Strongyloides stercoralis and other Enteroparasites in Children at Uberlândia City, State of Minas Gerais, Brazil

Rodrigues Machado, Eleuza; Costa-Cruz, Julia Maria

doi:10.1590/S0074-02761998000200004

Abstract

To evaluate the rate of infection by Strongyloides stercoralis and other enteroparasites a survey was conducted in the city of Uberlândia, State of Minas Gerais, Brazil. A total of 900 stool samples from 300 children aging from four months to seven years, randomly selected in ten nursery schools from September 1994 to December 1995, were examined, both by the Baermann-Moraes and Lutz methods. Thirty nine children (13%) were found to be infected by S. stercoralis, 64.1% were boys and 35.9% were girls. Taking all the enteroparasites as a whole the results of the survey pointed out that 265 (88.4%) of the 300 children were infected by the following: Giardia lamblia, 78.3%; Ascaris lumbricoides, 15.3%; S. stercoralis, 13%; Hymenolepis nana, 6.7%; hookworms, 6%; Enterobius vermicularis, 4%; Hymenole-pis diminuta, 4% and Trichuris trichiura, 0.7%. From 265 infected children 64.5% were mono-infected, 27.2% were infected by two parasites and 8.3% had a poly-specific parasite burden. It was concluded that strongyloidiasis is hyperendemic in this area

Strongyloides stercoralis; intestinal parasites; children; Brazil

Strongyloides stercoralis and other Enteroparasites in Children at Uberlândia City, State of Minas Gerais, Brazil

Vol. 93(2): 161-164

Eleuza Rodrigues Machado, Julia Maria Costa-Cruz⁺

Laboratório de Parasitologia, Departamento de Patologia, Universidade Federal de Uberlândia, Av. Pará 1720, 38400-902 Uberlândia, MG, Brasil

To evaluate the rate of infection by Strongyloides stercoralis and other enteroparasites a survey was conducted in the city of Uberlândia, State of Minas Gerais, Brazil. A total of 900 stool samples from 300 children aging from four months to seven years, randomly selected in ten nursery schools from September 1994 to December 1995, were examined, both by the Baermann-Moraes and Lutz methods. Thirty nine children (13%) were found to be infected by S. stercoralis, 64.1% were boys and 35.9% were girls. Taking all the enteroparasites as a whole the results of the survey pointed out that 265 (88.4%) of the 300 children were infected by the following: Giardia lamblia, 78.3%; Ascaris lumbricoides, 15.3%; S. stercoralis, 13%; Hymenolepis nana, 6.7%; hookworms, 6%; Enterobius vermicularis, 4%; Hymenole-pis diminuta, 4% and Trichuris trichiura, 0.7%. From 265 infected children 64.5% were mono-infected, 27.2% were infected by two parasites and 8.3% had a poly-specific parasite burden. It was concluded that strongyloidiasis is hyperendemic in this area.

Key words: Strongyloides stercoralis - intestinal parasites - children - Brazil

Strongyloidiasis has heterogenic worldwide distribution, with three world regions, according to the predominance of the infection by Strongyloides stercoralis (Bavay, 1876): sporadic (<1%), endemic (1-5%) and hyperendemic (>5%) (Stuerchler 1981 apud Pires & Dreyer 1993).

The occurrence of S. stercoralis in children aged from 0-14 years in some Brazilian states is summarized in Table I.

This study aimed at surveying the prevalence of S. stercoralis and other enteroparasites in nursing school children aging from four months to seven years, in Uberlândia, State of Minas Gerais, Brazil, from September 1994 to December 1995.

In 1994 Uberlândia had 49 nursery schools, from these ten were taken at random. The size of the sample was calculated according to the formula: n = Z²x P x Q/d² (Rodrigues 1986) considering (Z) of 95%; (d) of 5%; (P) of 10%, obtained in a pilot study in three nursery schools, and a non-observed value (Q) of 90%; with the size of the sample (n) evaluated at 138 persons. This sample was amplified and 300 children were selected at random, 30 at each of the pre-determined school; these children were later identified according to sex and age following the agreement of their parents or tutors for their participation.

Three fecal samples from each child were collected in plastic vials without preservatives with intervals of four to six days. The samples were stored in boxes with ice and analyzed at the Laboratory of Parasitology of the Universidade Federal de Uberlândia by the methods of Baermann and Moraes (BM) (Baermann 1917, Moraes 1948) and Lutz (Lutz 1919). For more adequate reading of the slides the larvae were fixed using 0.2 ml of a 10% solution of formalin applied to the residue of the first method. Five slides were prepared for the BM analysis and six for the Lutz analysis for each of the 900 samples. The total number of slides examination was thus 9900.

All the families of the children received the results of the laboratory diagnosis. The positive cases were referred to the Pediatric Polyclinic, where they received specific treatment.

The data were processed using the analysis of variance (Anova) and the Students' t according to Malleta (1992).

S. stercoralisinfection - From the 300 children studied 39 (13%) were infected with larvae of S. stercoralis in one of the three periods sampled. Of these cases, 28 cases were detected only by BM method (71.8%), nine of them only by the Lutz' method (23.1%) and two by both methods (5.1%). These differences were statistically significant by Anova, GL 2 and 6. Of these 39 cases nine (23%) were diagnosed only in the first sample; one (2.6%) in the first and third; one (2.6%) in all three samples; 14 cases (35.9%) in the second sample and 14 (35.9%) only in the third sample. These variations were not statistically significant by Anova GL 2 and 6. Regarding sex 25 (64.1%) cases of S. stercoralis were detected in boys and 14 (35.9%) in girls. Children in all ages were infected, except in those from zero up to one year. Table II has the number of children studied and test results by age category. There was no statistically significant difference in rates of infection by sex or age. Positive cases of S. stercoralis varied from 3.3% to 23.3% in the ten nursery schools.

Other enteroparasites - Of the 300 children studied 149 (49.7%) were boys and 151, girls (50.3%). Of these 265 (88.4%) were infected: 132 (49.8%) were boys and 133 (50.2%) were girls. The distribution of parasites, (excluding the positive children from the other sample) is represented in Table III. There were 171 (64.5%) children mono-infected; 72 (27.2%) bi-infected and 22 (8.3%) poly-infected. From the bi and poly-infected children there were 32 associated infections of S. stercoralis: Giardia lamblia, Stiles, 1915, in 17 cases (53.1%); Ascaris lumbricoides, Linnaeus, 1758, in four (12.5%); hookworms either Ancylostoma duodenale (Dubini, 1843) or Necator americanus, Stiles, 1903, in one (3.1%); Hymenolepis nana (Siebold, 1852) in one (3.1%); together with G. lamblia and A. lumbricoides in five (15.6%); G. lamblia and hookworms in two (6.2%); G. lamblia and H. nana in one (3.1%) and G. lamblia and Enterobius vermicularis (Linnaeus, 1771) in one (3.1%).

To the present time the records of children infected with S. stercoralis in the city of Uberlândia varied from zero (Berbert-Ferreira & Costa-Cruz 1995) and 2.1% (Gennari-Cardoso et al. 1996). Both of these studies were conducted using only one sample per case and using only the Lutz' method.

Using the procedure of three samples per child and two methods for diagnosis the rate of infection was found to be considerably increased, 13%. It is recommend that for effective diagnosis three samples are necessary: 71.8% of the cases in the present research were identified only in second and third samples. Additionally, the BM method was able to identify the infection in 30 (76.9%) of children studied.

No children of the 0-1 age category were found to be infected with S. stercoralis compatible with other research previously published: Marzochi and Carvalheiro (1978), Almeida and Costa-Cruz (1988), Berbert-Ferreira and Costa-Cruz (1995), Guimarães and Sogayar (1995). In the other age categories the rate of positive cases varied from 10.3% to 20.5% for S. stercoralis involving, 10.9% to 19% of children, indicating that this parasite is hyperendemic in the city.

In terms of other detected enteroparasites the rate of infection (88.4%) was classified as severe considering the damage that these etiologic entities may inflict on their hosts. This rate of infection is the highest found so far in this city, even when other age categories have been included (Costa-Cruz et al. 1991, Sá & Costa-Cruz 1991, Berbert-Ferreira & Costa-Cruz 1995, Costa-Cruz et al. 1996, Gennari-Cardoso et al. 1996). G. lamblia was the only pathogenic protozoon detected (235 cases). Seven species of helminthes were identified, of which A. lumbricoides presented the highest rate: 15.3%. The occurrence of 35.5% of children infected by more than one parasite demonstrated that enteroparasites represent a serious problem to the public health of Uberlândia.

To Maria Cristina Mouta Rink for statistical analysis, to Prof. Dr Uriel Franco Rocha and Dr David G Francis for suggestions.

Supported by CAPES.

⁺Corresponding author. Fax: +55-34-218.2333

Received 10 July 1997

Accepted 17 November 1997

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REFERENCES Albuquerque LMM, Cavalcanti-Junior CB, Ribeiro MD 1990. Eosinofilia sangüínea em crianças com helmintíases intestinais. Rev Anál Clin 22: 26-30.
Almeida IS 1992. Prevalęncia de Giardia lamblia em populaçăo infantil e condiçőes ambientais no bairro Nossa Senhora de Fátima, Planaltina, D.F. Bras Méd 29: 5-10.
Almeida LP, Costa-Cruz JM 1988. Incidęncia de enteroparasitas em habitantes do município de Araguari, Minas Gerais. Rev Cen Ci Bioméd Univ Fed Uberlândia 4: 9-17.
Alonso MT 1967. Incidęncia de protozooses e helmintoses intestinais em crianças no Triângulo Mineiro. Hospital 72: 315-320.
Alves JGB, Ferreira OS, Rocha JA 1982. Parasitoses intestinais em crianças atendidas no Ambulatório do Instituto Materno Infantil de Pernambuco (IMIP). J Pediat Rio de Janeiro 52: 15-16.
Baermann G 1917. Eine Einfache Methode zur Auffindung von Ankylostomum (Nematoden) Larven in Erdproben. Mededeel mit h. Geneesk. Lab Weltvreden Feestbundel, Batavia, p. 41-47.
Berbert-Ferreira M, Costa-Cruz JM 1995. Parasitas intestinais em lactentes de 4 a 12 meses, usuários das creches da Universidade Federal de Uberlândia, Minas Gerais. J Pediatr Rio de Janeiro 71: 219-222.
Cavalcanti-Junior GB, Ribeiro MD, Brito TNS, Araujo MCPE, Medeiros MCC 1987. Freqüęncia de parasitoses intestinais numa amostra da populaçăo infantil do Rio Grande do Norte. Rev Bras Anál Clin 19: 75-76.
Costa-Cruz JM, Ambrósio MR, Marques DE, Gennari-Cardoso ML, Couto JDV 1991. Inquérito coproparasitológico em escolares de Uberlândia, MG. Rev Soc Bras Med Trop 24 (Suppl. II): 141.
Costa-Cruz JM, Ferreira MS, Rossin IR 1996. Intestinal parasites in AIDS and +HIV patients in Uberlândia, Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 91: 685-686.
Cutrim-Junior RJC, Fonseca PHM, Carneiro SFM 1985. Prevalęncia de entero-helmintos em pré-escolares e escolares do bairro da Vila Palmeira, Săo Luís - MA. Arq Bras Med 59: 467-468.
Ferraroni MJR, Montoril-Filho M, Ferraroni JJ 1979. Parasitas intestinais numa populaçăo humana da cidade de Nova Olinda do Norte, Amazonas. Acta Amazônica 9: 657-659.
Gennari-Cardoso ML, Costa-Cruz JM, Castro E, Lima LMFS, Prudente DV 1996. Cryptosporidium sp. in children suffering from acute diarrhea at Uberlândia city, State of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 91: 551-552.
Guimarăes S, Sogayar MJL 1995. Occurrence of Giardia lamblia in children of municipal day-care centers from Botucatu, Săo Paulo State, Brazil. Rev Inst Med Trop Săo Paulo 37: 501-506.
Latorraca MQ, Meirelles SMP, Marchini JS 1988. Indicadores das condiçőes nutricionais na regiăo polonoroeste. V: desnutriçăo proteico-energética e parasitoses intestinais em um grupo de crianças de 3 a 72 meses de idade da cidade de Mirassol d'oeste, Mato Grosso, Brasil. Rev Inst Med Trop Săo Paulo 30: 192-196.
Lutz AV 1919. Schistosoma mansoni e a schistosomose, segundo observaçőes feitas no Brasil. Mem Inst Oswaldo Cruz 11: 121-125.
Maletta CHM 1992. Bioestatística em Saúde Pública 2nd. ed., Coopmed, Belo Horizonte, MG, 301 pp.
Marzochi MC, Carvalheiro JR 1978. Estudos dos fatores envolvidos na disseminaçăo dos enteroparasitas. Rev Inst Med Trop Săo Paulo 20: 31-35.
Moraes RG 1948. Contribuiçăo para o estudo do Strongyloides stercoralis e da estrongiloidíase no Brasil. Rev Saú Públ 1: 507-624.
Okazaki M, Miranda P, Neto J, Diegues V, Alves J, Machado C, Tanabe M, Kobayashi S, Kaneto N, Nagakura K, Kobayashi M, Motta S, Taneto S, Takeuchi T 1988. Parasitological and serological studies on amoebiasis and other intestinal parasitic infections in Recife and its suburban area, Northeast - Brazil. Rev Inst Med Trop Săo Paulo 30: 313-321.
Pires ML, Dreyer G 1993. Revendo a importância do Strongyloides stercoralis Rev Hosp Clin Fac Med Săo Paulo 48: 175-182.
Rodrigues PC 1986. Bioestatística, Ed. Universitária, Niterói, RJ, 227 pp.
Sá MAR, Costa-Cruz JM 1991. Incidęncia de enteroparasitas nos centros de saúde do município de Uberlândia-MG, no ano de 1988. Rev Soc Bras Med Trop 24 (Suppl. II): 141.
Santos MAQ, Paçô JM, Isac E, Alves EL, Vieira MA 1990. Prevalęncia estimada de parasitas intestinais em escolares de creches e estabelecimentos de ensino em Goiânia - Goiás. Rev Patol Trop Goiânia 19: 35-45.

Publication Dates

Publication in this collection
08 Oct 1998
Date of issue
Mar 1998

History

Accepted
17 Nov 1997
Received
10 July 1997

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] REFERENCES Albuquerque LMM, Cavalcanti-Junior CB, Ribeiro MD 1990. Eosinofilia sangüínea em crianças com helmintíases intestinais. Rev Anál Clin 22: 26-30.

[2] Almeida IS 1992. Prevalęncia de Giardia lamblia em populaçăo infantil e condiçőes ambientais no bairro Nossa Senhora de Fátima, Planaltina, D.F. Bras Méd 29: 5-10.

[3] Almeida LP, Costa-Cruz JM 1988. Incidęncia de enteroparasitas em habitantes do município de Araguari, Minas Gerais. Rev Cen Ci Bioméd Univ Fed Uberlândia 4: 9-17.

[4] Alonso MT 1967. Incidęncia de protozooses e helmintoses intestinais em crianças no Triângulo Mineiro. Hospital 72: 315-320.

[5] Alves JGB, Ferreira OS, Rocha JA 1982. Parasitoses intestinais em crianças atendidas no Ambulatório do Instituto Materno Infantil de Pernambuco (IMIP). J Pediat Rio de Janeiro 52: 15-16.

[6] Baermann G 1917. Eine Einfache Methode zur Auffindung von Ankylostomum (Nematoden) Larven in Erdproben. Mededeel mit h. Geneesk. Lab Weltvreden Feestbundel, Batavia, p. 41-47.

[7] Berbert-Ferreira M, Costa-Cruz JM 1995. Parasitas intestinais em lactentes de 4 a 12 meses, usuários das creches da Universidade Federal de Uberlândia, Minas Gerais. J Pediatr Rio de Janeiro 71: 219-222.

[8] Cavalcanti-Junior GB, Ribeiro MD, Brito TNS, Araujo MCPE, Medeiros MCC 1987. Freqüęncia de parasitoses intestinais numa amostra da populaçăo infantil do Rio Grande do Norte. Rev Bras Anál Clin 19: 75-76.

[9] Costa-Cruz JM, Ambrósio MR, Marques DE, Gennari-Cardoso ML, Couto JDV 1991. Inquérito coproparasitológico em escolares de Uberlândia, MG. Rev Soc Bras Med Trop 24 (Suppl. II): 141.

[10] Costa-Cruz JM, Ferreira MS, Rossin IR 1996. Intestinal parasites in AIDS and +HIV patients in Uberlândia, Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 91: 685-686.

[11] Cutrim-Junior RJC, Fonseca PHM, Carneiro SFM 1985. Prevalęncia de entero-helmintos em pré-escolares e escolares do bairro da Vila Palmeira, Săo Luís - MA. Arq Bras Med 59: 467-468.

[12] Ferraroni MJR, Montoril-Filho M, Ferraroni JJ 1979. Parasitas intestinais numa populaçăo humana da cidade de Nova Olinda do Norte, Amazonas. Acta Amazônica 9: 657-659.

[13] Gennari-Cardoso ML, Costa-Cruz JM, Castro E, Lima LMFS, Prudente DV 1996. Cryptosporidium sp. in children suffering from acute diarrhea at Uberlândia city, State of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 91: 551-552.

[14] Guimarăes S, Sogayar MJL 1995. Occurrence of Giardia lamblia in children of municipal day-care centers from Botucatu, Săo Paulo State, Brazil. Rev Inst Med Trop Săo Paulo 37: 501-506.

[15] Latorraca MQ, Meirelles SMP, Marchini JS 1988. Indicadores das condiçőes nutricionais na regiăo polonoroeste. V: desnutriçăo proteico-energética e parasitoses intestinais em um grupo de crianças de 3 a 72 meses de idade da cidade de Mirassol d'oeste, Mato Grosso, Brasil. Rev Inst Med Trop Săo Paulo 30: 192-196.

[16] Lutz AV 1919. Schistosoma mansoni e a schistosomose, segundo observaçőes feitas no Brasil. Mem Inst Oswaldo Cruz 11: 121-125.

[17] Maletta CHM 1992. Bioestatística em Saúde Pública 2nd. ed., Coopmed, Belo Horizonte, MG, 301 pp.

[18] Marzochi MC, Carvalheiro JR 1978. Estudos dos fatores envolvidos na disseminaçăo dos enteroparasitas. Rev Inst Med Trop Săo Paulo 20: 31-35.

[19] Moraes RG 1948. Contribuiçăo para o estudo do Strongyloides stercoralis e da estrongiloidíase no Brasil. Rev Saú Públ 1: 507-624.

[20] Okazaki M, Miranda P, Neto J, Diegues V, Alves J, Machado C, Tanabe M, Kobayashi S, Kaneto N, Nagakura K, Kobayashi M, Motta S, Taneto S, Takeuchi T 1988. Parasitological and serological studies on amoebiasis and other intestinal parasitic infections in Recife and its suburban area, Northeast - Brazil. Rev Inst Med Trop Săo Paulo 30: 313-321.

[21] Pires ML, Dreyer G 1993. Revendo a importância do Strongyloides stercoralis Rev Hosp Clin Fac Med Săo Paulo 48: 175-182.

[22] Rodrigues PC 1986. Bioestatística, Ed. Universitária, Niterói, RJ, 227 pp.

[23] Sá MAR, Costa-Cruz JM 1991. Incidęncia de enteroparasitas nos centros de saúde do município de Uberlândia-MG, no ano de 1988. Rev Soc Bras Med Trop 24 (Suppl. II): 141.

[24] Santos MAQ, Paçô JM, Isac E, Alves EL, Vieira MA 1990. Prevalęncia estimada de parasitas intestinais em escolares de creches e estabelecimentos de ensino em Goiânia - Goiás. Rev Patol Trop Goiânia 19: 35-45.