Multiparasitism and intensity of helminth infections in relation to symptoms and nutritional status among children: A cross-sectional study in southern Lao People's Democratic Republic

Acta Tropica

Volumn 141, Issue Part B, 2015, Pages 322-331

  Sayasone, Somphou ^a,b,c   Utzinger, Jürg ^b,c   Akkhavong, Kongsap ^a   Odermatt, Peter ^b,c  

^a Ministry of Health   (Laos)

^b SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Anaemia; Food borne trematodiasis; Lao People's Democratic Republic; Nutrition; Soil transmitted helminthiasis; Symptoms

Indexed keywords

ANEMIA; INFECTIOUS DISEASE; MORBIDITY; NUTRITION; NUTRITIONAL STATUS; PARASITISM; SYMPTOM;

ABDOMINAL PAIN; ANEMIA; ARTICLE; BODY MASS; CHILD; CHILD HEALTH; CLINICAL FEATURE; CONJUNCTIVA; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DISEASE SEVERITY; FECES ANALYSIS; FEMALE; HELMINTHIASIS; HEPATOMEGALY; HUMAN; LAOS; MAJOR CLINICAL STUDY; MALE; MORBIDITY; NUTRITIONAL STATUS; OPISTHORCHIS VIVERRINI; PARASITISM; PHYSICAL EXAMINATION; PRESCHOOL CHILD; SCHISTOSOMA; SCHISTOSOMA MEKONGI; SCHOOL CHILD; SEX DIFFERENCE; ANCYLOSTOMIASIS; ANIMAL; BODY WEIGHT; COINFECTION; COMPLICATION; FECES; GASTROINTESTINAL HEMORRHAGE; HELMINTH; HOOKWORM; HOOKWORM INFECTIONS; INFANT; INTESTINAL DISEASES, PARASITIC; OPISTHORCHIASIS; OPISTHORCHIS; PATHOPHYSIOLOGY; PREVALENCE; QUESTIONNAIRE; RURAL POPULATION; SCHISTOSOMIASIS; STATISTICAL MODEL; STATISTICS AND NUMERICAL DATA;

LAOS;

ANCYLOSTOMATOIDEA; OPISTHORCHIS VIVERRINI; SCHISTOSOMA MEKONGI; VERMES;

ANCYLOSTOMATOIDEA; ANCYLOSTOMIASIS; ANEMIA; ANIMALS; CHILD; CHILD, PRESCHOOL; COINFECTION; CROSS-SECTIONAL STUDIES; FECES; FEMALE; GASTROINTESTINAL HEMORRHAGE; HELMINTHIASIS; HELMINTHS; HOOKWORM INFECTIONS; HUMANS; INFANT; INTESTINAL DISEASES, PARASITIC; LAOS; LOGISTIC MODELS; MALE; NUTRITIONAL STATUS; OPISTHORCHIASIS; OPISTHORCHIS; PREVALENCE; RURAL POPULATION; SCHISTOSOMIASIS; SURVEYS AND QUESTIONNAIRES; THINNESS;

EID: 84916927319     PISSN: 0001706X     EISSN: 18736254     Source Type: Journal    
DOI: 10.1016/j.actatropica.2014.09.015     Document Type: Article

References (62)

1. Al-Mekhlafi H.M., Azlin M., Aini U.N., Shaik A., Sa'iah A., Fatmah M.S., Ismail M.G., Ahmad F., Aisah M.Y., Rozlida A.R., Norhayatiy M. Protein-energy malnutrition and soil-transmitted helminthiases among Orang Asli children in Selangor, Malaysia. Asia Pac. J. Clin. Nutr. 2005, 14:188-194.
2. Alom J., Quddus M.A., Islam M.A. Nutritional status of under-five children in Bangladesh: a multilevel analysis. J. Biosoc. Sci. 2012, 44:525-535.
3. Becker S.L., Vogt J., Knopp S., Panning M., Warhurst D.C., Polman K., Marti H., von Müller L., Yansouni C.P., Jacobs J., Bottieau E., Sacko M., Rijal S., Meyanti F., Miles M.A., Boelaert M., Lutumba P., van Lieshout L., N'Goran E.K., Chappuis F., Utzinger J. Persistent digestive disorders in the tropics: causative infectious pathogens and reference diagnostic tests. BMC Infect. Dis. 2013, 13:37.
4. Bergquist R., Johansen M.V., Utzinger J. Diagnostic dilemmas in helminthology: what tools to use and when?. Trends Parasitol. 2009, 25:151-156.
5. Biays S., Stich A.H., Odermatt P., Long C., Yersin C., Men C., Saem C., Lormand J.D. [A foci of schistosomiasis mekongi rediscovered in Northeast Cambodia: cultural perception of the illness; description and clinical observation of 20 severe cases]. Trop. Med. Int. Health 1999, 4:662-673. (in French).
6. Brooker S., Hotez P.J., Bundy D.A.P. Hookworm-related anaemia among pregnant women: a systematic review. PLoS Negl. Trop. Dis. 2008, 2:e291.
7. Bryce J., Boschi-Pinto C., Shibuya K., Black R.E. WHO estimates of the causes of death in children. Lancet 2005, 365:1147-1152.
8. Bundy D.A.P., Kremer M., Bleakley H., Jukes M.C.H., Miguel E. Deworming and development: asking the right questions, asking the questions right. PLoS Negl. Trop Dis. 2009, 3:e362.
9. Bustinduy A.L., Parraga I.M., Thomas C.L., Mungai P.L., Mutuku F., Muchiri E.M., Kitron U., King C.H. Impact of polyparasitic infections on anemia and undernutrition among Kenyan children living in a Schistosoma haematobium-endemic area. Am. J. Trop. Med. Hyg. 2013, 88:433-440.
10. Chai J.Y., Han E.T., Guk S.M., Shin E.H., Sohn W.M., Yong T.S., Eom K.S., Lee K.H., Jeong H.G., Ryang Y.S., Hoang E.H., Phommasack B., Insisiengmay B., Lee S.H., Rim H.J. High prevalence of liver and intestinal fluke infections among residents of Savannakhet province in Laos. Korean J. Parasitol. 2007, 45:213-218.
11. Chai J.Y., Park J.H., Han E.T., Guk S.M., Shin E.H., Lin A., Kim J.L., Sohn W.M., Yong T.S., Eom K.S., Min D.Y., Hwang E.H., Phommmasack B., Insisiengmay B., Rim H.J. Mixed infections with Opisthorchis viverrini and intestinal flukes in residents of Vientiane municipality and Saravane province in Laos. J. Helminthol. 2005, 79:283-289.
12. Chen J.M., Zhang X.M., Wang L.J., Chen Y., Du Q., Cai J.T. Overt gastrointestinal bleeding because of hookworm infection. Asian Pac. J. Trop. Med. 2012, 5:331-332.
13. Colley D.G., Bustinduy A.L., Secor W.E., King C.H. Human schistosomiasis. Lancet 2014, 383:2253-2264.
14. Darapheak C., Takano T., Kizuki M., Nakamura K., Seino K. Consumption of animal source foods and dietary diversity reduce stunting in children in Cambodia. Int. Arch. Med. 2013, 6:29.
15. de Onis M., Onyango A.W., Borghi E., Siyam A., Nishida C., Siekmann J. Development of a WHO growth reference for school-aged children and adolescents. Bull. World Health Organ. 2007, 85:660-667.
16. Degarege A., Animut A., Medhin G., Legesse M., Erko B. The association between multiple intestinal helminth infections and blood group, anaemia and nutritional status in human populations from Dore Bafeno, southern Ethiopia. J. Helminthol. 2014, 88:152-159.
17. Eom K.S., Yong T.S., Sohn W.M., Chai J.Y., Min D.Y., Rim H.J., Jeon H.K., Banouvong V., Insisiengmay B., Phommasack B. Prevalence of helminthic infections among inhabitants of Lao PDR. Korean J. Parasitol. 2014, 52:51-56.
18. Ezeamama A.E., Friedman J.F., Olveda R.M., Acosta L.P., Kurtis J.D., Mor V., McGarvey S.T. Functional significance of low-intensity polyparasite helminth infections in anemia. J. Infect. Dis. 2005, 192:2160-2170.
19. Forrer A., Sayasone S., Vounatsou P., Vonghachack Y., Bouakhasith D., Vogt S., Glaser R., Utzinger J., Akkhavong K., Odermatt P. Spatial distribution of, and risk factors for, Opisthorchis viverrini infection in southern Lao PDR. PLoS Negl. Trop. Dis. 2012, 6:e1481.
20. Fürst T., Duthaler U., Sripa B., Utzinger J., Keiser J. Trematode infections: liver and lung flukes. Infect. Dis. Clin. North Am. 2012, 26:399-419.
21. Fürst T., Keiser J., Utzinger J. Global burden of human food-borne trematodiasis: a systematic review and meta-analysis. Lancet Infect. Dis. 2012, 12:210-221.
22. Gyorkos T.W., Gilbert N.L., Larocque R., Casapia M. Trichuris and hookworm infections associated with anaemia during pregnancy. Trop. Med. Int. Health 2011, 16:531-537.
23. Hackett L.W. Spleen measurement in malaria. J. Natl. Malar. Soc. 1944, 121-123.
24. Hall A., Hewitt G., Tuffrey V., de S.N. A review and meta-analysis of the impact of intestinal worms on child growth and nutrition. Matern. Child Nutr. 2008, 4(Suppl 1):118-236.
25. Hotez P.J., Brindley P.J., Bethony J.M., King C.H., Pearce E.J., Jacobson J. Helminth infections: the great neglected tropical diseases. J. Clin. Invest. 2008, 118:1311-1321.
26. Kamiya Y. Socioeconomic determinants of nutritional status of children in Lao PDR: effects of household and community factors. J. Health Popul. Nutr. 2011, 29:339-348.
27. Katz N., Chaves A., Pellegrino J. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev. Inst. Med. Trop. São Paulo 1972, 14:397-400.
28. Knopp S., Mgeni A.F., Khamis I.S., Steinmann P., Stothard J.R., Rollinson D., Marti H., Utzinger J. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl. Trop. Dis. 2008, 2:e331.
29. Lao PDR Country Programme Document, 2007-2011 2014, Lao People's Democratic Republic, Available at: www.unicef.org/about/execboard/files/Lao.
30. Larocque R., Casapia M., Gotuzzo E., Gyorkos T.W. Relationship between intensity of soil-transmitted helminth infections and anemia during pregnancy. Am. J. Trop. Med. Hyg. 2005, 73:783-789.
31. Lovis L., Mak T.K., Phongluxa K., Aye-Soukhathammavong P., Vonghachack Y., Keiser J., Vounatsou P., Tanner M., Hatz C., Utzinger J., Odermatt P., Akkhavong K. Efficacy of praziquantel against Schistosoma mekongi and Opisthorchis viverrini: a randomized, single-blinded dose-comparison trial. PLoS Negl. Trop. Dis. 2012, 6:e1726.
32. Maleewong W., Intapan P., Wongwajana S., Sitthithaworn P., Pipitgool V., Wongkham C., Daenseegaew W. Prevalence and intensity of Opisthorchis viverrini in rural community near the Mekong River on the Thai-Laos border in northeast Thailand. J. Med. Assoc. Thai. 1992, 75:231-235.
33. Manning L., Laman M., Rosanas-Urgell A., Michon P., Aipit S., Bona C., Siba P., Mueller I., Davis T.M. Severe anemia in Papua New Guinean children from a malaria-endemic area: a case-control etiologic study. PLoS Negl. Trop Dis. 2012, 6:e1972.
34. MOH Diagnosis and treatment in district hospitals. A Diagnosis and Treatment Guideline for the District Hospital in Lao PDR 2004, Ministry of Health, Vientiane.
35. Mondal D., Minak J., Alam M., Liu Y., Dai J., Korpe P., Liu L., Haque R., Petri W.A. Contribution of enteric infection, altered intestinal barrier function, and maternal malnutrition to infant malnutrition in Bangladesh. Clin. Infect. Dis. 2012, 54:185-192.
36. Murray C.J.L., Vos T., Lozano R., Naghavi M., Flaxman A.D., Michaud C., Ezzati M., Shibuya K., Salomon J.A., Abdalla S., Aboyans V., Abraham J., Ackerman I., Aggarwal R., Ahn S.Y., Ali M.K., Alvarado M., Anderson H.R., Anderson L.M., Andrews K.G., Atkinson C., Baddour L.M., Bahalim A.N., Barker-Collo S., Barrero L.H., et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012, 380:2197-2223.
37. Muth S., Sayasone S., Odermatt-Biays S., Phompida S., Duong S., Odermatt P. Schistosoma mekongi in Cambodia and Lao People's Democratic Republic. Adv. Parasitol. 2010, 72:179-203.
38. Ngui R., Lim Y.A., Chong K.L., Sek C.C., Jaffar S. Association between anaemia, iron deficiency anaemia, neglected parasitic infections and socioeconomic factors in rural children of West Malaysia. PLoS Negl. Trop. Dis. 2012, 6:e1550.
39. Oninla S.O., Onayade A.A., Owa J.A. Impact of intestinal helminthiases on the nutritional status of primary-school children in Osun state, south-western Nigeria. Ann. Trop. Med. Parasitol. 2010, 104:583-594.
40. Pasricha S.R., Caruana S.R., Phuc T.Q., Casey G.J., Jolley D., Kingsland S., Tien N.T., MacGregor L., Montresor A., Biggs B.A. Anemia, iron deficiency, meat consumption, and hookworm infection in women of reproductive age in northwest Vietnam. Am. J. Trop. Med. Hyg. 2008, 78:375-381.
41. Phommasack B., Saklokham K., Chanthavisouk C., Nakhonesid-Fish V., Strandgaard H., Montresor A., Shuey D.A., Ehrenberg J. Coverage and costs of a school deworming programme in 2007 targeting all primary schools in Lao PDR. Trans. R. Soc. Trop. Med. Hyg. 2008, 102:1201-1206.
42. Phongluxa K., Xayaseng V., Vonghachack Y., Akkhavong K., van E.P., Odermatt P. Helminth infection in southern Laos: high prevalence and low awareness. Parasit. Vectors 2013, 6:328.
43. Pullan R.L., Brooker S.J. The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasit. Vectors 2012, 5:81.
44. Pullan R.L., Smith J.L., Jasrasaria R., Brooker S.J. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit. Vectors 2014, 7:37.
45. Quinnell R.J. Genetics of susceptibility to human helminth infection. Int. J. Parasitol. 2003, 33:1219-1231.
46. Righetti A.A., Adiossan L.G., Ouattara M., Glinz D., Hurrell R.F., N'Goran E.K., Wegmüller R., Utzinger J. Dynamics of anemia in relation to parasitic infections, micronutrient status, and increasing age in south-central CÔte d'Ivoire. J. Infect. Dis. 2013, 207:1604-1615.
47. Rim H.J., Chai J.Y., Min D.Y., Cho S.Y., Eom K.S., Hong S.J., Sohn W.M., Yong T.S., Deodato G., Standgaard H., Phommasack B., Yun C.H., Hoang E.H. Prevalence of intestinal parasite infections on a national scale among primary schoolchildren in Laos. Parasitol. Res. 2003, 91:267-272.
48. Savongsy O., Fucharoen S., Fucharoen G., Sanchaisuriya K., Sae-Ung N. Thalassemia and hemoglobinopathies in pregnant Lao women: carrier screening, prevalence and molecular basis. Ann. Hematol. 2008, 87:647-654.
49. Sayasone S., Mak T.K., Vanmany M., Rasphone O., Vounatsou P., Utzinger J., Akkhavong K., Odermatt P. Helminth and intestinal protozoa infections, multiparasitism and risk factors in Champasack province, Lao People's Democratic Republic. PLoS Negl. Trop. Dis. 2011, 5:e1037.
50. Sayasone S., Odermatt P., Phoumindr N., Vongsaravane X., Sensombath V., Phetsouvanh R., Choulamany X., Strobel M. Epidemiology of Opisthorchis viverrini in a rural district of southern Lao PDR. Trans. R. Soc. Trop. Med. Hyg. 2007, 101:40-47.
51. Sayasone S., Rasphone O., Vanmany M., Vounatsou P., Utzinger J., Tanner M., Akkhavong K., Hatz C., Odermatt P. Severe morbidity due to Opisthorchis viverrini and Schistosoma mekongi infection in Lao People's Democratic Republic. Clin. Infect. Dis 2012, 55:e54-e57.
52. Sayasone S., Vonghajack Y., Vanmany M., Rasphone O., Tesana S., Utzinger J., Akkhavong K., Odermatt P. Diversity of human intestinal helminthiasis in Lao PDR. Trans. R. Soc. Trop. Med. Hyg. 2009, 103:247-254.
53. Speich B., Knopp S., Mohammed K.A., Khamis I.S., Rinaldi L., Cringoli G., Rollinson D., Utzinger J. Comparative cost assessment of the Kato-Katz and FLOTAC techniques for soil-transmitted helminth diagnosis in epidemiological surveys. Parasit. Vectors 2010, 3:71.
54. Steinmann P., Du Z.W., Wang L.B., Wang X.Z., Jiang J.Y., Li L.H., Marti H., Zhou X.N., Utzinger J. Extensive multiparasitism in a village of Yunnan province, People's Republic of China, revealed by a suite of diagnostic methods. Am. J. Trop. Med. Hyg. 2008, 78:760-769.
55. Steinmann P., Utzinger J., Du Z.W., Zhou X.N. Multiparasitism: a neglected reality on global, regional and local scale. Adv. Parasitol. 2010, 73:21-50.
56. Taylor-Robinson D.C., Maayan N., Soares-Weiser K., Donegan S., Garner P. Deworming drugs for soil-transmitted intestinal worms in children: effects on nutritional indicators, haemoglobin and school performance. Cochrane Database Syst. Rev. 2012, 11:CD000371.
57. Tritipsombut J., Sanchaisuriya K., Phollarp P., Bouakhasith D., Sanchaisuriya P., Fucharoen G., Fucharoen S., Schelp F.P. Micromapping of thalassemia and hemoglobinopathies in diferent regions of northeast Thailand and Vientiane, Laos People's Democratic Republic. Hemoglobin 2012, 36:47-56.
58. Utzinger J., Becker S.L., Knopp S., Blum J., Neumayr A.L., Keiser J., Hatz C.F. Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Med. Wkly. 2012, 142:w13727.
59. WHO Deworming for health and development. Report of the Third Global Meeting of the Partners for Parasite Control 2005, World Health Organization.
60. WHO Growth Reference Data for 5-19 Years: WHO Anthro Plus Software Developed by Technical Group 2007, World Health Organization, Geneva, www.who.int/growthref/tools/en.
61. WHO Worldwide prevalence of anaemia 1993-2005 2014, Word Health Organization, Geneva, (Accessed 25.3.2009).
62. Yap P., Fürst T., Müller I., Kriemler S., Utzinger J., Steinmann P. Determining soil-transmitted helminth infection status and physical fitness of school-aged children. J. Vis. Exp. 2012, 66:e3966.