Pittner, E., Czervinski, T., Moraes, I. F., Moreira, M. M., Sanches, H. F. and Monteiro, M. C. (2007). Spatial distribution of enteroparasites among school children from Guarapuava, State of Paraná, Brazil. Revista Brasileira de Epidemiologia 10, 568–578. doi: 10.1590/S1415-790X2007000400015.CrossRefGoogle Scholar
Campos-Filho, P. C., Barros, L. M., Campos, J. O., Braga, V. B., Cazorla, I. M., Albuquerque, G. R. and Carvalho, S. M. S. (2008). Parasitas zoonóticos em fezes de cães em praças públicas do município de Itabuna, Bahia, Brasil. Revista Brasileira de Parasitologia Veterinária 17, 206–209.CrossRefGoogle Scholar
Capuano, D. M., Lazzarini, M. P. T., Giacometti Júnior, E. and Takayanagui, O. M. (2008). Enteroparasitoses em manipuladores de alimentos do município de Ribeirão Preto – SP, Brasil, 2000. Revista Brasileira de Epidemiologia 11, 687–695. doi: 10.1590/S1415-790X2008000400015.CrossRefGoogle Scholar
Carmo, E. A., Perez, E. P., Gerolomo, M., Silva, M. P. and Alves, R. M. S. (2005). Plano nacional de vigilância e controle das enteroparasitoses. 42p. http://portal.saude.gov.br/portal/arquivos/pdf/Enteroparasitoses_Plano_nacional_%2006%2007%202005.pdf (acessado em 3/8/2010).Google Scholar
Carvalho, T. B., Carvalho, L. R. and Mascarini, L. M. (2006). Occurrence of enteroparasites in day care centers in Botucatu (São Paulo State, Brazil) with emphasis on Cryptosporidium sp., Giardia duodenalis and Enterobius vermicularis. Revista do Instituto de Medicina Tropical de São Paulo 48, 269–273. doi: 10.1590/S0036-46652006000500006.CrossRefGoogle Scholar
Castro, A. Z., Viana, J. D. C., Penedo, A. A. and Donatele, D. M. (2004). Levantamento das parasitoses intestinais em escolares da rede pública na cidade de Cachoeiro de Itapemirim – ES. NewsLab 63, 102–105.Google Scholar
Chieffi, P. P., Chiattone, C. S., Feltrim, E. N., Alves, R. C. and Paschoalotti, M. A. (2000). Coinfection by Strongyloides stercoralis in blood donors infected with human T-cell leukemia/lymphoma virus type 1 in São Paulo City, Brazil. Memórias do Instituto Oswaldo Cruz 95, 711–712. doi: 10.1590/S0074-02762000000500017.CrossRefGoogle Scholar
Cimerman, S., Cimerman, B. and Lewi, D. S. (1999). Prevalence of intestinal parasitic infections in patients with acquired immunodeficiency syndrome in Brazil. International Journal of Infectious Diseases 3, 203–206.CrossRefGoogle ScholarPubMed
Concha, R., Harrington, W. Jr. and Rogers, A. I. (2005). Intestinal strongyloidiasis: recognition, management, and determinants of outcome. Journal Clinical Gastroenterology 39, 203–211.CrossRefGoogle ScholarPubMed
Costa-Cruz, J. M. (2005). Estrongiloidíase In Parasitologia Humana (ed. Neves, D. P., Melo, A. L., Linardi, P. M. and Vitor, R. W. A.), pp. 275–284. Atheneu, São Paulo, Brazil.Google Scholar
Costa-Cruz, J. M., Bullamah, C. B., Gonçalves-Pires, M. R. F., Campos, D. M. and Vieira, M. A. (1997). Cryo-microtome sections of coproculture larvae of Strongyloides stercoralis and Strongyloides ratti as antigen sources for the immunodiagnosis of human strongyloidiasis. Revista do Instituto de Medicina Tropical de São Paulo 39, 313–317. doi: 10.1590/S0036-46651997000600001.CrossRefGoogle ScholarPubMed
Costa-Cruz, J. M., Cardoso, M. L. G. and Marques, D. E. (1995). Intestinal parasites in school food handlers in the city of Uberlândia, Minas Gerais, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 37, 191–196. doi: 10.1590/S0036-46651995000300002.CrossRefGoogle ScholarPubMed
Costa-Cruz, J. M., Ferreira, M. S. and Rossin, I. R. (1996). Intestinal parasites in AIDS and +HIV patients in Uberlândia, Minas Gerais, Brazil. Memórias do Instituto Oswaldo Cruz 91, 685–686. doi: 10.1590/S0074-027619960000600004.CrossRefGoogle ScholarPubMed
Costa-Cruz, J. M., Machado, E. R. and Campos, D. M. (1998). Seroepidemiological study of human strongyloidiasis with blood samples collected on filter paper, in Abadia dos Dourados (Minas Gerais, Brazil). Revista do Instituto de Medicina Tropical de São Paulo 40, 329–331. doi: 10.1590/S0036-46651998000500013.CrossRefGoogle ScholarPubMed
Costa-Cruz, J. M., Madalena, J., Silva, D. A. O., Sopelete, M. C., Campos, D. M. B. and Taketomi, E. A. (2003). Heterologous antigen extract in ELISA for the detection of human IgE anti-Strongyloides stercoralis. Revista do Instituo de Medicina Tropical de São Paulo 45, 265–268. doi: 10.1590/S0036-46652003000500005.Google ScholarPubMed
Costa-Macedo, L. M., Machado-Silva, J. R., Rodrigues-Silva, J. R., Oliveira, L. M. and Vianna, M. S. K. (1998). Enteroparasitose em pré-escolares de comunidades favelizadas da cidade do Rio de Janeiro, Brasil. Cadernos de Saúde Pública 14, 851–855. doi: 10.1590/S0102-311X1998000400027.CrossRefGoogle Scholar
Coura, J. R., Willcox, H. P. F., Tavares, A. M., Paiva, D. D., Fernandes, O., Rada, E. L. J. C., Perez, E. P., Borges, L. C., Hidalgo, M. E. C. and Nogueira, M. L. C. (1994). Aspectos epidemiológicos, sociais e sanitários de uma área no Rio Negro, estado do Amazonas, com especial referência às parasitoses intestinais e a infecção chagásica. Cadernos de Saúde Pública 10 (Suppl. 2) S327–S336. doi: 10.1590/S0102-311X1994000800010.CrossRefGoogle Scholar
Cury, G. C., Salles, P. G. O., Reis, M. C. W., Rego, V. M., Arndt, A. W. and Souza Filho, C. B. A. (1994). Prevalência da esquistossomose mansoni e de parasitoses intestinais em escolares da área rural do município de Jaboticatubas, MG, 1992–1993. Revista da Sociedade Brasileira de Medicina Tropical 27, 217–220.CrossRefGoogle Scholar
De Carli, G. A., Mentz, M., Rott, M. B., Silva, A. C. A., Wendorff, A., Tasca, T., Castilhos, D. S., De Carli, G., Montenegro, R. A. and Mylius, L. (1997). Prevalência das enteroparasitoses na população urbana e rural da região carbonífera da cidade de Arroio dos Ratos, no Estado do Rio Grande do Sul. Revista Brasileira de Farmácia 78, 83–85.Google Scholar
Dias, R. M. D., Mangini, A. C. S., Torres, D. M. A. G. V., Vellosa, S. A. G., Silva, M. I. P. G., Silva, R. M., Corrêa, M. O. A. and Coletti, C. (1992). Ocorrência de Strongyloides stercoralis em pacientes portadores da síndrome de imunodeficiência adquirida (AIDS). Revista do Instituto de Medicina Tropical de São Paulo 34, 15–17. doi: 10.1590/S0036-46651992000100003.CrossRefGoogle ScholarPubMed
Dreyer, G., Fernandes-Silva, E., Alves, S., Rocha, A., Albuquerque, R. and Addiss, D. (1996). Patterns of detection of Strongyloides stercoralis in stool specimens: implications for diagnosis and clinical trials. Journal of Clinical Microbiology 34, 2569–2571.CrossRefGoogle ScholarPubMed
Dulley, F. L., Costa, S., Cosentino, R., Gamba, C. and Saboya, R. (2009). Strongyloides stercoralis hyperinfection after allogeneic stem cell transplantation. Bone Marrow Transplantation 43, 741–742. doi: 10.1038/bmt.2008.383.CrossRefGoogle ScholarPubMed
El-Badry, A. A. (2009). ELISA-based coproantigen in human strongyloidiasis: a diagnostic method correlating with worm burden. Journal of the Egyptian Society of Parasitology 39, 757–768.Google ScholarPubMed
Falavigna, D. L. M., Almeida, A. A., Iwazaki, R. S. and Araújo, S. M. (2008). Intestinal parasites in ecotourism region of the state of Paraná, Brazil. Brazilian Archives of Biology and Technology 51, 693–699. doi: 10.1590/S1516-89132008000400007.CrossRefGoogle Scholar
Faleiros, J. M. M., Gallo, G., Silva, M. M. K., Raful, R., Nasorri, A. R., Pipino, L. F. R., Junqueira, R. B. and Pinto, P. L. (2004). Ocorrência de enteroparasitoses em alunos de Escola Pública de Ensino Fundamental do município de Catanduva, (São Paulo, Brasil). Revista do Instituto Adolfo Lutz 63, 243–247.CrossRefGoogle Scholar
Faust, E. C., D'Antoni, J. S., Odom, V., Miller, M..J., Peres, C., Sawitz, W., Thomen, L. F., Tobie, J. and Walker, J. H. (1938). A critical study of clinical laboratory technics for the diagnosis of protozoan cysts and helminth eggs in feces. I. Preliminary communication. American Journal of Tropical Medicine 18, 169–183.Google Scholar
Feitosa, G., Bandeira, A. C., Sampaio, D. P., Badaró, R. and Brites, C. (2001). High prevalence of giardiasis and strongyloidiasis among HIV-infected patients in Bahia, Brazil. The Brazilian Journal of Infectious Diseases 5, 339–344. doi: 10.1590/S1413-86702001000600008.CrossRefGoogle ScholarPubMed
Feliciano, N. D., Gonzaga, H. T., Gonçalves-Pires, M. R. F., Gonçalves, A. L., Rodrigues, R. M., Ueta, M. T. and Costa-Cruz, J. M. (2010). Hydrophobic fractions from Strongyloides venezuelensis for use in the human immunodiagnosis of strongyloidiasis. Diagnostic Microbiology and Infectious Disease 67, 153–161. doi: 10.1016/j.diagmicrobio.2010.01.012.CrossRefGoogle ScholarPubMed
Ferreira, C. B. and Marçal Junior, O. (1997). Enteroparasitoses em escolares do distrito de Martinésia, Uberlândia, MG: um estudo-piloto. Revista da Sociedade Brasileira de Medicina Tropical 30, 373–377. doi: 10.1590/S0037-8682199700500004.CrossRefGoogle Scholar
Ferreira, C. M., Barbosa, N. S., Ferreira, W. A., Souza, R. L., Neves, M. A., Carvalho, A. L. and Barbosa, M. G. (2008). Infecção pulmonar por Strongyloides stercoralis em paciente tratado com imunosupressores. Revista de Patologia Tropical 37, 275–280.Google Scholar
Ferreira-Junior, A., Gonçalves-Pires, M. R. F., Silva, D. A., Gonçalves, A. L. and Costa-Cruz, J. M. (2006). Parasitological and serological diagnosis of Strongyloides stercoralis in domesticated dogs from southeastern Brazil. Veterinary Parasitology 136, 137–145. doi: 10.1016/j.vetpar.2005.10.022.CrossRefGoogle Scholar
Ferreira, M. S. (2003). Strongyloidiasis and acquired immunodeficiency syndrome. Enfermedades Emergentes 5, 18–26.Google Scholar
Ferreira, M. S., Nishioka, S. A., Borges, A. S., Costa-Cruz, J. M., Rossin, I. R., Rocha, A., Silvestre, M. T. and Nunes-Araújo, F. R. (1999). Strongyloidiasis and infection due to human immunodeficiency virus: 25 cases at a Brazilian teaching hospital, including seven cases of hyperinfection syndrome. Clinical Infectious Diseases 28, 154–155.CrossRefGoogle Scholar
Fontes, G., Oliveira, K. K. L., Oliveira, A. K. L. and Rocha, E. M. M. (2003). Influência do tratamento específico na prevalência de enteroparasitoses e esquistossomose mansonica em escolares do município de Barra de Santo Antônio, AL. Revista da Sociedade Brasileira de Medicina Tropical 36, 625–628. doi: 10.1590/S0037-86822003000500015.CrossRefGoogle Scholar
Fontbonne, A., Freese-de-Carvalho, E., Acioli, M. D., de Sá, G. A. and Cesse, E. A. P. (2001). Fatores de risco para poliparasitismo intestinal em uma comunidade indígena de Pernambuco, Brasil. Cadernos de Saúde Pública 17, 367–373. doi: 10.1590/311X2001000200011.CrossRefGoogle Scholar
Gennari-Cardoso, M. L., Costa-Cruz, J. M., Castro, E., Lima, L. M. F. S. and Prudente, D. V. (1996). Cryptosporidium sp. in children suffering from acute diarrhea at Uberlândia City, State of Minas Gerais, Brazil. Memórias do Instituto Oswaldo Cruz 91, 551–554. doi: 10.1590/S0074-0276199600500003.CrossRefGoogle ScholarPubMed
Genta, R. M. (1992). Dysregulation of strongyloidiasis: a new hypothesis. Clinical Microbiology Review 5, 345–355.CrossRefGoogle ScholarPubMed
Giavina-Bianchi, P., Silva, F. S., Toledo-Barros, M., Birolini, D., Kalil, J. and Rizzo, L. V. (2006). A rare intestinal manifestation in a patient with common variable immunodeficiency and strongyloidiasis. International Archives of Allergy and Immunology 140, 199–204. doi: 10.1159/000093205.CrossRefGoogle Scholar
Gioia, I. (1992). Prevalência de parasitoses intestinais entre os usuários do centro de saúde do distrito de Sousas, Campinas, São Paulo (1986–1990). Revista da Sociedade Brasileirda de Medicina Tropical 25, 177–182.CrossRefGoogle Scholar
Giraldi, N., Vidotto, O., Navarro, I. T. and Garcia, J. L. (2001). Enteroparasites prevalence among daycare and elementary school children of municipal schools, Rolândia, PR, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 34, 385–387. doi: 10.1590/S0037-86822001000400014.CrossRefGoogle ScholarPubMed
Godoy, P., Campos, C. M. C., Costa, G. and Castro, L. P. F. (1998). Associação timoma e estrongiloidíase intestinal grave. Revista da Sociedade Brasileira de Medicina Tropical 31, 481–485. doi: 10.1590/S0037-86821998000500009.CrossRefGoogle Scholar
Gonçalves, A. L. R., Machado, G. A., Gonçalves-Pires, M. R., Ferreira, A. Jr., Silva, D. A. and Costa-Cruz, J. M. (2007). Evaluation of strongyloidiasis in kennel dogs and keepers by parasitological and serological assays. Veterinary Parasitology 147, 132–139. doi: 10.1016/j.vetpar.2007.03.016.CrossRefGoogle ScholarPubMed
Gonçalves, A. L. R., Silva, C. V., Ueta, M. T. and Costa-Cruz, J. M. (2010). A new faecal antigen detection system for Strongyloides venezuelensis diagnosis in immunosuppressed rats. Experimental Parasitology 125, 338–341. doi: 10.1016/j.exppara.2010.02.015.CrossRefGoogle ScholarPubMed
Gonçalves, J. F., Tanabe, M., Medeiros, F. P. M., Gonçalves, F. J., Aca, I. S., Motta, S. B. N., Tateno, S. and Tkeuchi, T. (1990). Parasitological and serological studies on amoebiasis and other intestinal parasitic infections in the rural sector around Recife, Northeast Brazil. Revista do Instituto de Medicina Tropical de São Paulo 32, 428–435. doi: 10.1590/S0036-46651990000600007.CrossRefGoogle ScholarPubMed
Graeff-Teixeira, C., Leite, C. S. M., Sperhacke, C. L., Fassina, K., Petry, S. M. G., Mucenic, T., Pandolfi, C., Barcelos, S. and Job, F. (1997). Prospective study of strongyloidosis in patients with hematologic malignancies. Revista da Sociedade Brasileira de Medicina Tropical 30, 355–357. doi: 10.1590/S0037-86821997000500001.CrossRefGoogle ScholarPubMed
Grove, D. I. (1996). Human strongyloidiasis. Advances in Parasitolology 38, 251–309.CrossRefGoogle ScholarPubMed
Guerra, E. M., Vaz, A. J., Toledo, L. A. S., Ianoni, S. A., Quadros, C. M. S., Dias, R. M. D. and Barreto, O. C. O. (1991). Infecções por helmintos e protozoários intestinais em gestantes de primeira consulta atendidas em centros de saúde da rede estadual do subdistrito de Butantã, município de São Paulo. Revista do Instituto de Medicina Tropical de São Paulo 33, 303–308. doi: 10.1590/S0036-46651991000400010.CrossRefGoogle Scholar
Harada, U. and Mori, O. A. (1955). A new method for culturing hookworm. Yonago Acta Medica 1, 177–179.Google Scholar
Hernandez-Chavarria, F. (2001). Strongyloides stercoralis: um parásito subestimado. Parasitología al día 25, 40–49.CrossRefGoogle Scholar
Hurtado-Guerrero, A. F., Alencar, F. H. and Hurtado-Guerrero, J. C. (2005). Ocorrência de enteroparasitas na população geronte de Nova Olinda do Norte – Amazonas. Brazil. Acta Amazonica 35, 487–490. doi: 10.1590/S0044-59672005000400013.CrossRefGoogle Scholar
Keiser, P. B. and Nutman, T. B. (2004). Strongyloides stercoralis in the immunocompromised population. Clinical Microbiology Reviews 17, 208–217. doi: 10.1128/cmr.17.1208-217.2004.CrossRefGoogle ScholarPubMed
Kobayashi, J., Hasegawa, H., Forli, A. A., Nishimura, N. F., Yamana, A., Shimabukuro, T. and Sato, Y. (1995). Prevalence of intestinal parasitic infection in five farms in Holambra, São Paulo, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 37, 13–18. doi: 10.1590/S0036-46651995000100003.CrossRefGoogle ScholarPubMed
Kobayashi, J., Hasegawa, H., Soares, E. C., Toma, H., Dacal, A. R., Brito, M. C., Yamanaka, A., Foli, A. A. and Sato, Y. (1996). Studies on prevalence of Strongyloides infection in Holambra and Maceió, Brazil, by the agar plate faecal culture method. Revista do Instituto de Medicina Tropical de São Paulo 38, 279–284. doi: 10.1590/S0036-46651996000400007.CrossRefGoogle ScholarPubMed
Lam, C. S., Tong, M. K. H., Chan, K. M. and Siu, Y. P. (2006). Disseminated strongyloidiasis: a retrospective study of clinical course and outcome. European Journal of Clinical Microbiology & Infectious Diseases 25, 14–18. doi: 10.1007/S100096-005-0070-2.CrossRefGoogle ScholarPubMed
Lambertucci, J. R., Leão, F. C. C. and Barbosa, A. J. (2003). Gastric strongyloidiasis and infection by the human T cell lymphotropic virus type 1 (HTLV-1). Revista da Sociedade Brasileira de Medicina Tropical 36, 541–542. doi: 10.1590/S0037-86822003000400021.CrossRefGoogle ScholarPubMed
Lanelli, R. V., Silva, J. P. and Agostini, S. M. (1995). Parasitoses intestinais nos índios Xavánte de Parabubure, Mato Grosso, Brasil. Cadernos de Saúde Pública 11, 629–630. doi: 10.1590/S0102-311X1995000400013.CrossRefGoogle Scholar
Liu, L. X. and Weller, P. F. (1993). Strongylodiasis and other intestinal nematode infections. Infectious Diseases Clinics of North American 37, 655–682.CrossRefGoogle Scholar
Ludwig, K. M., Frei, F., Alvares Filho, F. and Ribeiro-Paes, J. T. (1999). Correlação entre condições de saneamento básico e parasitoses intestinais na população de Assis, Estados de São Paulo, Brasil. Revista da Sociedade Brasileira de Medicina Tropical 32, 547–555. doi: 10.1590/S0037-86821999000500013.CrossRefGoogle Scholar
Lutz, A. O. (1919). Schistosoma mansoni e a schistosomose, segundo observações feitas no Brazil. Memórias do Instituto Oswaldo Cruz 11, 121–155.CrossRefGoogle Scholar
Macedo, L. M. C. and Rey, L. (1996). Enteroparasitoses em gestantes e puérperas no Rio de Janeiro. Cadernos de Saúde Pública 12, 383–388. doi: 10.1590/S0102-311X199600011.CrossRefGoogle ScholarPubMed
Machado, E. R. and Costa-Cruz, J. M. (1998). Strongyloides stercoralis and other enteroparasites in children at Uberlândia city, state of Minas Gerais, Brazil. Memórias do Instituto Oswaldo Cruz 93, 161–164. doi: 10.1590/S0074-02761998000200004.CrossRefGoogle ScholarPubMed
Machado, E. R., Santos, D. S. and Costa-Cruz, J. M. (2008 a). Enteroparasites and commensals among children in four peripheral districts of Uberlândia, State of Minas Gerais. Revista da Sociedade Brasileira de Medicina Tropical 41, 581–585. doi: 10.1590/S0037-86822008000600007.CrossRefGoogle ScholarPubMed
Machado, E. R., Souza, T. S., Costa, J. and Costa-Cruz, J. M. (2008 b). Enteroparasites and commensals among individuals living in rural and urban areas in Abadia dos Dourados, Minas Gerais state, Brazil. Parasitología Latinoamericana 63, 34–39. doi: 10.4067/S0717-77122008000100006.CrossRefGoogle Scholar
Machado, E. R., Faccioli, L. H., Costa-Cruz, J. M., Lourenço, E. V., Roque-Barreira, M. C., Gonçalves-Pires, M. F. R. and Ueta, M. T. (2008 c). Strongyloides venezuelensis: the antigenic identity of eight strains for the immunodiagnosis of human strongyloidiasis. Experimental Parasitology 119, 7–14. doi: 10.1016/j.exppara.2007012.008.CrossRefGoogle ScholarPubMed
Machado, E. R., Teixeira, E. M., Gonçalves-Pires, M. R. F., Loureiro, Z. M., Araújo, R. A. and Costa-Cruz, J. M. (2008 d). Parasitological and immunological diagnosis of Strongyloides stercoralis in patients with gastrointestinal cancer. Scandinavian Journal of Infectious Diseases 40, 154–158. doi: 10.1080/00365540701558730.CrossRefGoogle ScholarPubMed
Machado, E. R., Teixeira, E. M., Paula, F. M., Gonçalves-Pires, M. R. F., Ueta, M. T. and Costa-Cruz, J. M. (2007). Immunoparasitological diagnosis of Strongyloides stercoralis in garbage collectors in Uberlândia, MG, Brazil. Parasitología Latinoamericana 62, 180–182. doi: 10.4067/S0717-77122007000200013.CrossRefGoogle Scholar
Machado, E. R., Ueta, M. T., Gonçalves-Pires, M. R. F., Oliveira, J. B. A., Faccioli, L. H. and Costa-Cruz, J. M. (2003). Strongyloides venezuelensis alkaline extract for the diagnosis of human strongyloidiasis by enzyme-linked immunosorbent assay. Memórias do Instituto Oswaldo Cruz 98, 849–851. doi: 10.1590/S0074-02762003000600024.CrossRefGoogle ScholarPubMed
Machado, E. R., Ueta, M. T., Gonçalves-Pires, M. R., Oliveira, J. B., Faccioli, L. H. and Costa-Cruz, J. M. (2001). Diagnosis of human strongyloidiasis using particulate antigen of two strains of Strongyloides venezuelensis in indirect immunofluorescence antibody test. Experimental Parasitology 99, 52–55. doi: 10.1006/j.expr.2001.4632.CrossRefGoogle ScholarPubMed
Malta, R. C. G., Waib, C. M. and Branco, A. C. Jr. (2002). Investigação epidemiológica sobre enteroparasitos em crianças em idade pré-escolar no município de Lins (SP). Revista de Patologia Tropical 31, 109–120.Google Scholar
Marcos, L. A., Terashima, A., DuPont, H. L. and Gotuzzo, E. (2008). Strongyloides hyperinfection syndrome: an emerging global infectious disease. Transactions of the Royal Society of Tropical Medicine Hygiene 102, 314–318. doi: 10.1016/j.trstmh.2008.01.020.CrossRefGoogle ScholarPubMed
Marques, C. C., Zago-Gomes, M. P., Gonçalves, C. S. and Pereira, F. E. (2010). Alcoholism and Strongyloides stercoralis: daily ethanol ingestion has a positive correlation with the frequency of Strongyloides larvae in the stools. PLoS Neglect Tropical Diseases 22, e717.CrossRefGoogle Scholar
Marra, N. M., Chiuso-Minicucci, F., Machado, G. C., Zorzella-Pezavento, S. F. G., França, T. G. D., Ishikawa, L. L. W., Amarante, A. F. T., Sartori, A. and Amarante, M. R. V. (2010). Faecal examination and PCR to detect Strongyloides venezuelensis in experimentally infected Lewis rats. Memórias do Instituto Oswaldo Cruz 105, 57–61. doi: 10.1590/S0074-027620100000100008.CrossRefGoogle ScholarPubMed
Martins, L. P. A., Serapião, A. A. T. B., Valenciano, R. F., Pires, J. E. C. and Castanho, R. E. P. (2007). Frequência de Blastocystis hominis e outras enteroparasitoses em amostras fecais analisadas no Laboratório de Parasitologia da Faculdade de Medicina de Marília-SP. Revista de Patologia Tropical 36, 47–53.Google Scholar
Mendonça, S. C., Gonçalves-Pires, M. R. F., Rodrigues, R. M., Ferreira, A. Jr. and Costa-Cruz, J. M. (2006). Is there an association between positive Strongyloides stercoralis serology and diabetes mellitus? Acta Tropica 99, 102–105. doi: 10.1016/j.actatropica.2006.06.006.CrossRefGoogle ScholarPubMed
Miné, J. C. and Rosa, J. A. (2008). Frequency of Blastocystis hominis and other intestinal parasites in stool samples examined at the Parasitology Laboratory of the School of Pharmaceutical Sciences at the São Paulo State University, Araraquara. Revista da Sociedade Brasileira de Medicina Tropical 41, 565–569. doi: 10.1590/S0037-8682200800060004.CrossRefGoogle ScholarPubMed
Minematsu, H., Hokama, A., Makishi, T., Arakaki, K., Kinjo, F. and Fujita, J. (2011). Colonoscopic findings and pathologic characteristics of Strongyloides colitis: a case series. Digestion 83, 210–214. doi: 10.1159/000321812.CrossRefGoogle ScholarPubMed
Ministério da fazenda (2007). PAC. Programa de Aceleração do Crescimento. Disponível em www.fazenda.gov.brGoogle Scholar
Miranda, R. A., Xavier, F. B. and Menezes, R. C. (1998). Parasitismo intestinal em uma aldeia indígena Parakanã, sudeste do Estado do Pará, Brasil. Cadernos de Saúde Pública 14, 507–511. doi: 10.1590/S0102-311X1998000300007.CrossRefGoogle Scholar
Monteiro, A. M. C., Silva, E. F., Almeida, K. S., Sousa, J. J. N., Mathias, L. A., Baptista, F. and Freitas, F. L. C. (2009). Parasitoses intestinais em crianças de creches públicas localizadas em bairros periféricos do município de Coari, Amazonas, Brasil. Revista de Patologia Tropical 38, 284–290.Google Scholar
Moraes, R. G. (1948). Contribuição para o estudo de Strongyloides stercoralis e da estrongiloidíase no Brasil. Revista de Saúde Pública 1, 507–624.Google Scholar
Morrone, F. B., Carneiro, J. A., Reis, C., Cardozo, C. M., Ubal, C. and De Carli, G. A. (2004). Study of enteroparasites infection frequency and chemotherapeutic agents used in pediatric patients in a community living in Porto Alegre, RS, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 46, 77–80. doi: 10.1590/S0036-46652004000200004.CrossRefGoogle Scholar
Mota-Ferreira, D. M. L., Gonçalves-Pires, M. R. F., Ferreira, A. Jr., Sopelete, M. C., Adballah, V. O. S. and Costa-Cruz, J. M. (2009). Specific IgA and IgG antibodies in paired serum and breast milk samples in human strongyloidiasis. Acta Tropica 109, 103–107. doi: 10.1016/j.actatropica.2008.09.023.CrossRefGoogle ScholarPubMed
Moura, E. C., Bragazza, L. M., Coelho, M. F. and Aun, S. M. F. (1997). Prevalência de parasitose intestinal em escolares da primeira série de uma escola publica. Jornal de Pediatria (Rio de Janeiro) 73, 406–410.CrossRefGoogle Scholar
Muniz-Junqueira, M. I. and Queiroz, F. O. (2002). Relationship between protein-energy malnutrition, vitamin A, and parasitoses in children living in Brasília. Rev Soc Bras Med Trop 2002; 35:133–141. Revista do Instituto de Medicina Tropical de São Paulo 35, 133–141. doi: 10.1590/S0037-86822002000200002.Google Scholar
Nageswaran, C., Craig, P. S. and Devaney, E. (1994). Coproantigen detection in rats experimentally infected with Strongyloides ratti. Parasitology 108, 335–342.CrossRefGoogle ScholarPubMed
Nascimento, S. A. and Moitinho, M. L. R. (2005). Blastocystis hominis and other intestinal parasites in a community of Pitanga City, Paraná State, Brazil. Rev Inst Med Trop São Paulo 2005; 47:213–217. Revista do Instituto de Medicina Tropical de São Paulo 47, 213–217. doi: 10.1590/S0036-46652005000400007.CrossRefGoogle Scholar
Nolla, A. C. and Cantos, G. A. (2005). Relação entre a ocorrência de enteroparasitoses em manipuladores de alimentos e aspectos epidemiológicos em Florianópolis, Santa Catarina, Brasil. Cadernos de Saúde Pública 21, 641–645. doi: 10.1590/S0102-311X2005000200033.CrossRefGoogle Scholar
Nunes, A. L. B., Cunha, A. M. O. and Marçal, O. Jr. (2006). Coletores de lixo e enteroparasitoses: o papel das representações sociais em suas atitudes preventivas. Ciência & Educação 12, 25–38.CrossRefGoogle Scholar
Oliveira, L. C., Ribeiro, C. T., Mendes, D. M., Oliveira, T. C. and Costa-Cruz, J. M. (2002). Frequency of Strongyloides stercoralis infection in alcoholics. Memórias do Instituto Oswaldo Cruz 97, 119–121. doi: 10.1590/S0074-02762002000100021.CrossRefGoogle ScholarPubMed
Oliveira, M. C., Silva, C. V. and Costa-Cruz, J. M. (2003). Intestinal parasites and commensals among individuals from a landless camping in the rural area of Uberlândia, Minas Gerais, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 45, 173–176. doi: 10.1590/S0036-46652003000300011.CrossRefGoogle ScholarPubMed
Olsen, A., van Lieshout, L., Marti, H., Polderman, T., Polman, K., Steinmann, P., Stothard, R., Thybo, S., Verweij, J. J. and Magnussen, P. (2009). Strongyloidiasis – the most neglected of the neglected tropical diseases? Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 967–972. doi: 10.1016/j.trstmh.2009.02.013.CrossRefGoogle ScholarPubMed
Page, W. A., Dempsey, K. and McCarthy, J. S. (2006). Utility of serological follow-up of chronic strongyloidiasis after anthelminthic chemotherapy. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 1056–1062. doi: 10.1016/j.trstmh.2005.12.006.CrossRefGoogle ScholarPubMed
Paula, F. M., Castro, E., Gonçalves-Pires, M., Marçal, M. G., Campos, D. M. and Costa-Cruz, J. M. (2000). Parasitological and immunological diagnoses of strongyloidiasis in immunocompromised and non-immunocompromised children at Uberlândia, State of Minas Gerais, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 42, 51–55. doi: 10.1590/S0036.46652000000100009.CrossRefGoogle ScholarPubMed
Pedrazzani, E. S., Mello, D. A., Pizzigatti, C. P. and Barbosa, C. A. A. (1990). Aspectos educacionais da intervenção em helmintoses intestinais, no Subdistrito de Santa Eudóxia, município de São Carlos – SP. Cadernos de Saúde Pública 6, 74–85. doi: 10.1590/S0102-311X1990000100008.CrossRefGoogle Scholar
Pires, M. L. and Dreyer, G. (1993). Revendo a importância do Strongyloides stercoralis. Revista do Hospital das Clinicas 48, 175–182.Google ScholarPubMed
Porto, A. F., Oliveira Filho, J., Neva, F. A., Orge, G., Alcântara, L., Gam, A. and Carvalho, E. M. (2001). Influence of human T-cell lymphocytotropic virus type 1 infection on serologic and skin tests for strongyloidiasis. The American Journal of Tropical Medicine and Hygiene 65, 610–613.CrossRefGoogle ScholarPubMed
Porto, M. A., Alcântara, L. M., Leal, M., Castro, N. and Carvalho, E. M. (2005). Atypical clinical presentation of strongyloidiasis in a patient co-infected with human T cell lymphotrophic virus type I. The American Journal of Tropical Medicine and Hygiene 72, 124–125.CrossRefGoogle Scholar
Porto, M. A., Muniz, A., Oliveira Júnior, J. and Carvalho, E. M. (2002). Implicações clínicas e imunológicas da associação entre o HTLV-1 e a estrongiloidíase. Revista da Sociedade Brasileira de Medicina Tropical 35, 641–649. doi: 10.1590/S0037-86822002000600016.CrossRefGoogle Scholar
Rezende, C. H. A., Costa-Cruz, J. M. and Gennari-Cardoso, M. L. (1997). Enteroparasitoses em manipuladores de alimentos de escolas públicas em Uberlândia (Minas Gerais), Brasil. Revista Panamericana de Salud Pública 2, 392–397. doi: 10.1590/S1020-49891997001200004.CrossRefGoogle Scholar
Ribeiro, M. C. M. and Marçal Júnior, O. (2003). Prevalência e fatores de risco para geo-helmintíases em escolares da zona rural de Uberlândia (MG). Revista de Patologia Tropical 32, 105–115.Google Scholar
Ritchie, L. S. (1948). An ether sedimentation technique for routine stoll examination.(1948). Bulletin of United States Army Medical Department 8, 326–334.Google Scholar
Rios, L., Cutolo, A. S., Giatti, L. L., Castro, M., Rocha, A. A., Toledo, R. F., Pelicioni, M. C. F., Barreira, L. P. and Santos, J. G. (2007). Prevalência de parasitas intestinais e aspectos socioambientais em comunidade indígena no distrito de Iauaretê, município de São Gabriel da Cachoeira (Amazonas, Brasil). Saúde e Sociedade - São Paulo 16, 76–86.CrossRefGoogle Scholar
Rocha, R. S., Silva, J. G., Peixoto, S. V., Caldeira, R. L., Firmo, J. O. A., Carvalho, O. S. and Katz, N. (2000). Avaliação da esquistossomose e de outras parasitoses intestinais, em escolares do município de Bambuí, Minas Gerais, Brasil. Revista da Sociedade Brasileira de Medicina Tropical 33, 431–436. doi: 10.1590/S0037-86822000000500004.CrossRefGoogle Scholar
Rodrigues, M. A., Fróes, R. C., Anefalos, A. and Kobayasi, S. (2001). Invasive enteritis by Strongyloides stercoralis presenting as acute abdominal distress under corticosteroid therapy. Revista do Hospital das Clinicas 56, 103–106. doi: 10.1590/S0041-87812001000400002.CrossRefGoogle ScholarPubMed
Rodrigues, R. M., Oliveira, M. C., Sopelete, M. C., Silva, D. A., Campos, D. M., Taketomi, E. A. and Costa-Cruz, J. M. (2007). IgG1, IgG4 and IgE antibody responses in human strongyloidiasis by ELISA using Strongyloides ratti saline extract as heterologous antigen. Parasitology Research 101, 1209–1214. doi: 10.1007/s00436-007-0602-2.CrossRefGoogle ScholarPubMed
Rodrigues, R. M., Sopelete, M. C., Silva, D. A., Cunha-Junior, J. P., Taketomi, E. A. and Costa-Cruz, J. M. (2004). Strongyloides ratti antigenic components recognized by IgE antibodies in immunoblotting as an additional tool for improving the immunodiagnosis in human strongyloidiasis. Memórias do Instituto Oswaldo Cruz 99, 89–93. doi: 10.1590/50074-02762004000100016.CrossRefGoogle ScholarPubMed
Rossi, C. L., Partel, C. D., Teixeira, A. L., Takahashi, E. E., De Barros-Mazon, S. and Da Silva, L. J. (1993). Strongyloidiasis in Campinas city region (Brazil). Parasitological and serological data. Tropical and Geographical Medicine 45, 189–190.Google ScholarPubMed
Rossi, C. L., Takahashi, E. E., Teixeira, A. L., de Barros-Mazon, S. and Trevisa, R. G. (1193). Avaliação de preparações antigênicas de Strongyloides stercoralis para o imunodiagnóstico da estrongiloidíase. Revista da Sociedade Brasileira de Medicina Tropical 26, 83–87.CrossRefGoogle Scholar
Rugai, E., Mattos, T. and Brisola, A. P. (1954). Nova técnica para isolar larvas de nematóides das fezes – modificação do método de Baermann. Revista do Instituto Adolfo Lutz 14, 5–8.CrossRefGoogle ScholarPubMed
Safdar, A., Malathum, K., Rodriguez, S. J., Husni, R. and Rolston, K. V. I. (2004). Strongyloidiasis in patients at a comprehensive cancer center in the United States: a retrospective study covering the years 1971–2003. Cancer 100, 1531–1536. doi: 10.1002/cncr.20120.CrossRefGoogle Scholar
Salluh, J. I. F., Bozza, F. A., Pinto, T. S., Toscano, L., Wellers, P. F. and Soares, M. (2005). Cutaneous periumbilical purpura in disseminated strongyloidiasis in cancer patients: a pathognomonic feature of potentially lethal disease? Brazilian Journal of Infectious Diseases 9, 419–424. doi: 10.1590/S1413-86702005000500010.Google ScholarPubMed
Santos, L. P., Santos, F. L. N. and Soares, N. M. (2007). Prevalência de parasitoses intestinais em pacientes atendidos no Hospital Universitário Professor Edgar Santos, Salvador, Bahia. Revista de Patologia Tropical 36, 237–246.Google Scholar
Santos, M. C., Costa-Cruz, J. M., Carvalho-Neto, C., Lima, M. M. R. and Cristina, M. (1998). Enteric parasites and commensals in pregnant women seen at the University Hospital, Federal University of Uberlândia, State of Minas Gerais, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 40, 193–196. doi: 10.1590/S0036-46651998000300011.CrossRefGoogle ScholarPubMed
Santos, R. V., Coimbra, C. E. A. Jr., Flowers, N. M. and Silva, J. P. (1995). Intestinal parasitism in the Xavánte indians, Central Brazil. Revista do Instituto de Medicina Tropical de São Paulo 37, 145–148. doi: 10.1590/S0036-46651995000200009.CrossRefGoogle ScholarPubMed
Sato, Y., Kobayashi, J. and Shiroma, Y. (1995). Serodiagnosis of strongyloidiasis. The application and significance. Revista do Instituto de Medicina Tropical São Paulo 37, 35–41. doi: 10.1590/S0036-4665199500010000.6.CrossRefGoogle ScholarPubMed
Schaffel, R., Nucci, M., Carvalho, E., Braga, M., Almeida, L., Portugal, R. and Pulcheri, W. (2001). The value of an immunoenzymatic test (enzyme-linked immunosorbent assay) for the diagnosis of strongyloidiasis in patients immunosuppressed by hematologic malignancies. The American Journal of Tropical Medicine and Hygiene 65, 346–350.CrossRefGoogle ScholarPubMed
Siddiqui, A. A. and Berk, S. L. (2003). Strongyloidiasis. Current Treatment Options in Infectious Diseases 5, 283–289.Google Scholar
Silva, C. V., Ferreira, M. S., Borges, A. S. and Costa-Cruz, J. M. (2005). Intestinal parasitic infections in HIV/AIDS patients: experience at a teaching hospital in central Brazil. Scandinavian Journal of Infectious Diseases 37, 211–215. doi: 10.1080/00365540410020875.CrossRefGoogle Scholar
Silva, E. F., Silva, E. B., Almeida, K. S., Sousa, J. J. N. and Freitas, F. L. C. (2009). Enteroparasitoses em crianças de áreas rurais do município de Coari, Amazonas, Brasil. Revista de Patologia Tropical 38, 35–43.Google Scholar
Silva, L. P., Barcelos, I. S., Passos-Lima, A. B., Espindola, F. S., Campos, D. M. and Costa-Cruz, J. M. (2003). Western blotting using Strongyloides ratti antigen for the detection of IgG antibodies as confirmatory test in human strongyloidiasis. Memórias do Instituto Oswaldo Cruz 98, 687–691. doi: 10.1590/S0074-02762003000500017.CrossRefGoogle ScholarPubMed
Souza, E. A., Silva-Nunes, M., Malafronte, R. S., Muniz, P. T., Cardoso, M. A. and Ferreira, M. U. (2007). Prevalence and spatial distribution of intestinal parasitic infections in a rural Amazonian settlement, Acre State, Brazil. Cadernos de Saúde Pública 23, 427–434. doi: 10.1590/S0102-311X2007000200019.CrossRefGoogle Scholar
Sudré, A. P., Macedo, H. W., Peralta, R. H. S. and Peralta, J. M. (2006). Diagnóstico da estrongiloidíase humana: importância e técnicas. Revista de Patologia Tropical 35, 173–184.Google Scholar
Sudré, A. P., Siqueira, R. C., Barreto, M. G., Peralta, R. H., Macedo, H. W. and Peralta, J. M. (2007). Identification of a 26-kDa protein fraction as an important antigen for application in the immunodiagnosis of strongyloidiasis. Parasitology Research 101, 1117–1123. doi: 10.1007/s00436-007-0596-6.CrossRefGoogle ScholarPubMed
Tavares, A. M. (2000). Prevalência da estrongiloidíase na sede de dez municípios do Estado do Amazonas e sua relação com a composição físico química do solo e da água. Revista da Sociedade Brasileira de Medicina Tropical 33, 107–108. doi: 10.1590/50037-86822000000100022.CrossRefGoogle Scholar
Tavares-Dias, M. and Grandini, A. A. (1999). Prevalência e aspectos epidemiológicos de enteroparasitoses na população de São José da Bela Vista, São Paulo. Revista da Sociedade Brasileira de Medicina Tropical 32, 63–65. doi: 10.1590/50037-86821999000100012.CrossRefGoogle Scholar
Takayanagui, O. M., Lofrano, M. M., Araújo, M. B. and Chimelli, L. (1995). Detection of Strongyloides stercoralis in the cerebrospinal fluid of a patient with acquired immunodeficiency syndrome. Neurology 45, 193–194.CrossRefGoogle ScholarPubMed
Tietz Marques, S. M., Bandeira, C. and Marinho de Quadros, R. (2005). Prevalência de enteroparasitoses em Concórdia, Santa Catarina, Brasil. Parasitología Latinoamericana 60, 78–81. doi: 10.4067/S0717-77122005000100014.CrossRefGoogle Scholar
Toledo, M. J. O., Paludetto, A. W., Moura, F. T., Nascimento, E. S., Chaves, M., Araújo, S. M. and Mota, L. T. (2009). Avaliação de atividades de controle para enteroparasitoses em aldeia Kaingáng do Paraná. Revista de Saúde Pública 43, 981–990. doi: 10.1590/S0034-89102009005000083CrossRefGoogle Scholar
Uparanukraw, P., Phongsri, S. and Morakote, N. (1999). Fluctuations of larval excretion in Strongyloides stercoralis infection. The American Journal of Tropical Medicine and Hygiene 60, 967–973.CrossRefGoogle ScholarPubMed
Valar, C., Keitel, E., Dal Prá, R. L., Gnatta, D., Santos, A. F., Bianco, P. D., Sukienni, T. C. T., Pegas, K. L., Bittar, A. E., Oliveira, K. T. and Garcia, V. D. (2007). Parasitic infection in renal transplant recipients. Transplantation Proceedings 39, 460–462. doi: 10.1016/j.transproceed.2007.01.025.CrossRefGoogle ScholarPubMed
Varatharajalu, R., Parandaman, V., Ndao, M., Andersen, J. F. and Neva, F. A. (2011). Strongyloides stercoralis excretory/secretory protein strongylastacin specifically recognized by IgE antibodies in infected human sera. Microbiology and Immunology 55, 115–122. doi: 10.1111/j.1348.0421.2010.00289.x.CrossRefGoogle ScholarPubMed
Veloso, M. G. P., Porto, A. S. and Moraes, M. (2008). Hiperinfecção por Strongyloides stercoralis: relato de caso autopsiado. Revista da Sociedade Brasileira de Medicina Tropical 41, 413–415. doi: 10.1590/S0037-86822008000400018.CrossRefGoogle Scholar
Verweij, J. J., Canales, M., Polman, K., Ziem, J., Brienen, E. A., Polderman, A. M. and van Lishout, L. (2009). Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Transactions of the Royal Society of Tropical Medicine and Hygiene 103, 342–346. doi: 10.1016/j.trstmh.2008.12.001.CrossRefGoogle ScholarPubMed
Vilela, E. G., Clemente, W. T., Mira, R. R. L., Torres, H. O. G., Veloso, L. F., Fonseca, L. P., Fonseca, L. R. C., França, M. C. and Lima, A. S. (2009). Strongyloides stercoralis hyperinfection syndrome after liver transplantation: case report and literature review. Transplant Infectious Disease 11, 132–136. doi: 10.1111/j.1399-3062.2008.00350.x.CrossRefGoogle ScholarPubMed
Willcox, H. P. and Coura, J. R. (1991). The efficiency of Lutz, Kato-Katz and Baermann-Moraes (adapted) techniques association to the diagnosis of intestinal helminths. Memórias do Instituto Oswaldo Cruz 86, 457–460. doi: 10.1590/50074-02761991000400015.CrossRefGoogle Scholar
World Health Organization (2005). Deworming for health and development. WHO Report of the third global meeting of the partners for parasite control. CDS/PVC/2005.14, Geneva.Google Scholar
Zago-Gomes, M. P., Aikawa, K. F., Perazzio, S. F., Gonçalves, C. S. and Pereira, F. E. (2002). Prevalence of intestinal nematodes in alcoholic patients. Revista da Sociedade Brasileira de Medicina Tropical 35, 571–571. doi: 10.1590/50037-86822002000600004.CrossRefGoogle ScholarPubMed
Figure 0

Fig. 1. Changes in the prevalence of Strongyloides stercoralis in Brazil in the period 1990–2009 as assessed by parasitological methods of diagnosis.

Figure 1

Table 1. Occurrence of Strongyloides stercoralis infection in humans, considering the parasitological diagnosis, region, state and population in Brazil from 1990 to 2009

(% Positive parasitological methods, without discrimination of rural and urban general, All (studies without discrimination of age).)
Figure 2

Fig. 2. Changes in the prevalence of Strongyloides stercoralis, by the age of the Brazilian population, in the period 1990–2009 as assessed by parasitological methods of diagnosis. * The population was not weighted by the age distribution of the sampled members.

Figure 3

Table 2. Occurrence of Strongyloides stercoralis infection in humans using parasitological methods and/or serological diagnosis, distributed according to the type of immunosuppression (1990–2009)