INTRODUCTION
Cryptosporidiosis in an enteric disease caused by a coccidian parasite of the genus Cryptosporidium, which includes several species that affect wild and domestic mammals such as calves, cats, and dogs, as well as humans.1–4 Initially described in mice,5 this parasite was first reported in humans in 19766 and was associated with immune compromised hosts. Cryptosporidiosis is regarded as an emerging diarrheic disease that characteristically produces 6–8 watery diarrheic episodes per day, which define a clinical picture of acute diarrhea.7,8 Since first being reported, cryptosporidiosis has been detected in patients with several immune impairments such as acquired immunodeficiency syndrome,9–11 diabetes mellitus,12 acute leukemia and other hematologic disorders,13,14 interferon deficiencies,15 graft transplants,16 hospitalized and malnourished children,17 and populations living with health risks factors.18–25 Poverty, unsafe drinking water, and poor housing and education in developing countries facilitate gastrointestinal infections, mainly affecting from newborn to 12 years old children who usually have abdominal pain, acute diarrhea, nausea, vomiting, fever, and dehydration.10,18,26 Malnourished, non–breast-fed children, those less than six months old, and those living in poor hygienic environments are most affected.27 In developing countries, many outbreaks of diarrheal diseases have been associated with contaminated drinking water,21,22,28,29 while in the United States, Canada, and the United Kingdom, cryptosporidiosis outbreaks have been associated with swimming pool users and defective treatment of water supplies.30–34 However, Cryptosporidium is not the only pathogen causing acute diarrhea because other protozoa such as Giardia lamblia, Entamoeba histolytica, Cyclospora, and Enterocytozoon have also been identified in patients with diarrheal disease, and combinations of these parasites have occasionally been isolated from the same patients.35–38
There are few reports on the prevalence of cryptosporidiosis in Mexico. Therefore, we conducted a parasitologic study in children with diarrhea and other clinical symptoms. The main objectives were 1) to determine the prevalence of cryptosporidiosis in children less than one year of age in Mexico City, and 2) to correlate Cryptosporidium infection with gastrointestinal symptoms.
MATERIALS AND METHODS
Two hundred children in Mexico City less than one year of age who were seen at the Gabriel Mancera Familiar Medicine Unit of the Instituto Mexicano del Seguro Social were included in the study. The population was divided into two groups. Group A was composed of 100 children seen at the emergency service for acute diarrheic disease, and group B was composed of 100 healthy children seen for periodic check ups. All children’s parents were informed and asked to give their consent. One rectal fecal sample per child was obtained to yield 200 samples. Each fecal sample was smeared on three clean slides, stained by the modified Kinyoun acid-fast technique,39 and observed by light microscopy at magnifications of 100×, 400×, and 1,000×.
RESULTS
Forty-four of 100 children in group A had protozoan cysts or oocysts. Of the 44 protozoa-positive cases, Cryptosporidium oocysts were detected in 18 (41%) (Figure 1), G. lamblia in 22 (50%) (Figure 2), and E. histolytica in 4 (9%) (Figure 3). The signs and symptoms found in the patients with these parasites are shown in Table 1. The incidence of Cryptosporidium infection was higher in males (77.78%) than in females (22.22%), while that of G. lamblia was higher in females (81%) than in males (0.88%). However, E. histolytica did not show a difference in distribution by sex (50% in males and 50% in females). Although the other 56 children in group A had no parasitic protozoan infections, they had the same signs and symptoms as the positive cases. Abdominal distension was present in most cases (57.14%), followed by vomiting (46.43%), fever (42.85%), dehydration (21.43%), and blood in the feces (7.14%). No intestinal parasites were detected in the children in group B.
DISCUSSION
The important role played by Cryptosporidium spp. in diarrheic diseases affecting children in developing countries is well known. Although many immunodeficient individuals are infected by this parasite, it is not uncommon to find it in infants with a normal immune status in whom the infections may be either asymptomatic or self limited.40 In rural areas of Mexico, a high prevalence of infections with Cryptosporidium has been sporadically reported,41 but this infection is also endemic in urban environments.
Our findings demonstrate a high incidence of acute Cryptosporidium infection in children in Mexico City with no immune disorders and apparently adequate sanitary conditions at home and in the surrounding environment. The families of the children in this study had chlorinated water, adequate drainage around their homes, and practiced personal hygiene (e.g., took showers). The parents of these children washed their hands before preparing and eating meals, took showers daily, and were aware of the involvement of parasites in intestinal infections. In addition, all children studied had normal ranges of height and weight.
The detection of other intestinal parasites such as G. lamblia and E. histolytica infecting these children suggests exposure of the children to fecal contamination sources in the places where they live. Since G. lamblia is a common parasite in Mexico City among children less than five years old and has the same transmission mechanisms as Cryptosporidium, it is not surprising to find both parasites in our patients. Our finding of a higher susceptibility for giardiasis in girls and cryptosporidiosis in boys is consistent with previous observations in developing and developed regions of Mexico.42
Children with clinical gastrointestinal findings, but with no infections by intestinal protozoa, could be infected by other pathogens such as bacteria or viruses.43–45 However, examination of only one fecal sample, as in this study, does not eliminate infections by other parasites, which require examination of three consecutive samples for a more accurate diagnosis. Some years ago, amebiasis was among the main causes of diarrhea in children in Mexico City.46 However, the present results on E. histolytica morbidity suggests changes in the current epidemiologic patterns.
In conclusion, if one considers the increasing importance of Cryptosporidium infections in human and farm animal hosts, the development of a vaccine against this parasite would be of great benefit to both children in developing countries and neonatal ruminants.47
Signs and symptoms in 44 children with acute diarrhea infected by intestinal protozoa
Signs and symptoms | ||||||
---|---|---|---|---|---|---|
Protozoa No. (%) | Fever | Dehydration | Vomiting | Abdominal distension | Feed repulsion | Blood in feces |
Giardia lamblia 22 (50) | 14 | 9 | 6 | 22 | 2 | 0 |
Cryptosporidium 18 (41) | 18 | 0 | 0 | 18 | 0 | 0 |
Entamoeba histolytica 4 (9) | 4 | 0 | 0 | 4 | 0 | 4 |

Cryptosporidium spp. cysts in feces (Kinyoun acid-fast stained, magnification ×1,000).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 75, 6; 10.4269/ajtmh.2006.75.1095

Cryptosporidium spp. cysts in feces (Kinyoun acid-fast stained, magnification ×1,000).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 75, 6; 10.4269/ajtmh.2006.75.1095
Cryptosporidium spp. cysts in feces (Kinyoun acid-fast stained, magnification ×1,000).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 75, 6; 10.4269/ajtmh.2006.75.1095

Giardia lamblia cysts in feces (Kinyoun acid-fast stained, magnification ×400).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 75, 6; 10.4269/ajtmh.2006.75.1095

Giardia lamblia cysts in feces (Kinyoun acid-fast stained, magnification ×400).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 75, 6; 10.4269/ajtmh.2006.75.1095
Giardia lamblia cysts in feces (Kinyoun acid-fast stained, magnification ×400).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 75, 6; 10.4269/ajtmh.2006.75.1095

Entamoeba histolytica cyst in feces (Kinyoun acid-fast stained, magnification ×400).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 75, 6; 10.4269/ajtmh.2006.75.1095

Entamoeba histolytica cyst in feces (Kinyoun acid-fast stained, magnification ×400).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 75, 6; 10.4269/ajtmh.2006.75.1095
Entamoeba histolytica cyst in feces (Kinyoun acid-fast stained, magnification ×400).
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 75, 6; 10.4269/ajtmh.2006.75.1095
Address correspondence to José T. Sánchez-Vega, Laboratorio de Parasitologia, Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México y Unidad de Medicina Familiar Gabriel Mancera, Instituto Mexicano del Seguro Social, Cd. Universitaria, DF, 04510, Del. Coyoacán, Mexico City, DF, Mexico. E-mail: josetsanve@hotmail.com
Authors’ address: José T. Sánchez-Vega, Jorge Tay-Zavala, Artemisa Aguilar-Chiu, Dora Ruiz-Sánchez, Filiberto Malagón, José A. Rodríguez-Covarrubias, Javier Ordóñez-Martínez, and Leticia Calderón-Romero, Laboratorio de Parasitología, Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México y Unidad de Medicina Familiar Gabriel Mancera, Instituto Mexicano del Seguro Social, Cd. Universitaria, DF, 04510, Del. Coyoacán, Mexico City, DF, Mexico, Telephone: 52-5623-2380, Fax: 52-5623-2386, E-mails: josetsanve@hotmail.com and dorars@hotmail.com.
REFERENCES
- 1↑
Ditrich O, Palkovic L, Sterba J, Prokovic J, Loudova J, Giboda M, 1991. The first finding of Cryptosporidium baileyi in man. Parasitol Res 77 :44–47.
- 2
Xiao L, Bern C, Limor J, Sulaiman I, Roberts J, Checkley W, Cabrera L, Gilman R, Las A, 2001. Identification of 5 types of Cryptosporidium parasites in children in Lima, Peru. J Infect Dis 183 :492–497.
- 3
Tay J, Lara AR, Velasco CO, Gutiérrez QM, 2002. Parasitología Médica. Seventh edition. Mexico City: Méndez Publishing.
- 4↑
Sánchez-Vega JT, Tay J, 2003. Fundamentos de Microbiología y Parasitología Médicas. Mexico City: Méndez Publishing.
- 5↑
Vetterling JM, Jervis HR, Merrill TG, Sprinz H, 1971. Cryptosporidium wrairy from the guinea pig Cavia porcellus with an emendation of the genus. J Protozool 18 :243.
- 6↑
Nime FA, Burek JD, Page DL, Holscher MA, Yardley JH, 1976. Acute enterocolitis in a human being infected with the protozoan Cryptosporidium. Gastroenterology 70 :592–598.
- 7↑
Meisel JL, Perera DR, Meligro C, Rubin CE, 1976. Overwhelming watery diarrhea associated with Cryptosporidium in an immunosuppressed patient. Gastroenterology 70 :1156–1160.
- 8↑
Matukaitis JM, 1997. The emerging recognition of Cryptosporidium as a health hazard. J Community Health Nurs 14 :135–140.
- 9↑
Barriga-Angulo G, Cardeña-Capetillo J, Estrada-Parra S, Padierna-Olivos L, Cruz-Carranza E, Ruiz-Sánchez D, 1985. Cryptosporidiosis asociada a SIDA: informe de un caso. Infectología 2 :33–37.
- 10↑
Hunting P, Nichols G, 2002. Epidemiology and clinical features of Cryptosporidium infection in immunocompromised patients. Clin Microbiol Rev 15 :145–154.
- 11↑
Guarino A, Castaldo A, Russo S, Spagnuolo MI, Berni CR, Tavallo L, 1997. Enteric cryptosporidiosis in pediatric HIV infection. J Pediatr Gastroenterol Nutr 25 :182–187.
- 12↑
Chan AW, MacFarlane IA, Rhodes JM, 1989. Cryptosporidiosis as a cause of chronic diarrhoea in a patient with insulin-dependent diabetes mellitus. J Infect 19 :293.
- 13↑
Foot AB, Oakhill A, Mott MG, 1990. Cryptosporidiosis and acute leukaemia. Arch Dis Child 65 :236–237.
- 14↑
Gentile G, Vendetti M, Micozzi A, Caprioli A, Donelli G, Titindelli C, Meloni A, Arcrese W, Martino P, 1991. Cryptosporidiosis in patients with hematologic malignancies. Rev Infect Dis 13 :842–846.
- 15↑
Gómez-Morales MA, Ausiello CM, Guarino A, Vobani F, Spagnuolo MI, Pignata C, Pozio E, 1996. Severe protracted cryptosporidiosis associated with interferon gamma deficiency: pediatric case report. Clin Infect Dis 22 :848–850.
- 16↑
Gerber DA, Green M, Jaffe R, Greenberg D, Mazariegos G, Reyes J, 2000. Cryptosporidial infections after solid organ transplantation in children. Pediatr Transplant 4 :50–55.
- 17↑
Menon BS, Abdullah S, Mahamud F, Morgan UM, Malik AS, Choo KE, 2001. Low prevalence of Cryptopsoridium parvum in hospitalized children in Kota Bahru, Malasya. Southeast Asian J Trop Med Public Health 32 :319–322.
- 18↑
Kirkpatrick BD, Daniels MM, Jean SS, Pape JW, Karp C, Littenberg B, Fitzgerald DW, Lederman HM, Nataro JP, Sears CL, 2002. Cryptosporidiosis stimulates an inflammatory intestinal response in malnourished Haitian children. J Infect Dis 186 :94–101.
- 19
Genari-Cardoso ML, Costa-Cruz JM, de Castro E, Lima LM, Prudente DV, 1996. Cryptosporidium sp. in children suffering from acute diarrhea at Uberlandia City, State of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz 91 :551–554.
- 20
Rose JB, 1997. Environmental ecology of Cryptosporidium and public health implications. Annu Rev Public Health 18 :135–161.
- 22↑
Leach C, Koo F, Kuhls T, Hilsenbeck S, Jenson H, 2000. Prevalence of Cryptosporidium parvum infection in children among the Texas-Mexico border and associated to risk factors. Am J Trop Med Hyg 62 :656–661.
- 23
Khalakdina A, Vugia D, Nadle J, Rothrock GA, Colford JM Jr, 2003. Is drinking water a risk factor for endemic cryptosporidiosis? A case-control study in the immunocompetent general population of the San Francisco Bay area. BMC Public Health 3 :11–27.
- 24
Lima AA, Moore SR, Barboza MS Jr, Soares AM, Schleupner MA, Newman RD, Sears CL, Nataro JP, Fedorko DP, Nuhib T, Schorlling JB, Guerrant RL, 2000. Persistent diarrhea signals and critical period of increased diarrhea burdens and nutritional shortfalls: a prospective cohort study among children in northeastern Brazil. J Infect Dis 181 :1643–1651.
- 25↑
Moisier AD, Oberst RD, 2000. Cryptosporidiosis. A global challenge. Ann N Y Acad Sci 916 :102–111.
- 26↑
Chai JY, Kim NY, Guk SM, Park YK, Soo M, Han ET, 2001. High prevalence and seasonality of cryptosporidiosis in a small rural village occupied predominantly by aged people in the Republic of Korea. Am J Trop Med Hyg 65 :518–522.
- 27↑
Iqbal J, Hira PR, Al-Ali F, Philip R, 2001. Cryptosporidiosis in Kuwaiti children: seasonality and endemicity. Clin Microbiol Infect 7 :261–266.
- 28↑
Enriquez FJ, Avila CR, Santos JI, Tanaka-Kido J, Vallejo O, Sterling CR, 1997. Cryptosporidium infections in Mexican children: clinical, nutritional enteropathogenic and diagnostic evaluations. Am J Trop Med Hyg 56 :254–257.
- 29↑
Moles B, Torres L, Milagro A, Gorricho J, Seoane A, Navascues J, 1998. Incidencia de Cryptosporidium en Zaragoza: un estudio de 8 años (1989–1996). Enferm Infect Microbiol Clin 16 :356–358.
- 30↑
Centers for Disease Control and Prevention, 2000. Protracted outbreaks of cryptosporidiosis associated with swimming pool-use–Ohio and Nebraska. JAMA 23 :2967–2969.
- 31
McDonald AC, MacKenzie WR, Addiss DG, Gradus MS, Linke G, Zembrowski E, Hurd MR, Arrowood MJ, Lammie PJ, Priest JW, 2001. Cryptosporidium parvum-specific antibody responses among children residing in Milwaukee during the 1993 waterborne outbreak. J Infect Dis 183 :1373–1379.
- 32
Majowics SE, Michel P, Aramini JJ, Mc Ewen SA, Wilson JB, 2001. Descriptive analysis of endemic cryptosporidiosis cases reported in Ontario, 1996–1997. Can J Public Health 92 :62–66.
- 33
Qamruddin A, Keaney MG, McCann R, Chadwick PR, 2002. Increased stool sampling during a waterborne outbreak of cryptosporidiosis does not increase the detection of other faecal pathogens. J Clin Pathol 55 :271–274.
- 34↑
Lindo JF, Levy VA, Baum MK, Palmer CJ, 1998. Epidemiology of giardiasis and cryptosporidiosis in Jamaica. Am J Trop Med Hyg 59 :717–721.
- 35↑
Cegielski J, Ortega YR, McKee S, Madden JF, Gaido L, Schwartz D, 1999. Cryptosporidium, Enterocytozoon and Cyclospora infections in pediatric and adult patients with diarrhea in Tanzania. Clin Infect Dis 28 :314–321.
- 36
Naumova E, Chen J, Griffiths J, Matyas B, Estes-Smargiassi S, Morris R, 2000. Use of passive surveillance data to study temporal and spatial variation in the incidence of giardiasis and cryptosporidiosis. Public Health Rep 115 :436–447.
- 37
Bern C, Ortega Y, Checkley W, Roberts JM, Lescano AG, Cabrera L, 2002. Epidemiologic differences between cyclosporiasis and cryptosporidiosis in Peruvian children. Emerg Infect Dis 8 :581–585.
- 38↑
Redlinger T, Corella-Braud V, Graham J, Galindo A, Avitia R, Cardenas V, 2002. Hyperendemic Cryptosporidium and Giardia in households lacking municipal sewers and water on the United States-Mexico border. Am J Trop Med Hyg 66 :794–798.
- 39↑
Kinyoun JJ, 1915. A note on Uhlenhuth’s method for sputum examination for tubercle bacilli. Am J Public Health 5 :867–869.
- 40↑
Hunter PR, 2000. Modelling the impact of prior immunity, case misclassification and bias on case-control studies diarrhea in a Mexican rural population. Rev Invest Clin 52 :625–631.
- 41↑
Dietz V, Roberts J, 2000. National surveillance for infection with Cryptosporidium parvum, 1995–1998: What have we learned? Public Health Rep 115 :358–363.
- 42↑
Solorzano-Santos F, Penagos-Paniagua M, Meneses-Esquivel R, Miranda-Novales MG, Leanos-Miranda B, Angulo-González D, Fajardo-Gutiérrez A, 2000. Infección por Cryptosporidium parvum en niños desnutridos y no desnutridos sin diarrea en una población rural Mexicana. Rev Invest Clin 52 :625–631.
- 43↑
González C, Robledo E, Tay J, 1962. Utilidad del estudio de una muestra de materia fecal en el diagnóstico de diversas parasitosis intestinales. Bol Med Hosp Infect Mex 4 :455–458.
- 44
Amato-Neto V, Braz LM, Di Pietro AO, Modolo JR, 1966. Pesquisa de oocistos de Cryptosporidium sp em fezes: compaçao entre os metodos de Kinyoun modificado e de Heine. Rev Soc Bras Med Trop 29 :575–578.
- 45↑
Crook P, Mayon-White R, Reacher M, 2002. Enhancing surveillance of cryptosporidiosis: test all faecal specimens for children. Comm Dis Public Health 5 :112–113.
- 46↑
Tay J, Ruiz HA, Schenone H, Robert GL, Sánchez VJT, Uribarren BT, Becerril MA, Romero CR, 1994. Frecuencia de parasitosis intestinales en la República Mexicana. Bol Chil Parasitol 49 :9–15.
- 47↑
de Graaf DC, Spano F, Petra F, Sogodiva S, Bonnin A, 1999. Speculation of whether a vaccine against cryptosporidiosis is a reality or fantasy? Int J Parasitol 29 :1283–1306.