• View in gallery

    Graphic representation of the community studied within the Mexican Republic; locations of the 3 echinococcosis cases found in the community are shown with circles.

  • View in gallery

    US images of the 3 cases of cystic echinococcosis found in the study. A unilocular cyst with its germinal layer, seen as a white floating membrane inside the cyst fluid, was found in the index case (A); a unilocular anechoic lesion was detected in the second case (B); and a unilocular lesion was observed in the right hepatic lobule with two densities—one anechoic and the other with internal echoes—and having the appearance of a snowflake; an irregular wall was also found in the third case (C).

  • 1

    Thompson RCA, McManus DP, 2001. Aetiology: parasites and life cycles. Eckert J, Gammell F, Meslin X, and Pawlowski ZS, eds. WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. Geneva: World Health Organization, 1–19.

  • 2

    Flisser A, 2002. Larval tapeworm infections: cysticercosis, cystic echinococcosis, and alveolar echinococcosis. Richardson DJ and Krause PJ, eds. North American Parasitic Zoonoses. Norwell, MA: Kluwer Academic Publishers, 57–71.

  • 3

    Thompson RCA, McManus DP, 2002. Towards a taxonomic revision of the genus Echinococcus. Trends Parasitol 18 :452–457.

  • 4

    Teggi A, DiVico B, 2002. Craig P and Pawlowski Z (eds). Cestode Zoonoses: Echinococcosis And Cysticercosis. An Emergent and Global Problem. NATO Science Series, Vol 341. Amsterdam: IOS Press, 125–134.

  • 5

    Zhang W, Li J, McManus DP, 2003. Concepts in immunology and diagnosis of hydatid disease. Clin Microbiol Rev 16 :18–36.

  • 6

    Carmona CR, Perdomo A, Carbo C, Alvarez J, Monti R, Grauert D, Stern D, Perera G, Lloyd S, Bazini R, Gemmell MA, Yarzabal L, 1998. Risk factors associated with human cystic echinococcosis in Florida, Uruguay: results of a mass screening study using ultrasound and serology. Am J Trop Med Hyg 58 :599–605.

    • Search Google Scholar
    • Export Citation
  • 7

    MacPherson CNL, Roming T, Zeyhle E, Rees PH, Were JB, 1987. Portable ultrasound scanner versus serology in screening for hydatidid cysts in a nomadic population. Lancet 1 :259–261.

    • Search Google Scholar
    • Export Citation
  • 8

    Matsaniotis N, Karpathios TH, Koutoyzis J, Nicolaidou P, Fretzayas A, Papadellis F, Thomaidis TH, 1983. Hydatid disease in Greek children. Am J Trop Med Hyg 32 :1075–1078.

    • Search Google Scholar
    • Export Citation
  • 9

    Cohen H, Paolillo E, Bonifacino R, Botta B, Parada L, Cabrera P, Snowden K, Gasser R, Tessier R, Dibarboure L, Wen H, Allan JC, Soto de Alfaro H, Rogan MT, Craig P, 1998. Human cystic echinococcosis in a Uruguayan community: a sonographic, serologic and epidemiologic study. Am J Trop Med Hyg 59 :620–627.

    • Search Google Scholar
    • Export Citation
  • 10

    Pawlowski ZS, Eckert J, Vuitton DA, Ammann RW, Kern P, Craig PS, Dar KF, De Rosa F, Filice C, Gottstein B, Grimm F, MacPherson CNL, Stato N, Todorov T, Uchino J, von Sinner W, Wen H, 2001. Echinococcosis in humans: clinical aspects, diagnosis and treatment. Eckert J, Gammell F, Meslin X, and Pawlowski ZS, eds. WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. Geneva: World Health Organization, 20–71.

  • 11

    El-Thai MI, Omojola MF, Malatani T, Al-Saig AH, Ogunbiyi OA, 1992. Hydatid disease of the liver: evaluation of ultrasound and computed tomography. Br J Radiol 65 :390–392.

    • Search Google Scholar
    • Export Citation
  • 12

    Maddison SE, Slemenda SB, Schantz PM, Fried JA, Wilson M, Tsang VCW, 1989. A specific diagnostic antigen of Echinococcus granulosus with an apparent molecular weight of 8 kDa. Am J Trop Med Hyg 40 :377–383.

    • Search Google Scholar
    • Export Citation
  • 13

    Vargas-Rivera I, Martínez-Maya JJ, Jaramillo-Arango CJ, 1995. Caracterización de la hidatidosis porcina en el rastro frigorífico Los Reyes La Paz, Estado de México, México. Vet Mex 26 :365–368.

    • Search Google Scholar
    • Export Citation
  • 14

    Pérez Fernandez LF, Alaman P, Castañeda Herrera I, García Orendain DH, 1971. Hidatidosis Pulmonar Autóctona. Problemas del Tórax en la Práctica Diaria. Mexico City: Ediciones del Instituto Nacional de Neumología, 9–32.

  • 15

    Villarreal A, Padua G, Lezama C, Galindo MA, Argüero R, 1994. Quiste hidatídico pulmonar con ruptura mixta. Informe de un caso. Rev Med IMSS 33 :47.

    • Search Google Scholar
    • Export Citation
  • 16

    Suárez JP, Rivera E, Rico FG, Ramírez P, López de Lara A, 1995. Paquipleuritis granulomatosa de origen parasitario. Rev Inst Nal Enf Resp Méx 8 :54.

    • Search Google Scholar
    • Export Citation
  • 17

    Anuarios Estadísticos Secretaría de Salud, México. Egresos Hospitalarios por Grupos de Edad y Sexo, 1990–1999. Mexico, Secretaria de Salud, Mexico DF, 1991–2000.

  • 18

    Sánchez-González J, Rivera CA, Vázquez MA, Cruz Luna A, Farfán MR, Andrade QM, 1997. Anticuerpos anti-Echinococcus (hidatidosis) mediante hemaglutinación pasiva, en sujetos expuestos a riesgo. Rev Mex Patol Clin 44 :233–239.

    • Search Google Scholar
    • Export Citation
  • 19

    Palacios-Ruiz JA, Ramírez-Solís E, Moreno-Moller M, Cárdenas-Mejía A, Aguirre-Alcántara MT, Bonilla-Rodriguez C, Mata-Miranda P, Maravilla P, Flisser A, 2003. Identificación y manejo integral de un caso autóctono de hidatidosis en México. Rev Gastroenterol Mex 68 :42–45.

    • Search Google Scholar
    • Export Citation
  • 20

    Maravilla P, Thompson A, Palacios-Ruiz JA, Estcourt A, Ramírez-Solis E, Mondragón-de-la-Peña C, Moreno-Moller M, Cárdenas-Mejia A, Mata-Miranda P, Aguirre-Alcantera T, Bonilla-Rodriguez C, Flisser A, 2004. Echinococcus granulosus cattle strain identification in an autochthonous case of cystic echinococcosis in central Mexico. Acta Trop 92 :231–236.

    • Search Google Scholar
    • Export Citation
  • 21

    Selvin S, 1991. Poisson distribution: relative risk. Monographs in Epidemiology and Biostatistics, Vol 17: Statistical Analysis of Epidemiologic Data. New York: Oxford University Press, 75–77.

  • 22

    Moro PL, Garcia HH, Gonzalez AE, Bonilla JJ, Verastegui M, Gilman RH, 2005. Screening for cystic echinococcosis in an endemic region of Peru using portable ultrasonography and the enzyme-linked immunoelectrotransfer blot (EITB) assay. Parasitol Res 96 :242–246.

    • Search Google Scholar
    • Export Citation
  • 23

    Valadéz AR, 1995. El Perro Mexicano. Ciudad Universitaria, México: Instituto de Investigaciones Antropológicas, Universidad Nacional Autónoma de México, 45 pp.

 

 

 

 

 

Epidemiologic and Ultrasonographic Study of Echinococcosis in a Community in the State of México

View More View Less
  • 1 Dirección de Investigación. Hospital General “Dr. Manuel Gea Gonzalez”, México DF 14000, México; División de Radiología, Hospital General “Dr. Manuel Gea Gonzalez”, México DF 14000, México; Diplomado en Ultrasonido, Facultad de Medicina, Universidad Nacional Autónoma de México, México DF 04510, México; Programa de Residencia en Epidemiología Aplicada. Dirección General de Epidemiología, México DF 01480, México; Departamento de Medicina Preventiva y Salud Pública, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, México DF 04510, México; Departamento de Salud Pública, Facultad de Medicina, Universidad Nacional Autónoma de México, México DF 04510, México; Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, México DF 04510, México

No epidemiologic study for cystic echinococcosis in México has yet been described. The objective of this work was to determine the prevalence and distribution of human echinococcosis in a community of the state of México and its probable risk factors. A cross-sectional study was performed; household census was used to randomly select houses. The larval stage of Echinococcus was searched by ultrasound in liver, spleen, and kidney. A questionnaire was used for the investigation of risk factors. The study was performed with 401 persons, 64% were female. The prevalence of echinococcosis was 0.75%. Cases were distributed in the same sector of the community. The close distribution of cases suggests the same exposure source. There were 426 dogs in the community; feces were collected from 414 of these in search of cestode eggs. After treatment, 3 dogs had Taenia pisiformis but none had Echinococcus. This paper pioneers the search of human echinococcosis in México because it provides evidence of the presence of this tissue parasite at the community level.

INTRODUCTION

Echinococcosis is a cosmopolitan zoonotic disease affecting mainly populations with extensive livestock (cattle, ovine, porcine, equine).1 This parasitic disease is acquired orally from dog feces contaminated with Echinococcus eggs. Echinococcus granulosus is the species most frequently found.13 Natural history of echinococcosis in humans is poorly known because the disease is usually asymptomatic for several years, and when signs and symptoms appear, they are not pathognomonic because the parasites cause mechanical compressive phenomena or an intense inflammatory reaction due to rupture of the cyst and release of antigens.4,5

The frequency of echinococcosis reported from endemic regions is between 1.6% and 30%, depending on the diagnostic method used.49 Ultrasound (US) is the method of choice because of its high sensitivity and specificity; images have been classified in 5 stages.511 Immunodiagnosis is performed using ELISA and western blot, the latter allowing identification of a specific 8-kDa band.2,12 The domestic cycle of the parasite is facilitated when pastoral dogs are allowed to eat viscera of the slaughtered livestock and people have incorrect habits toward dogs.1,2 The frequency of the disease is not known in México, as only scarce data are available: 0.3% of 40,073 pigs in slaughterhouses in central México were positive by meat inspection of infected viscera13; six cases in hospitals for tuberculosis have been reported in Mexican patients1416 and some nonspecified hospital discharges17 as well as the presence of antibodies in 15% of an suburban population living close to a slaughterhouse that detected pigs with echinococcosis.18 An autochthonous case was identified and treated a few years ago in the Hospital General “Dr. Manuel Gea Gonzalez”. The patient lives in a rural area in the state of México, the house has cement floors but no sewage system, therefore latrines are used. The family has a small farm where there are 4 dogs, 4 sheep, 3 cows, 2 horses, and 1 pig. Feces collected from the dogs were all negative for taeniid eggs.19,20 The epidemiologic survey performed in the patient’s house identified risk conditions that motivated an in-depth study, which is the purpose of the present paper.

MATERIALS AND METHODS

The community studied is located in the State of México at 19°42′50″ northern latitude, 99°13′24″ west from the Greenwich meridian, at 2,300 meters above sea level; it has temperate climate, and is surrounded by four mountain chains: Sierra Madre Occidental, Neovolcanic axis, Sierra Madre Oriental and Sierra Madre del Sur. Government and health authorities of the municipality and the community were asked to authorize our study. The protocol was approved by the Ethics and Research Commissions of the General Hospital “Dr. Manuel Gea Gonzalez.” Between September and November 2002, a transversal study was performed. An initial census regarding demographic data, housing characteristics, ownership of animals, and possible risk factors6 of the population identified 1911 persons in 394 inhabited houses. Each house was considered as a sampling unit, and a 20% rate of nonparticipation was calculated. Houses were numbered and randomly selected. Inhabitants were invited to participate by telephone calls or personally at their homes, explaining the importance of performing an US that could identify cystic echinococcosis and other diseases. Interested persons received a comprehensive explanation, and those who agreed to participate signed a letter of informed consent. Questionnaires were applied to everyone 6 years and older on physical contact with dogs and to people 18 and older regarding knowledge of echinococcosis. US studies were performed with portable equipment (Echo Camera Mode SSD-500, 3.5 MHz; Aloka, Tokyo, Japan) in the health center. Cysts were searched in liver, spleen, and kidneys, those identified were classified according to criteria provided by WHO.10 Case operational definition was: patient with a unilocular cystic lesion detected by US, which had a uniform anechoic contents, not delimitated with an hyperechoic ring, normally round or oval and of variable size, according to grades 1 to 5.10 People with images suggestive of cystic echinococcosis were asked for a blood simple, sera were sent to CDC (Atlanta, GA) for western blot analysis. Statistical analysis was performed with SPSS 10.0 software (SPSS Inc., Chicago, IL). Most dogs present in the community were sampled once for feces using a rectal spoon; ≈1 g was introduced in small plastic flasks, kept at 4°C, and taken to the central laboratory. Coproparasitoscopic analyses were performed by the Faust technique, and eggs were viewed under an optical microscope (Nikon, Tokyo, Japan). Animals positive for cestode eggs were isolated in cages with fecal collection facilities, which were maintained in the backyards of their homes, and were treated orally with praziquantel at 30 mg/kg and 90 min later with arecoline hydrobromide at 6 mg/kg. Dogs were kept in the cage between 30 min and 4 hours until they expelled the tapeworms. After collection of feces, the dogs were released.

RESULTS

The community has electricity, chlorinated drinking water, and telephone services; 98% of the streets are paved; it is mainly agricultural but people also work in factories and other suburban employment; only 53 sheep, 27 cows, 9 horses, 6 pigs, and 4 goats were counted. Frequencies of known risk conditions for echinococcosis were as follows: 64% kept water in buckets or vats, 23% fed dogs with uncooked livestock viscera, and 22% grew vegetables in the backyard. It is important to note that 86% of the livestock residues were obtained from the butcher shop and only 14% from livestock slaughtered at home.

A sample of 401 inhabitants from 94 households, integrated by 64% female and 36% male with an average of 28 years of age (± 20) was studied; this sample had similar characteristics to the overall population. For the questionnaire about dogs, 167 dogs were counted in the sample, of which 62 were guardians, and the rest were pets, but in general, the significance of the dog in the household varied with age and with type of relationship (Table 1). Around 89% of the dogs stay outside the home, 6% live inside, and 5% of owners do not know exactly where the dogs stay. About 68% of the owners indicated that they like dogs; 3% said that their dogs had access to viscera of sheep, pigs, and cows, and 97% said that their dogs had access to chicken remains. Furthermore, 30% of interviewed people said that contact with dogs was by the hands, 25% only talk to them, 9% had no manifestation of affection to dogs, 9% hug or kiss dogs, and the remaining people did not answer this question. Nine percent of adults (people over 18 years) answered that they had heard of hydatid cysts or “sandy cysts,” and 16% answered that they had seen cysts with “sand” in the viscera of livestock. Dog owners allowed sampling 414 from the 426 dogs present in the community, and feces were collected in search of cestode eggs; 4 dogs were positive. These animals were treated: Taenia pisiformis adult parasites were recovered from 3 dogs, none had Echinococcus, and one dog did not release any tapeworm.

The case detected at General Hospital “Dr. Manuel Gea Gonzalez”19,20 was included in this study; two other people presented cysts under US. Figure 1 shows the map of the community with regard to the Mexican Republic and the locations of the 3 cases; interestingly, they were distributed in the same sector of the community. The index case, a 38-year-old female, had a solitary hydatid cyst in the liver, 60 mm in diameter, with undulating hyperechoic membranes floating inside the cyst fluid and a hyperechoic ring (Figure 2A). The second case, a 46-year-old female, had a unilocular anechoic lesion in the left hepatic lobule, with the wall mildly delimitated by a round hyperechoic ring, measuring 55 × 48 mm (Figure 2B). The third case, an 89-year-old male, had a unilocular lesion in the right hepatic lobule with two densities: one anechoic and another one with internal echoes, having the image of a snowflake, and an irregular wall, measuring 76 × 72 mm (Figure 2C). Only the index case had symptoms and specific antibodies; the other two cases were asymptomatic and did not show the specific band in western blot. Therefore, the prevalence was 0.75% (3/401). No statistical analysis provided significant differences between cases and controls, including odds ratios and Poisson regression analyses for rare events.21

DISCUSSION

This is the first community-based study performed in Mexico in search of autochthonous echinococcosis. Only 75% of the population participated in the study in spite of the fact that the US examination was free of charge and that people were told it would identify some visceral diseases; 3 people who had lived all their lives in the community were identified to have liver hydatid cysts. Therefore, US made it possible for us to detect a prevalence of 0.75% in a country where echinococcosis is considered practically absent. It is known that the disease is frequently asymptomatic,2,10 and in these types of cases, no humoral immune response is usually detected.9,10 Recently, in a community-based study performed using US and western blot in Peru, 4.9% of healthy people were positive by US and only 2.6% were positive by western blot.22 Known risk factors,6 such as feeding dogs with uncooked livestock viscera, keeping water in buckets or vats, and growing vegetables in gardens that are not necessarily sheltered from dogs and their feces and thus become a source of ingesting Echinococcus eggs, added to the clustered distribution of the 3 cases in the community give reliability to the results obtained in the study. In addition, an anthropological study performed in Mexico showed that dogs are considered mainly as partners, pets, and guardians,23 and that study also resembles the present data. Although dogs were not practically considered as shepherds, and the questionnaire about dogs showed that only 3% of owners feed them with livestock viscera, the community census indicated that 23% of owners did permit their dogs to eat uncooked livestock viscera.

The 3 cases had hepatic cysts, which is the most common location of cysts worldwide,2,10 in contrast with the 6 hospitalized cases reported previously in Mexico that were pulmonary in nature.1416 The size of the Echinococcus cysts diagnosed was very similar (5–7 cm), suggesting exposure at similar times and a long-lasting evolution, because cyst growth is very slow.10 This information validates the absence of Echinococcus in dogs during the present study.

The prevalence of echinococcosis was 0.75%, confirming clinical data indicating this disease is not common in Mexico1417,19; therefore, no clear association with risk factors was found. In livestock, echinococcosis has only been reported in Mexico in low frequency in pigs,13 and the index case had the bovine strain.20 All of these data suggest that other factors should be considered to explain the low frequency, such as genetic resistance of humans, livestock, and especially dogs to E. granulosus. Interestingly, the cases (living all their lives in the same house) were distributed in the same sector of the community, suggesting the same exposure source. This paper is pioneering in the search of human echinococcosis in Mexico because it provides evidence of the presence of this tissue parasite at the community level.

Table 1

Perceived role of the domestic dog according to age of owners

Owner age, grouped by years
Role6–1213–2021–3031–4041–50> 51
Guardian8 (11%)11 (20%)19 (29%)33 (56%)26 (56%)26 (50%)
Friend34 (46%)12 (22%)8 (12%)9 (15%)1 (2%)5 (10%)
Pet15 (20%)11 (20%)14 (22%)6 (10%)7 (15%)5 (10%)
Partner1 (2%)12 (22%)14 (22%)2 (4%)3 (7%)7 (14%)
Illness vector3 (4%)3 (5%)5 (8%)6 (12%)6 (12%)6 (12%)
Toy11 (15%)3 (5%)1 (2%)1 (2%)0 (0%)0 (0%)
Responsibility1 (2%)4 (7%)3 (4%)1 (2%)3 (7%)1 (2%)
Shepherd0 (0%)0 (0%)0 (0%)0 (0%)0 (0%)1 (2%)
Total735465594652
Figure 1.
Figure 1.

Graphic representation of the community studied within the Mexican Republic; locations of the 3 echinococcosis cases found in the community are shown with circles.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 77, 3; 10.4269/ajtmh.2007.77.500

Figure 2.
Figure 2.

US images of the 3 cases of cystic echinococcosis found in the study. A unilocular cyst with its germinal layer, seen as a white floating membrane inside the cyst fluid, was found in the index case (A); a unilocular anechoic lesion was detected in the second case (B); and a unilocular lesion was observed in the right hepatic lobule with two densities—one anechoic and the other with internal echoes—and having the appearance of a snowflake; an irregular wall was also found in the third case (C).

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 77, 3; 10.4269/ajtmh.2007.77.500

*

Address correspondence to Ana Flisser, Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Ciudad Universitaria, Av. Universidad 3000, Coyoacán, 04510 México DF, Mexico. E-mail: flisser@servidor.unam.mx

Authors’ addresses: Pilar Mata-Miranda, Ulises Rodríguez-Prado, América Gutiérrez-Marín, and Pablo Maravilla, Dirección de Investigación. Hospital General “Dr. Manuel Gea Gonzalez”, México DF 14000, Mexico. Israel Osnaya-Palma and Luis Villalvaso, División de Radiología, Hospital General “Dr. Manuel Gea Gonzalez”, México DF 14000, Mexico. Marcos Tawil and Sandy Hernández-González, Diplomado en Ultrasonido, Facultad de Medicina, Universidad Nacional Autónoma de México, México DF 04510, Mexico. Miguel Solano-Ceh, Programa de Residencia en Epidemiología Aplicada, Dirección General de Epidemiología, México DF 01480, Mexico. José Juan Martínez-Maya, Departamento de Medicina Preventiva y Salud Pública, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, México DF 04510, Mexico. Guadalupe García-de-la-Torre, Departamento de Salud Pública, Facultad de Medicina, Universidad Nacional Autónoma de México, México DF 04510, Mexico. Ana Flisser, Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México, México DF 04510, Mexico.

Acknowledgments: We thank Dr. Christine Budke (Texas A&M University) for critical review of the manuscript. We also thank QBP Fernando Gonzalez (Hospital General “Dr. Manuel Gea Gonzalez”) for assistance with Figure 1. PAPIIT/UNAM (grant IN218503) supported fieldwork for dog fecal analysis; CONACYT (grant SNI/2543) supported A.G.M.

REFERENCES

  • 1

    Thompson RCA, McManus DP, 2001. Aetiology: parasites and life cycles. Eckert J, Gammell F, Meslin X, and Pawlowski ZS, eds. WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. Geneva: World Health Organization, 1–19.

  • 2

    Flisser A, 2002. Larval tapeworm infections: cysticercosis, cystic echinococcosis, and alveolar echinococcosis. Richardson DJ and Krause PJ, eds. North American Parasitic Zoonoses. Norwell, MA: Kluwer Academic Publishers, 57–71.

  • 3

    Thompson RCA, McManus DP, 2002. Towards a taxonomic revision of the genus Echinococcus. Trends Parasitol 18 :452–457.

  • 4

    Teggi A, DiVico B, 2002. Craig P and Pawlowski Z (eds). Cestode Zoonoses: Echinococcosis And Cysticercosis. An Emergent and Global Problem. NATO Science Series, Vol 341. Amsterdam: IOS Press, 125–134.

  • 5

    Zhang W, Li J, McManus DP, 2003. Concepts in immunology and diagnosis of hydatid disease. Clin Microbiol Rev 16 :18–36.

  • 6

    Carmona CR, Perdomo A, Carbo C, Alvarez J, Monti R, Grauert D, Stern D, Perera G, Lloyd S, Bazini R, Gemmell MA, Yarzabal L, 1998. Risk factors associated with human cystic echinococcosis in Florida, Uruguay: results of a mass screening study using ultrasound and serology. Am J Trop Med Hyg 58 :599–605.

    • Search Google Scholar
    • Export Citation
  • 7

    MacPherson CNL, Roming T, Zeyhle E, Rees PH, Were JB, 1987. Portable ultrasound scanner versus serology in screening for hydatidid cysts in a nomadic population. Lancet 1 :259–261.

    • Search Google Scholar
    • Export Citation
  • 8

    Matsaniotis N, Karpathios TH, Koutoyzis J, Nicolaidou P, Fretzayas A, Papadellis F, Thomaidis TH, 1983. Hydatid disease in Greek children. Am J Trop Med Hyg 32 :1075–1078.

    • Search Google Scholar
    • Export Citation
  • 9

    Cohen H, Paolillo E, Bonifacino R, Botta B, Parada L, Cabrera P, Snowden K, Gasser R, Tessier R, Dibarboure L, Wen H, Allan JC, Soto de Alfaro H, Rogan MT, Craig P, 1998. Human cystic echinococcosis in a Uruguayan community: a sonographic, serologic and epidemiologic study. Am J Trop Med Hyg 59 :620–627.

    • Search Google Scholar
    • Export Citation
  • 10

    Pawlowski ZS, Eckert J, Vuitton DA, Ammann RW, Kern P, Craig PS, Dar KF, De Rosa F, Filice C, Gottstein B, Grimm F, MacPherson CNL, Stato N, Todorov T, Uchino J, von Sinner W, Wen H, 2001. Echinococcosis in humans: clinical aspects, diagnosis and treatment. Eckert J, Gammell F, Meslin X, and Pawlowski ZS, eds. WHO/OIE Manual on Echinococcosis in Humans and Animals: A Public Health Problem of Global Concern. Geneva: World Health Organization, 20–71.

  • 11

    El-Thai MI, Omojola MF, Malatani T, Al-Saig AH, Ogunbiyi OA, 1992. Hydatid disease of the liver: evaluation of ultrasound and computed tomography. Br J Radiol 65 :390–392.

    • Search Google Scholar
    • Export Citation
  • 12

    Maddison SE, Slemenda SB, Schantz PM, Fried JA, Wilson M, Tsang VCW, 1989. A specific diagnostic antigen of Echinococcus granulosus with an apparent molecular weight of 8 kDa. Am J Trop Med Hyg 40 :377–383.

    • Search Google Scholar
    • Export Citation
  • 13

    Vargas-Rivera I, Martínez-Maya JJ, Jaramillo-Arango CJ, 1995. Caracterización de la hidatidosis porcina en el rastro frigorífico Los Reyes La Paz, Estado de México, México. Vet Mex 26 :365–368.

    • Search Google Scholar
    • Export Citation
  • 14

    Pérez Fernandez LF, Alaman P, Castañeda Herrera I, García Orendain DH, 1971. Hidatidosis Pulmonar Autóctona. Problemas del Tórax en la Práctica Diaria. Mexico City: Ediciones del Instituto Nacional de Neumología, 9–32.

  • 15

    Villarreal A, Padua G, Lezama C, Galindo MA, Argüero R, 1994. Quiste hidatídico pulmonar con ruptura mixta. Informe de un caso. Rev Med IMSS 33 :47.

    • Search Google Scholar
    • Export Citation
  • 16

    Suárez JP, Rivera E, Rico FG, Ramírez P, López de Lara A, 1995. Paquipleuritis granulomatosa de origen parasitario. Rev Inst Nal Enf Resp Méx 8 :54.

    • Search Google Scholar
    • Export Citation
  • 17

    Anuarios Estadísticos Secretaría de Salud, México. Egresos Hospitalarios por Grupos de Edad y Sexo, 1990–1999. Mexico, Secretaria de Salud, Mexico DF, 1991–2000.

  • 18

    Sánchez-González J, Rivera CA, Vázquez MA, Cruz Luna A, Farfán MR, Andrade QM, 1997. Anticuerpos anti-Echinococcus (hidatidosis) mediante hemaglutinación pasiva, en sujetos expuestos a riesgo. Rev Mex Patol Clin 44 :233–239.

    • Search Google Scholar
    • Export Citation
  • 19

    Palacios-Ruiz JA, Ramírez-Solís E, Moreno-Moller M, Cárdenas-Mejía A, Aguirre-Alcántara MT, Bonilla-Rodriguez C, Mata-Miranda P, Maravilla P, Flisser A, 2003. Identificación y manejo integral de un caso autóctono de hidatidosis en México. Rev Gastroenterol Mex 68 :42–45.

    • Search Google Scholar
    • Export Citation
  • 20

    Maravilla P, Thompson A, Palacios-Ruiz JA, Estcourt A, Ramírez-Solis E, Mondragón-de-la-Peña C, Moreno-Moller M, Cárdenas-Mejia A, Mata-Miranda P, Aguirre-Alcantera T, Bonilla-Rodriguez C, Flisser A, 2004. Echinococcus granulosus cattle strain identification in an autochthonous case of cystic echinococcosis in central Mexico. Acta Trop 92 :231–236.

    • Search Google Scholar
    • Export Citation
  • 21

    Selvin S, 1991. Poisson distribution: relative risk. Monographs in Epidemiology and Biostatistics, Vol 17: Statistical Analysis of Epidemiologic Data. New York: Oxford University Press, 75–77.

  • 22

    Moro PL, Garcia HH, Gonzalez AE, Bonilla JJ, Verastegui M, Gilman RH, 2005. Screening for cystic echinococcosis in an endemic region of Peru using portable ultrasonography and the enzyme-linked immunoelectrotransfer blot (EITB) assay. Parasitol Res 96 :242–246.

    • Search Google Scholar
    • Export Citation
  • 23

    Valadéz AR, 1995. El Perro Mexicano. Ciudad Universitaria, México: Instituto de Investigaciones Antropológicas, Universidad Nacional Autónoma de México, 45 pp.

Author Notes

Reprint requests: Ana Flisser, Departamento de Microbiología y Parasitología, Facultad de Medicina, Universidad Nacional Autónoma de México (UNAM), Ciudad Universitaria, Av. Universidad 3000, Coyoacán, 04510 México DF, Mexico. E-mail: flisser@servidor.unam.mx.
Save