High prevalence of Giardia duodenalis Assemblage B infection and association with underweight in Rwandan children

Ralf Ignatius, Jean Bosco Gahutu, Christian Klotz, Christian Steininger, Cyprien Shyirambere, Michel Lyng, Andre Musemakweri, Toni Aebischer, Peter Martus, Gundel Harms, Frank P Mockenhaupt, Ralf Ignatius, Jean Bosco Gahutu, Christian Klotz, Christian Steininger, Cyprien Shyirambere, Michel Lyng, Andre Musemakweri, Toni Aebischer, Peter Martus, Gundel Harms, Frank P Mockenhaupt

Abstract

Background: Giardia duodenalis is highly endemic in East Africa but its effects on child health, particularly of submicroscopic infections, i.e., those below the threshold of microscopy, and of genetic subgroups (assemblages), are not well understood. We aimed at addressing these questions and at examining epidemiological characteristics of G. duodenalis in southern highland Rwanda.

Methodology/principal findings: In 583 children <5 years of age from communities and health facilities, intestinal parasites were assessed by triplicate light microscopy and by PCR assays, and G. duodenalis assemblages were genotyped. Cluster effects of villages were taken into account in statistical analysis. The prevalence of G. duodenalis as detected by microscopy was 19.8% but 60.1% including PCR results. Prevalence differed with residence, increased with age, and was reduced by breastfeeding. In 492 community children without, with submicroscopic and with microscopic infection, underweight (weight-for-age z-score <-2 standard deviations) was observed in 19.7%, 22.1%, and 33.1%, respectively, and clinically assessed severe malnutrition in 4.5%, 9.5%, and 16.7%. Multivariate analysis identified microscopically detectable G. duodenalis infection as an independent predictor of underweight and clinically assessed severe malnutrition. Submicroscopic infection showed respective trends. Overall, G. duodenalis was not associated with gastrointestinal symptoms but assemblages A parasites (proportion, 13%) were increased among children with vomiting and abdominal pain.

Conclusions/significance: The prevalence of G. duodenalis in high-endemicity areas may be greatly underestimated by light microscopy, particularly when only single stool samples are analysed. Children with submicroscopic infections show limited overt manifestation, but constitute unrecognized reservoirs of transmission. The predominance of assemblage B in Rwanda may be involved in the seemingly unimposing manifestation of G. duodenalis infection. However, the association with impaired child growth points to its actual relevance. Longitudinal studies considering abundant submicroscopic infections are needed to clarify the actual contribution of G. duodenalis to morbidity in areas of high endemicity.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1. Distribution of Giardia duodenalis in…
Figure 1. Distribution of Giardia duodenalis in children <5 years of age in Huye sector, Rwanda.

References

    1. Thompson RC, Smith A. Zoonotic enteric protozoa. Vet Parasitol. 2011;182:70– 78.
    1. Pierce KK, Kirkpatrick BD. Update on human infections caused by intestinal protozoa. Curr Opin Gastroenterol. 2009;25:12– 17.
    1. Bodhidatta L, McDaniel P, Sornsakrin S, Srijan A, Serichantalergs O, et al. Case-control study of diarrheal disease etiology in a remote rural area in Western Thailand. Am J Trop Med Hyg. 2010;83:1106– 1109.
    1. Veenemans J, Mank T, Ottenhof M, Baidjoe A, Mbugi EV, et al. Protection against diarrhea associated with Giardia intestinalis Is lost with multi-nutrient supplementation: a study in Tanzanian children. PLoS Negl Trop Dis. 2011;5:e1158.
    1. Berkman DS, Lescano AG, Gilman RH, Lopez SL, Black MM. Effects of stunting, diarrhoeal disease, and parasitic infection during infancy on cognition in late childhood: a follow-up study. Lancet. 2002;359:564– 571.
    1. Caccio SM, Ryan U. Molecular epidemiology of giardiasis. Mol Biochem Parasitol. 2008;160:75– 80.
    1. Lasek-Nesselquist E, Welch DM, Sogin ML. The identification of a new Giardia duodenalis assemblage in marine vertebrates and a preliminary analysis of G. duodenalis population biology in marine systems. Int J Parasitol. 2010;40:1063– 1074.
    1. Read C, Walters J, Robertson ID, Thompson RC. Correlation between genotype of Giardia duodenalis and diarrhoea. Int J Parasitol. 2002;32:229– 231.
    1. Haque R, Roy S, Kabir M, Stroup SE, Mondal D, et al. Giardia assemblage A infection and diarrhea in Bangladesh. J Infect Dis. 2005;192:2171– 2173.
    1. Haque R, Mondal D, Karim A, Molla IH, Rahim A, et al. Prospective case-control study of the association between common enteric protozoal parasites and diarrhea in Bangladesh. Clin Infect Dis. 2009;48:1191– 1197.
    1. Perez Cordon G, Cordova Paz Soldan O, Vargas Vasquez F, Velasco Soto JR, Sempere Bordes L, et al. Prevalence of enteroparasites and genotyping of Giardia lamblia in Peruvian children. Parasitol Res. 2008;103:459– 465.
    1. Sahagun J, Clavel A, Goni P, Seral C, Llorente MT, et al. Correlation between the presence of symptoms and the Giardia duodenalis genotype. Eur J Clin Microbiol Infect Dis. 2008;27:81– 83.
    1. Breathnach AS, McHugh TD, Butcher PD. Prevalence and clinical correlations of genetic subtypes of Giardia lamblia in an urban setting. Epidemiol Infect. 2010;138:1459– 1467.
    1. Homan WL, Mank TG. Human giardiasis: genotype linked differences in clinical symptomatology. Int J Parasitol. 2001;31:822– 826.
    1. Gelanew T, Lalle M, Hailu A, Pozio E, Caccio SM. Molecular characterization of human isolates of Giardia duodenalis from Ethiopia. Acta Trop. 2007;102:92– 99.
    1. Kohli A, Bushen OY, Pinkerton RC, Houpt E, Newman RD, et al. Giardia duodenalis assemblage, clinical presentation and markers of intestinal inflammation in Brazilian children. Trans R Soc Trop Med Hyg. 2008;102:718– 725.
    1. Solaymani-Mohammadi S, Singer SM. Host immunity and pathogen strain contribute to intestinal disaccharidase impairment following gut infection. J Immunol. 2011;187:3769– 3775.
    1. Garcia LS, Shimizu RY. Evaluation of nine immunoassay kits (enzyme immunoassay and direct fluorescence) for detection of Giardia lamblia and Cryptosporidium parvum in human fecal specimens. J Clin Microbiol. 1997;35:1526– 1529.
    1. Regnath T, Klemm T, Ignatius R. Rapid and accurate detection of Giardia lamblia and Cryptosporidium spp. antigens in human fecal specimens by new commercially available qualitative immunochromatographic assays. Eur J Clin Microbiol Infect Dis. 2006;25:807– 809.
    1. Verweij JJ, Blange RA, Templeton K, Schinkel J, Brienen EA, et al. Simultaneous detection of Entamoeba histolytica, Giardia lamblia, and Cryptosporidium parvum in fecal samples by using multiplex real-time PCR. J Clin Microbiol. 2004;42:1220– 1223.
    1. Johnston AR, Gillespie TR, Rwego IB, McLachlan TL, Kent AD, et al. Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda. PLoS Negl Trop Dis. 2010;4:e683.
    1. Ekdahl K, Andersson Y. Imported giardiasis: impact of international travel, immigration, and adoption. Am J Trop Med Hyg. 2005;72:825– 830.
    1. Twahirwa A. Sharing the burden of sickness: mutual health insurance in Rwanda. Bull World Health Organ. 2008;86:823– 824.
    1. Gahutu JB, Steininger C, Shyirambere C, Zeile I, Cwinya-Ay N. Prevalence and risk factors of malaria among children in southern highland Rwanda. Malar J. 2011;10:134.
    1. WHO WHO Anthro software.
    1. Ministry of Health K, Rwanda Protocoles des Services de Santé.
    1. Allen AV, Ridley DS. Further observations on the formol-ether concentration technique for faecal parasites. J Clin Pathol. 1970;23:545– 546.
    1. Niesters HG. Clinical virology in real time. J Clin Virol. 2002;25:S3– 12.
    1. Verweij JJ, Brienen EA, Ziem J, Yelifari L, Polderman AM, et al. Simultaneous detection and quantification of Ancylostoma duodenale, Necator americanus, and Oesophagostomum bifurcum in fecal samples using multiplex real-time PCR. Am J Trop Med Hyg. 2007;77:685– 690.
    1. Basuni M, Muhi J, Othman N, Verweij JJ, Ahmad M, et al. A pentaplex real-time polymerase chain reaction assay for detection of four species of soil-transmitted helminths. Am J Trop Med Hyg. 2011;84:338– 343.
    1. Sulaiman IM, Fayer R, Bern C, Gilman RH, Trout JM, et al. Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis. Emerg Infect Dis. 2003;9:1444– 1452.
    1. Sprong H, Caccio SM, van der Giessen JW. Identification of zoonotic genotypes of Giardia duodenalis. PLoS Negl Trop Dis. 2009;3:e558.
    1. Zeger SL, Liang KY. Longitudinal data analysis for discrete and continuous outcomes. Biometrics. 1986;42:121– 130.
    1. Stensvold CR, Nielsen HV. Comparison of microscopy and PCR for detection of intestinal parasites in Danish patients supports an incentive for molecular screening platforms. J Clin Microbiol. 2012;50:540– 541.
    1. Schuurman T, Lankamp P, van Belkum A, Kooistra-Smid M, van Zwet A. Comparison of microscopy, real-time PCR and a rapid immunoassay for the detection of Giardia lamblia in human stool specimens. Clin Microbiol Infect. 2007;13:1186– 1191.
    1. Muniz-Junqueira MI, Queiroz EF. Relationship between protein-energy malnutrition, vitamin A, and parasitoses in living in Brasilia. Rev Soc Bras Med Trop. 2002;35:133– 141.
    1. Nematian J, Gholamrezanezhad A, Nematian E. Giardiasis and other intestinal parasitic infections in relation to anthropometric indicators of malnutrition: a large, population-based survey of schoolchildren in Tehran. Ann Trop Med Parasitol. 2008;102:209– 214.
    1. Loewenson R, Mason PR, Patterson BA. Giardiasis and the nutritional status of Zimbabwean schoolchildren. Ann Trop Paediatr. 1986;6:73– 78.
    1. Fraser D, Bilenko N, Deckelbaum RJ, Dagan R, El-On J, et al. Giardia lamblia carriage in Israeli Bedouin infants: risk factors and consequences. Clin Infect Dis. 2000;30:419– 424.
    1. Newman RD, Moore SR, Lima AA, Nataro JP, Guerrant RL, et al. A longitudinal study of Giardia lamblia infection in north-east Brazilian children. Trop Med Int Health. 2001;6:624– 634.
    1. Al-Mekhlafi MS, Azlin M, Nor Aini U, Shaik A, Sa'iah A, et al. Giardiasis as a predictor of childhood malnutrition in Orang Asli children in Malaysia. Trans R Soc Trop Med Hyg. 2005;99:686– 691.
    1. Carvalho-Costa FA, Goncalves AQ, Lassance SL, Silva Neto LM, Salmazo CA, et al. Giardia lamblia and other intestinal parasitic infections and their relationships with nutritional status in children in Brazilian Amazon. Rev Inst Med Trop Sao Paulo. 2007;49:147– 153.
    1. Molina N, Minvielle M, Grenovero S, Salomon C, Basualdo J. High prevalences of infection with Giardia intestinalis genotype B among children in urban and rural areas of Argentina. Ann Trop Med Parasitol. 2011;105:299– 309.
    1. Mahmud MA, Chappell CL, Hossain MM, Huang DB, Habib M, et al. Impact of breast-feeding on Giardia lamblia infections in Bilbeis, Egypt. Am J Trop Med Hyg. 2001;65:257– 260.
    1. Tellez A, Winiecka-Krusnell J, Paniagua M, Linder E. Antibodies in mother's milk protect children against giardiasis. Scand J Infect Dis. 2003;35:322– 325.
    1. Langford TD, Housley MP, Boes M, Chen J, Kagnoff MF, et al. Central importance of immunoglobulin A in host defense against Giardia spp. Infect Immun. 2002;70:11– 18.
    1. Ochoa TJ, Chea-Woo E, Campos M, Pecho I, Prada A, et al. Impact of lactoferrin supplementation on growth and prevalence of Giardia colonization in children. Clin Infect Dis. 2008;46:1881– 1883.
    1. Franca-Botelho AC, Honorio-Franca AC, Franca EL, Gomes MA, Costa-Cruz JM. Phagocytosis of Giardia lamblia trophozoites by human colostral leukocytes. Acta Paediatr. 2006;95:438– 443.
    1. Sullivan PS, DuPont HL, Arafat RR, Thornton SA, Selwyn BJ, et al. Illness and reservoirs associated with Giardia lamblia infection in rural Egypt: the case against treatment in developing world environments of high endemicity. Am J Epidemiol. 1988;127:1272– 1281.
    1. Prado MS, Cairncross S, Strina A, Barreto ML, Oliveira-Assis AM, et al. Asymptomatic giardiasis and growth in young children; a longitudinal study in Salvador, Brazil. Parasitology. 2005;131:51– 56.
    1. Goto R, Mascie-Taylor CG, Lunn PG. Impact of anti-Giardia and anthelminthic treatment on infant growth and intestinal permeability in rural Bangladesh: a randomised double-blind controlled study. Trans R Soc Trop Med Hyg. 2009;103:520– 529.
    1. Long KZ, Rosado JL, Montoya Y, de Lourdes Solano M, Hertzmark E, et al. Effect of vitamin A and zinc supplementation on gastrointestinal parasitic infections among Mexican children. Pediatrics. 2007;120:e846– 855.

Source: PubMed

Patrocinadores y Colaboradores

Condiciones médicas

Intervenciones de drogas

3
Suscribir