Predominio del subconjunto AII de Giardia duodenalis en niños pequeños de Salvador, Bahía, Brasil

Flávia Thamiris Figueiredo Pacheco , Renata Kelly Novaes Rodrigues Silva , Silvia Souza de Carvalho , Felipe Carvalho Rocha , Gisele Maria Trindade das Chagas , Daisy Chagas Gomes , Hugo da Costa-Ribeiro Junior , Tereza Cristina Medrado Ribeiro, Ângela Peixoto de Mattos , Luciano Kalabric Silva , Neci Matos Soares , Márcia Cristina Aquino Teixeira, .

Palabras clave: giardiasis/epidemiología, niño, guarderías, Brasil

Resumen

Introducción. Giardia duodenalis es un protozoo intestinal de gran prevalencia en los niños de los países en desarrollo. En estudios moleculares se ha evidenciado la gran diversidad genética de G. duodenalis y se han identificado los conjuntos A y B, principalmente en humanos. A pesar de su importancia, el conocimiento de la epidemiología molecular de la giardiasis humana aún es limitado en Brasil.
Objetivo. Caracterizar los aislamientos moleculares de G. duodenalis de muestras tomadas a niños de Salvador, Bahía, Brasil.
Materiales y métodos. Las muestras fecales positivas para G. duodenalis se obtuvieron de 71 niños de dos guarderías y de 39 usuarios de un laboratorio de análisis clínicos. Las muestras se analizaron mediante PCR-RFLP de los genes gdh y beta-giardin, y secuenciación de beta-giardin.
Resultados. De las 110 muestras de G. duodenalis, en 80 (72,7 %) se amplificaron uno o ambos genes. De estos, 62 (77,5 %) se identificaron como pertenecientes al conjunto A y 18 (22,5 %) al B. El subconjunto AII se identificó en el 58,8 % (n=47) de los aislamientos, seguido del AI en el 18,8% (n=15), el BIV en el 11,2% (n=9) y el BIII en el 5,0% (n=4).
El subconjunto AII fue el más frecuente en los niños de ambas guarderías, en tanto que el AI solo se encontró en el grupo atendido en el laboratorio clínico. El subconjunto AII predominó en los niños menores de dos años.
Conclusiones. La mayor frecuencia del subconjunto AII sugiere que la transmisión antroponótica es más común en Salvador, pero también existen vías de transmisión zoonóticas, y que pueden ocurrir cambios en la sensibilidad frente a diferentes patrones moleculares de Giardia durante el crecimiento infantil.

Descargas

La descarga de datos todavía no está disponible.

Referencias bibliográficas

Nesti MM, Goldbaum M. Infectious diseases and daycare and preschool education. J Pediatr (Rio J). 2007;83:299-312. https://doi.org/10.4269/ajtmh.199 0.42.206

Papier K, Williams GM, Luceres-Catubig R, Ahmed F, Olveda RM, McManus DP, et al. Childhood malnutrition and parasitic helminth interactions. Clin Infec Dis. 2014;59:234-43. https://doi.org/10.1093/cid/ciu211

Yones DA, Galal LA, Abdallah AM, Zaghlol KS. Effect of enteric parasitic infection on serum trace elements and nutritional status in upper Egyptian children. Trop Parasitol. 2015;5:29-35. https://doi.org/10.4103/2229-5070.145581

Thompson RCA. The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Vet Parasitol. 2004;126:15-35. https://doi.org/10.1016/j.vetpar.2004.09.008

Ryan U, Hijjawi N, Feng Y, Xiao L. Giardia: An under-reported foodborne parasite. Int J Parasitol. 2019;49:1-11. https://doi.org/10.1016/j.ijpara.2018.07.003

Thompson RCA. Giardiasis as a re-emerging infectious disease and its zoonotic potential. Int J Parasitol. 2000;30:1259-67. https://doi.org/10.1016/S0020-7519(00)00127-2

Cacciò SM, De Giacomo M, Pozio E. Sequence analysis of the beta-giardin gene and development of a polymerase chain reaction-restriction fragment length polymorphism assay to genotype Giardia duodenalis cysts from human faecal samples. Int J Parasitol. 2002;32:1023-30. https://doi.org/10.1016/S0020-7519(02)00068-1

Feng Y, Xiao L. Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin Microbiol Rev. 2011;24:110-40. https://doi.org/10.1128/CMR.00033-10

Plutzer J, Ongerth J, Karanis P. Giardia taxonomy, phylogeny and epidemiology: Facts and open questions. Int J Hyg Environ Health. 2010;213:321-33. https://doi.org/10.1016/j.ijheh.2010.06.005

Thompson RCA, Ash A. Molecular epidemiology of Giardia and Cryptosporidium infections. Infect Genet Evol. 2016;40:315-23. https://doi.org/10.1016/j.meegid.2015.09.028

Monis PT, Andrews RH, Mayrhofer G, Ey PL. Genetic diversity within the morphological species Giardia intestinalis and its relationship to host origin. Infect Genet Evol. 2003;3:29-38. https://doi.org/10.1016/S1567-1348(02)00149-1

Ballweber LR, Xiao L, Bowman DD, Kahn G, Cama VA. Giardiasis in dogs and cats: Update on epidemiology and public health significance. Trends Parasitol. 2010;26:180-9. https://doi.org/10.1016/j.pt.2010.02.005

Sprong H, Cacciò SM, van der Giessen JWB, ZOOPNET network and partners. Identification of zoonotic genotypes of Giardia duodenalis. PLoS Negl Trop Dis. 2009;3:e558. https://doi.org/10.1371/journal.pntd.0000558

Haque R, Roy S, Kabir M, Stroup SE, Mondal D, Houpt ER. Giardia assemblage A infection and diarrhea in Bangladesh. J Infect Dis. 2005;192:2171-3. https://doi.org/10.1086/498169

Sousa MC, Morais JB, Machado JE , Poiares-da-Silva J. Genotyping of Giardia lamblia human isolates from Portugal by PCR-RFLP and sequencing. J Eukaryot Microbiol. 2006;53:174-6. https://doi.org/10.1111/j.1550-7408.2006.00221.x

Karanis P, Ey PL. Characterization of axenic isolates of Giardia intestinalis established from humans and animals in Germany. Parasitol Res. 1998;84:442-9. https://doi.org/10.1007/s004360050427

Johnston AR, Gillespie TR, Rwego IB, McLachlan TLT, Kent AD, Goldberg TL. Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda. PLoS Negl Trop Dis. 2010;4:e683. https://doi.org/10.1371/journal.pntd.0000683

Skhal D, Aboualchamat G, Al Mariri A, Al Nahhas S. Prevalence of Giardia duodenalis assemblages and sub-assemblages in symptomatic patients from Damascus city and its suburbs. Infect Genet Evol. 2017;47:155-60. https://doi.org/10.1016/j.meegid.2016.11.030

Lee MF, Auer H, Lindo JF, Walochnik J. Multilocus sequence analysis of Giardia spp. isolated from patients with diarrhea in Austria. Parasitol Res. 2017;116:477-81. https://doi.org/10.1007/s00436-016-5306-9

Mbae C, Mulinge E, Guleid F, Wainaina J, Waruru A, Njiru ZK, et al. Molecular characterization of Giardia duodenalis in children in Kenya. BMC Infect Dis. 2016;16:135. https://doi.org/10.1186/s12879-016-1436-z

Osman M, El Safadi D, Cian A, Benamrouz S, Nourrisson C, Poirier P, et al. Prevalence and risk factors for intestinal protozoan infections with Cryptosporidium, Giardia, Blastocystis and Dientamoeba among schoolchildren in Tripoli, Lebanon. PLoS Negl Trop Dis. 2016;10:e0004496. https://doi.org/10.1371/journal.pntd.0004496

Iqbal A, Goldfarb DM, Slinger R, Dixon BR. Prevalence and molecular characterization of Cryptosporidium spp. and Giardia duodenalis in diarrhoeic patients in the Qikiqtani Region, Nunavut, Canada. Int J Circumpolar Health. 2015;74:27713. https://doi.org/10.3402/ijch.v74.27713

Fahmy HM, El-Serougi AO, El Deeb HK, Hussein HM, Abou-Seri HM, Klotz C, et al. Giardia duodenalis assemblages in Egyptian children with diarrhea. Eur J Clin Microbiol Infect Dis. 2015;34:1573-81. https://doi.org/10.1007/s10096-015-2389-7

Minvielle MC, Molina NB, Polverino D, Basualdo JA. First genotyping of Giardia lamblia from human and animal feces in Argentina, South America. Mem Inst Oswaldo Cruz. 2008;103:98-103. https://doi.org/10.1590/s0074-02762008000100015

Volotão AC, Costa-Macedo LM, Haddad FSM, Brandão A, Peralta JM, Fernandes O. Genotyping of Giardia duodenalis from human and animal samples from Brazil using betagiardin gene: A phylogenetic analysis. Acta Trop. 2007;102:10-9. https://doi.org/10.1016/j.actatropica.2007.02.010

Coradi ST, David EB, Oliveira-Sequeira TC, Ribolla PE, Carvalho TB, Guimarães S. Genotyping of Brazilian Giardia duodenalis human axenic isolates. J Venom Anim Toxins Incl Trop Dis. 2011;17:353-7. https://doi.org/10.1590/S1678-91992011000300016

Oliveira-Arbex AP, David EB, Oliveira-Sequeira TCG, Bittencourt GN, Guimarães S. Genotyping of Giardia duodenalis isolates in asymptomatic children attending daycare centre: Evidence of high risk for anthroponotic transmission. Epidemiol Infect. 2016;144:1418-28. https://doi.org/10.1017/S0950268815002514

Kohli A, Bushen OY, Pinkerton RC, Houpt E, Newman RD, Sears CL, et al. Giardia duodenalis assemblage, clinical presentation and markers of intestinal inflammation in Brazilian children. Trans R Soc Trop Med Hyg. 2008;102:718-25. https://doi.org/10.1016/j.trstmh.2008.03.002

Santos CK, Grama DF, Limongi JE, Costa FC, Couto TR, Soares RM, et al. Epidemiological, parasitological and molecular aspects of Giardia duodenalis infection in children attending public daycare centers in southeastern Brazil. Trans R Soc Trop Med Hyg. 2012;106:473-9. https://doi.org/10.1016/j.trstmh.2012.05.011

Faria CP, Zanini GM, Dias GS, da Silva S, Sousa MC. Molecular characterization of Giardia lamblia: First report of Assemblage B in human isolates from Rio de Janeiro (Brazil). PLOS ONE. 2016;11:e0160762. https://doi.org/10.1371/journal.pone.0160762

Pacheco FT, Silva RK, Martins AS, Oliveira RR, Alcântara-Neves NM, Silva MP, et al. Differences in the detection of Cryptosporidium and Isospora (Cystoisospora) oocysts according to the fecal concentration or staining method used in a clinical laboratory. J Parasitol. 2013;99:1002-8. https://doi.org/10.1645/12-33.1

Faust EC, Sawitz W, Tobie J, Odom V, Peres C, Lincicome DR. Comparative efficiency of various technics for the diagnosis of protozoa and helminths in feces. J Parasitol. 1938;25:241-62. https://doi.org/10.2307/3272508

Lalle M, Pozio E, Capelli G, Bruschi F, Crotti D, Cacciò SM. Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. Int J Parasitol. 2005;35:207-13. https://doi.org/10.1016/j.ijpara.2004.10.022

Read CM, Monis PT, Thompson RC. Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infect Genet Evol. 2004;4:125-30. https://doi.org/10.1016/j.meegid.2004.02.001

Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30:2725-9. https://doi.org/10.1093/molbev/mst197

Ryan U, Cacciò SM. Zoonotic potential of Giardia. Int J Parasitol. 2013;43:943-56. https://doi.org/10.1016/j.ijpara.2013.06.001

Wang H, Zhao G, Chen G, Jian F, Zhang S, Feng C, et al. Multilocus genotyping of Giardia duodenalis in dairy cattle in Henan, China. PLOS ONE. 2014; 9:e100453. https://doi.org/10.1371/journal.pone.0100453

Broglia A, Weitzel T, Harms G, Cacció SM, Nöckler K. Molecular typing of Giardia duodenalis isolates from German travellers. Parasitol Res. 2013;112:3449-56. https://doi.org/10.1007/s00436-013-3524-y

Wilke H, Robertson LJ. Preservation of Giardia cysts in stool samples for subsequent PCR analysis. J Microbiol Methods. 2009;78:292-6. https://doi.org/10.1016/j.mimet.2009.06.018

Kuk S, Yazar S, Cetinkaya U. Stool sample storage conditions for the preservation of Giardia intestinalis DNA. Mem Inst Oswaldo Cruz. 2012;107:965-8. https://doi.org/10.1590/S0074-02762012000800001

Azcona-Gutiérrez JM, de Lucio A, Hernández-de-Mingo M, García-García C, Soria-Blanco LM, Morales L, et al. Molecular diversity and frequency of the diarrheagenic enteric protozoan Giardia duodenalis and Cryptosporidium spp. in a hospital setting in Northern Spain. PLOS ONE. 2017;12:e0178575. https://doi.org/10.1371/journal.pone.0178 575

Hussein AH, Rashed SM, El-Hayawan IA, Aly NSM, Abou Ouf EA, Ali AT. Intestinal parasite infections and accuracy of direct thin and thick smear, formol-ether sedimentation, centrifugal flotation, and mini-FLOTAC techniques among patients with gastrointestinal tract disorders from the Greater Cairo Region, Egypt. Am J Trop Med Hyg. 2017;96:589-94. https://doi.org/10.4269/ajtmh.16-0436

Lee MF, Cadogan P, Eytle S, Copeland S, Walochnik J, Lindo JF. Molecular epidemiology and multilocus sequence analysis of potentially zoonotic Giardia spp. from humans and dogs in Jamaica. Parasitol Res. 2017;116:409-14. https://doi.org/10.1007/s00436-016-5304-y

Kasaei R, Carmena D, Jelowdar A, Beiromvand M. Molecular genotyping of Giardia duodenalis in children from Behbahan, southwestern Iran. Parasitol Res. 2018;117:1425-31. https://doi.org/10.1007/s00436-018-5826-6

Ramírez JD, Heredia RD, Hernández C, León CM, Moncada LI, Reyes P, et al. Molecular diagnosis and genotype analysis of Giardia duodenalis in asymptomatic children from a rural area in central Colombia. Infect Genet Evol. 2015;32:208-13. https://doi.org/10.1016/j.meegid.2015.03. 015

García-Cervantes PC, Báez-Flores ME, Delgado-Vargas F, Ponce-Macotela, M, Nawa Y, De-la-Cruz-Otero MDC, et al. Giardia duodenalis genotypes among schoolchildren and their families and pets in urban and rural areas of Sinaloa, Mexico. J Infect Dev Ctries. 2017;11:180-7. https://doi.org/10.3855/jidc.8223

Torres-Romero JC, Euan-Canto AJ, Benito-González N, Padilla-Montaño N, Huchin-Chan C, Lara-Riegos J, et al. Intestinal parasites and genotyping of Giardia duodenalis in children: First report of genotype B in isolates from human clinical samples in Mexico. Mem Inst Oswaldo Cruz. 2014;109:388-90. https://doi.org/10.1590/0074-0276140507

Colli CM, Bezagio RC, Nishi L, Bignotto TS, Ferreira ÉC, Falavigna-Guilherme AL, et al. Identical assemblage of Giardia duodenalis in humans, animals and vegetables in an urban area in southern Brazil indicates a relationship among them. PLOS ONE. 2015;10:e0118065. https://doi.org/10.1371/journal.pone.0118065

Coronato Nunes B, Pavan MG, Jaeger LH, Monteiro KJL, Xavier SCC, Monteiro FA, et al. Spatial and molecular epidemiology of Giardia intestinalis deep in the Amazon, Brazil. PLOS ONE. 2016;11:e0158805. https://doi.org/10.1371/journal.pone.0158805

David ÉB, Guimarães S, de Oliveira AP, Goulart de Oliveira-Sequeira TC, Nogueira Bittencourt G, Moraes Nardi AR, et al. Molecular characterization of intestinal protozoa in two poor communities in the State of São Paulo, Brazil. Parasit Vectors. 2015;8:103. https://doi.org/10.1186/s13071-015-0714-8

Quadros RM, Weiss PHE, Marques, SMT, Miletti LC. Potential cross-contamination of similar Giardia duodenalis assemblage in children and pet dogs in southern Brazil, as determined by PCR-RFLP. Rev Inst Med Trop Sao Paulo. 2016;58:66. https://doi.org/10.1590/S1678-9946201658066

Fantinatti M, Bello AR, Fernandes O, Da-Cruz AM. Identification of Giardia lamblia assemblage E in humans points to a new anthropozoonotic cycle. J Infect Dis. 2016;214:1256-9. http://doi.org/10.1093/infdis/jiw361

Seguí R, Muñoz-Antoli C, Klisiowicz DR, Oishi CY, Köster PC, de Lucio A, et al. Prevalence of intestinal parasites, with emphasis on the molecular epidemiology of Giardia duodenalis and Blastocystis sp., in the Paranaguá Bay, Brazil: A community survey. Parasit Vectors. 2018;11:490. https://doi.org/10.1186/s13071-018-3054-7

Durigan M, Abreu AG, Zucchi MI, Franco RMB, de Souza AP. Genetic diversity of Giardia duodenalis: Multilocus genotyping reveals zoonotic potential between clinical and environmental sources in a metropolitan region of Brazil. PLOS ONE. 2014;9:e115489. https://doi.org/10.1371/journal.pone.0115489

Boontanom P, Pipatsatitpong D, Tan-Ariya P, Mungthin M, Siripattanapipong S, Naaglor T, et al. Incidence and risk factors of Giardia duodenalis infection in an orphanage, Thailand. Trop Biomed. 2014;31:525-33.

Wegayehu T, Karim MR, Li J, Adamu H, Erko B, Zhang L, et al. Multilocus genotyping of Giardia duodenalis isolates from children in Oromia Special Zone, central Ethiopia. BMC Microbiol. 2016;16:89. https://doi.org/10.1186/s12866-016-0706-7

Mateo M, Mateo M, Montoya A, Bailo B, Saugar JM, Aguilera M, et al. Detection and molecular characterization of Giardia duodenalis in children attending day care centers in Majadahonda, Madrid, Central Spain. Medicine. 2014;93:e75. https://doi.org/10.1097/MD.0000000000000075

Damitie M, Mekonnen Z, Getahun T, Santiago D, Leyns L. Molecular epidemiology of Giardia duodenalis infection in humans in Southern Ethiopia: A triosephosphate isomerase genetargeted analysis. Infect Dis Poverty. 2018;7:17. https://doi.org/10.1186/s40249-018-0397-4

Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, et al. Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science. 2007;317:19216. https://doi.org/10.1126/science.1143837

Nabaa MT, Muhammed OM, Yassir DK. Iraqi genotyping of Giardia lamblia (A,B,E,F) in human stool in AL-Muthanna province –Iraq. Int J Adv Res. 2015;3:757-71.

Mohammed Mahdy AK, Surin J, Wan KL, Mohd-Adnan A, Al-Mekhlafi MSH, Lim YAL. Giardia intestinalis genotypes: Risk factors and correlation with clinical symptoms. Acta Trop. 2009;112:67-70. https://doi.org/10.1016/j.actatropica.2009.06.012

Tamer GS, Kasap M, Er DK. Genotyping and phylogenetic analysis of Giardia duodenalis isolates from Turkish children. Med Sci Monit. 2015;21:526-32. https://doi.org/10.12659/MSM.892318

Cómo citar
1.
Figueiredo Pacheco FT, Novaes Rodrigues Silva RK, Souza de Carvalho S, Carvalho Rocha F, Trindade das Chagas GM, Chagas Gomes D, da Costa-Ribeiro Junior H, Medrado Ribeiro TC, Peixoto de Mattos Ângela, Kalabric Silva L, Matos Soares N, Aquino Teixeira MC. Predominio del subconjunto AII de Giardia duodenalis en niños pequeños de Salvador, Bahía, Brasil. biomedica [Internet]. 1 de septiembre de 2020 [citado 19 de octubre de 2020];40(3):557-68. Disponible en: https://revistabiomedica.org/index.php/biomedica/article/view/5161
Publicado
2020-09-01
Sección
Artículos originales