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Published in: BMC Infectious Diseases 1/2014

Open Access 01-12-2014 | Research article

Enterobiasis and strongyloidiasis and associated co-infections and morbidity markers in infants, preschool- and school-aged children from rural coastal Tanzania: a cross-sectional study

Authors: Nahya Salim, Tobias Schindler, Ummi Abdul, Julian Rothen, Blaise Genton, Omar Lweno, Alisa S Mohammed, John Masimba, Denis Kwaba, Salim Abdulla, Marcel Tanner, Claudia Daubenberger, Stefanie Knopp

Published in: BMC Infectious Diseases | Issue 1/2014

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Abstract

Background

There is a paucity of data pertaining to the epidemiology and public health impact of Enterobius vermicularis and Strongyloides stercoralis infections. We aimed to determine the extent of enterobiasis, strongyloidiasis, and other helminth infections and their association with asymptomatic Plasmodium parasitaemia, anaemia, nutritional status, and blood cell counts in infants, preschool-aged (PSAC), and school-aged children (SAC) from rural coastal Tanzania.

Methods

A total of 1,033 children were included in a cross-sectional study implemented in the Bagamoyo district in 2011/2012. Faecal samples were examined for intestinal helminth infections using a broad set of quality controlled methods. Finger-prick blood samples were subjected to filariasis and Plasmodium parasitaemia testing and full blood cell count examination. Weight, length/height, and/or mid-upper arm circumference were measured and the nutritional status determined in accordance with age.

Results

E. vermicularis infections were found in 4.2% of infants, 16.7%, of PSAC, and 26.3% of SAC. S. stercoralis infections were detected in 5.8%, 7.5%, and 7.1% of infants, PSAC, and SAC, respectively. Multivariable regression analyses revealed higher odds of enterobiasis in children of all age-groups with a reported anthelminthic treatment history over the past six months (odds ratio (OR): 2.15; 95% confidence interval (CI): 1.22 - 3.79) and in SAC with a higher temperature (OR: 2.21; CI: 1.13 - 4.33). Strongyloidiasis was associated with eosinophilia (OR: 2.04; CI: 1.20-3.48) and with Trichuris trichiura infections (OR: 4.13; CI: 1.04-16.52) in children of all age-groups, and with asymptomatic Plasmodium parasitaemia (OR: 13.03; CI: 1.34 - 127.23) in infants. None of the investigated helminthiases impacted significantly on the nutritional status and anaemia, but moderate asymptomatic Plasmodium parasitaemia was a strong predictor for anaemia in children aged older than two years (OR: 2.69; 95% CI: 1.23 – 5.86).

Conclusions

E. vermicularis and S. stercoralis infections were moderately prevalent in children from rural coastal Tanzania. Our data can contribute to inform yet missing global burden of disease and prevalence estimates for strongyloidiasis and enterobiasis. The association between S stercoralis and asymptomatic Plasmodium parasitaemia found here warrants further comprehensive investigations.
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Literature
1.
go back to reference Utzinger J, Becker SL, Knopp S, Blum J, Neumayr AL, Keiser J, Hatz CF: Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Med Wkly. 2012, 142: w13727-PubMed Utzinger J, Becker SL, Knopp S, Blum J, Neumayr AL, Keiser J, Hatz CF: Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Med Wkly. 2012, 142: w13727-PubMed
2.
go back to reference Knopp S, Steinmann P, Keiser J, Utzinger J: Nematode infections: soil-transmitted helminths and Trichinella . Infect Dis Clin North Am. 2012, 26 (2): 341-358. 10.1016/j.idc.2012.02.006.CrossRefPubMed Knopp S, Steinmann P, Keiser J, Utzinger J: Nematode infections: soil-transmitted helminths and Trichinella . Infect Dis Clin North Am. 2012, 26 (2): 341-358. 10.1016/j.idc.2012.02.006.CrossRefPubMed
3.
go back to reference Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ: Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006, 367 (9521): 1521-1532. 10.1016/S0140-6736(06)68653-4.CrossRefPubMed Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ: Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006, 367 (9521): 1521-1532. 10.1016/S0140-6736(06)68653-4.CrossRefPubMed
4.
go back to reference Pullan RL, Smith JL, Jasrasaria R, Brooker SJ: Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014, 7: 37-10.1186/1756-3305-7-37.CrossRefPubMedPubMedCentral Pullan RL, Smith JL, Jasrasaria R, Brooker SJ: Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors. 2014, 7: 37-10.1186/1756-3305-7-37.CrossRefPubMedPubMedCentral
5.
go back to reference Hotez PJ, Alvarado M, Basáñez MG, Bolliger I, Bourne R, Boussinesq M, Brooker SJ, Brown AS, Buckle G, Budke CM, Carabin H, Coffeng LE, Fevre EM, Fürst T, Halasa YA, Jasrasaria R, Johns NE, Keiser J, King CH, Lozano R, Murdoch ME, O'Hanlon S, Pion SD, Pullan RL, Ramaiah KD, Roberts T, Shepard DS, Smith JL, Stolk WA, Undurraga EA, et al: The Global Burden of Disease Study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl Trop Dis. 2014, 8 (7): e2865-10.1371/journal.pntd.0002865.CrossRefPubMedPubMedCentral Hotez PJ, Alvarado M, Basáñez MG, Bolliger I, Bourne R, Boussinesq M, Brooker SJ, Brown AS, Buckle G, Budke CM, Carabin H, Coffeng LE, Fevre EM, Fürst T, Halasa YA, Jasrasaria R, Johns NE, Keiser J, King CH, Lozano R, Murdoch ME, O'Hanlon S, Pion SD, Pullan RL, Ramaiah KD, Roberts T, Shepard DS, Smith JL, Stolk WA, Undurraga EA, et al: The Global Burden of Disease Study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl Trop Dis. 2014, 8 (7): e2865-10.1371/journal.pntd.0002865.CrossRefPubMedPubMedCentral
6.
go back to reference Murray CJL, Vos T, Lozano R, Naghavi M, Flaxman AD, Michaud C, Ezzati M, Shibuya K, Salomon JA, Abdalla S, Aboyans V, Abraham J, Ackerman I, Aggarwal R, Ahn SY, Ali MK, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Bahalim AN, Barker-Collo S, Barrero LH, Bartels DH, Basáñez MG, Baxter A, Bell ML, Benjamin EJ, 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 (9859): 2197-2223. 10.1016/S0140-6736(12)61689-4.CrossRefPubMed Murray CJL, Vos T, Lozano R, Naghavi M, Flaxman AD, Michaud C, Ezzati M, Shibuya K, Salomon JA, Abdalla S, Aboyans V, Abraham J, Ackerman I, Aggarwal R, Ahn SY, Ali MK, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Bahalim AN, Barker-Collo S, Barrero LH, Bartels DH, Basáñez MG, Baxter A, Bell ML, Benjamin EJ, 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 (9859): 2197-2223. 10.1016/S0140-6736(12)61689-4.CrossRefPubMed
7.
go back to reference Krolewiecki AJ, Lammie P, Jacobson J, Gabrielli AF, Levecke B, Socias E, Arias LM, Sosa N, Abraham D, Cimino R, Echazu A, Crudo F, Vercruysse J, Albonico M: A public health response against Strongyloides stercoralis: time to look at soil-transmitted helminthiasis in full. PLoS Negl Trop Dis. 2013, 7 (5): e2165-10.1371/journal.pntd.0002165.CrossRefPubMedPubMedCentral Krolewiecki AJ, Lammie P, Jacobson J, Gabrielli AF, Levecke B, Socias E, Arias LM, Sosa N, Abraham D, Cimino R, Echazu A, Crudo F, Vercruysse J, Albonico M: A public health response against Strongyloides stercoralis: time to look at soil-transmitted helminthiasis in full. PLoS Negl Trop Dis. 2013, 7 (5): e2165-10.1371/journal.pntd.0002165.CrossRefPubMedPubMedCentral
8.
go back to reference Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P, Stothard R, Thybo S, Verweij JJ, Magnussen P: Strongyloidiasis – the most neglected of the neglected tropical diseases?. Trans R Soc Trop Med Hyg. 2009, 103: 967-972. 10.1016/j.trstmh.2009.02.013.CrossRefPubMed Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P, Stothard R, Thybo S, Verweij JJ, Magnussen P: Strongyloidiasis – the most neglected of the neglected tropical diseases?. Trans R Soc Trop Med Hyg. 2009, 103: 967-972. 10.1016/j.trstmh.2009.02.013.CrossRefPubMed
9.
go back to reference Knopp S, Salim N, Schindler T, Karagiannis Voules DA, Abduhl U, Rothen J, Lweno O, Mohammed AS, Genton B, Daubenberger C: Diagnostic accuracy of Kato-Katz, FLOTAC, Baermann and PCR methods for the detection of light intensity hookworm and Strongyloides stercoralis infections in Tanzania. Am J Trop Med. 2014, 90 (3): 535-545. 10.4269/ajtmh.13-0268.CrossRef Knopp S, Salim N, Schindler T, Karagiannis Voules DA, Abduhl U, Rothen J, Lweno O, Mohammed AS, Genton B, Daubenberger C: Diagnostic accuracy of Kato-Katz, FLOTAC, Baermann and PCR methods for the detection of light intensity hookworm and Strongyloides stercoralis infections in Tanzania. Am J Trop Med. 2014, 90 (3): 535-545. 10.4269/ajtmh.13-0268.CrossRef
10.
go back to reference Becker SL, Sieto B, Silue KD, Adjossan L, Kone S, Hatz C, Kern WV, N'Goran EK, Utzinger J: Diagnosis, clinical features, and self-reported morbidity of Strongyloides stercoralis and hookworm infection in a co-endemic setting. PLoS Negl Trop Dis. 2011, 5 (8): e1292-10.1371/journal.pntd.0001292.CrossRefPubMedPubMedCentral Becker SL, Sieto B, Silue KD, Adjossan L, Kone S, Hatz C, Kern WV, N'Goran EK, Utzinger J: Diagnosis, clinical features, and self-reported morbidity of Strongyloides stercoralis and hookworm infection in a co-endemic setting. PLoS Negl Trop Dis. 2011, 5 (8): e1292-10.1371/journal.pntd.0001292.CrossRefPubMedPubMedCentral
11.
go back to reference Montes M, Sawhney C, Barros N: Strongyloides stercoralis: there but not seen. Curr Opin Infect Dis. 2010, 23 (5): 500-504. 10.1097/QCO.0b013e32833df718.CrossRefPubMedPubMedCentral Montes M, Sawhney C, Barros N: Strongyloides stercoralis: there but not seen. Curr Opin Infect Dis. 2010, 23 (5): 500-504. 10.1097/QCO.0b013e32833df718.CrossRefPubMedPubMedCentral
12.
go back to reference Greaves D, Coggle S, Pollard C, Aliyu SH, Moore EM: Strongyloides stercoralis infection. BMJ. 2013, 347: f4610-10.1136/bmj.f4610.CrossRefPubMed Greaves D, Coggle S, Pollard C, Aliyu SH, Moore EM: Strongyloides stercoralis infection. BMJ. 2013, 347: f4610-10.1136/bmj.f4610.CrossRefPubMed
13.
go back to reference Leder K, Weller PF: Eosinophilia and helminthic infections. Baillieres Best Pract Res Clin Haematol. 2000, 13 (2): 301-317. 10.1053/beha.1999.0074.CrossRefPubMed Leder K, Weller PF: Eosinophilia and helminthic infections. Baillieres Best Pract Res Clin Haematol. 2000, 13 (2): 301-317. 10.1053/beha.1999.0074.CrossRefPubMed
14.
15.
go back to reference Khieu V, Srey S, Schar F, Muth S, Marti H, Odermatt P: Strongyloides stercoralis is a cause of abdominal pain, diarrhea and urticaria in rural Cambodia. BMC Res Notes. 2013, 6: 200-10.1186/1756-0500-6-200.CrossRefPubMedPubMedCentral Khieu V, Srey S, Schar F, Muth S, Marti H, Odermatt P: Strongyloides stercoralis is a cause of abdominal pain, diarrhea and urticaria in rural Cambodia. BMC Res Notes. 2013, 6: 200-10.1186/1756-0500-6-200.CrossRefPubMedPubMedCentral
16.
go back to reference Ardic N: [An overview of Strongyloides stercoralis and its infections]. Mikrobiyol Bul. 2009, 43 (1): 169-177.PubMed Ardic N: [An overview of Strongyloides stercoralis and its infections]. Mikrobiyol Bul. 2009, 43 (1): 169-177.PubMed
17.
go back to reference Nuesch R, Zimmerli L, Stockli R, Gyr N, Hatz CFR: Imported strongyloidosis: a longitudinal analysis of 31 cases. J Travel Med. 2005, 12: 80-84. 10.2310/7060.2005.12204.CrossRefPubMed Nuesch R, Zimmerli L, Stockli R, Gyr N, Hatz CFR: Imported strongyloidosis: a longitudinal analysis of 31 cases. J Travel Med. 2005, 12: 80-84. 10.2310/7060.2005.12204.CrossRefPubMed
18.
go back to reference Segarra-Newnham M: Manifestations, diagnosis, and treatment of Strongyloides stercoralis infection. Ann Pharmacother. 2007, 41 (12): 1992-2001. 10.1345/aph.1K302.CrossRefPubMed Segarra-Newnham M: Manifestations, diagnosis, and treatment of Strongyloides stercoralis infection. Ann Pharmacother. 2007, 41 (12): 1992-2001. 10.1345/aph.1K302.CrossRefPubMed
19.
go back to reference Schär F, Trostdorf U, Giardina F, Khieu V, Muth S, Marti H, Vounatsou P, Odermatt P: Strongyloides stercoralis: global distribution and risk factors. PLoS Negl Trop Dis. 2013, 7 (7): e2288-10.1371/journal.pntd.0002288.CrossRefPubMedPubMedCentral Schär F, Trostdorf U, Giardina F, Khieu V, Muth S, Marti H, Vounatsou P, Odermatt P: Strongyloides stercoralis: global distribution and risk factors. PLoS Negl Trop Dis. 2013, 7 (7): e2288-10.1371/journal.pntd.0002288.CrossRefPubMedPubMedCentral
20.
go back to reference Utzinger J, Raso G, Brooker S, De Savigny D, Tanner M, Ornbjerg N, Singer BH, N'Goran EK: Schistosomiasis and neglected tropical diseases: towards integrated and sustainable control and a word of caution. Parasitology. 2009, 136 (13): 1859--1874. 10.1017/S0031182009991600.CrossRefPubMedPubMedCentral Utzinger J, Raso G, Brooker S, De Savigny D, Tanner M, Ornbjerg N, Singer BH, N'Goran EK: Schistosomiasis and neglected tropical diseases: towards integrated and sustainable control and a word of caution. Parasitology. 2009, 136 (13): 1859--1874. 10.1017/S0031182009991600.CrossRefPubMedPubMedCentral
21.
go back to reference Bisoffi Z, Buonfrate D, Montresor A, Requena-Mendez A, Munoz J, Krolewiecki AJ, Gotuzzo E, Mena MA, Chiodini PL, Anselmi M, Moreira J, Albonico M: Strongyloides stercoralis: a plea for action. PLoS Negl Trop Dis. 2013, 7 (5): e2214-10.1371/journal.pntd.0002214.CrossRefPubMedPubMedCentral Bisoffi Z, Buonfrate D, Montresor A, Requena-Mendez A, Munoz J, Krolewiecki AJ, Gotuzzo E, Mena MA, Chiodini PL, Anselmi M, Moreira J, Albonico M: Strongyloides stercoralis: a plea for action. PLoS Negl Trop Dis. 2013, 7 (5): e2214-10.1371/journal.pntd.0002214.CrossRefPubMedPubMedCentral
22.
go back to reference St Georgiev V: Chemotherapy of enterobiasis (oxyuriasis). Expert Opin Pharmacother. 2001, 2 (2): 267-275. 10.1517/14656566.2.2.267.CrossRefPubMed St Georgiev V: Chemotherapy of enterobiasis (oxyuriasis). Expert Opin Pharmacother. 2001, 2 (2): 267-275. 10.1517/14656566.2.2.267.CrossRefPubMed
23.
go back to reference Arca MJ, Gates RL, Groner JI, Hammond S, Caniano DA: Clinical manifestations of appendiceal pinworms in children: an institutional experience and a review of the literature. Pediatr Surg Int. 2004, 20 (5): 372-375. 10.1007/s00383-004-1151-5.CrossRefPubMed Arca MJ, Gates RL, Groner JI, Hammond S, Caniano DA: Clinical manifestations of appendiceal pinworms in children: an institutional experience and a review of the literature. Pediatr Surg Int. 2004, 20 (5): 372-375. 10.1007/s00383-004-1151-5.CrossRefPubMed
24.
go back to reference Burkhart CN, Burkhart CG: Assessment of frequency, transmission, and genitourinary complications of enterobiasis (pinworms). Int J Dermatol. 2005, 44 (10): 837-840. 10.1111/j.1365-4632.2004.02332.x.CrossRefPubMed Burkhart CN, Burkhart CG: Assessment of frequency, transmission, and genitourinary complications of enterobiasis (pinworms). Int J Dermatol. 2005, 44 (10): 837-840. 10.1111/j.1365-4632.2004.02332.x.CrossRefPubMed
26.
go back to reference Fry GF, Moore JG: Enterobius vermicularis: 10,000-year-old human infection. Science. 1969, 166 (3913): 1620-10.1126/science.166.3913.1620.CrossRefPubMed Fry GF, Moore JG: Enterobius vermicularis: 10,000-year-old human infection. Science. 1969, 166 (3913): 1620-10.1126/science.166.3913.1620.CrossRefPubMed
28.
go back to reference Adegnika AA, Kremsner PG: Epidemiology of malaria and helminth interaction: a review from 2001 to 2011. Curr Opin HIV AIDS. 2012, 7 (3): 221-224. 10.1097/COH.0b013e3283524d90.CrossRefPubMed Adegnika AA, Kremsner PG: Epidemiology of malaria and helminth interaction: a review from 2001 to 2011. Curr Opin HIV AIDS. 2012, 7 (3): 221-224. 10.1097/COH.0b013e3283524d90.CrossRefPubMed
29.
go back to reference Rafi W, Ribeiro-Rodrigues R, Ellner JJ, Salgame P: Coinfection-helminthes and tuberculosis. Curr Opin HIV AIDS. 2012, 7 (3): 239-244. 10.1097/COH.0b013e3283524dc5.CrossRefPubMed Rafi W, Ribeiro-Rodrigues R, Ellner JJ, Salgame P: Coinfection-helminthes and tuberculosis. Curr Opin HIV AIDS. 2012, 7 (3): 239-244. 10.1097/COH.0b013e3283524dc5.CrossRefPubMed
30.
go back to reference Walson JL, Herrin BR, John-Stewart G: Deworming helminth co-infected individuals for delaying HIV disease progression. Cochrane Database Syst Rev. 2009, 3: CD006419-PubMed Walson JL, Herrin BR, John-Stewart G: Deworming helminth co-infected individuals for delaying HIV disease progression. Cochrane Database Syst Rev. 2009, 3: CD006419-PubMed
31.
go back to reference Secor WE: The effects of schistosomiasis on HIV/AIDS infection, progression and transmission. Curr Opin HIV AIDS. 2012, 7 (3): 254-259. 10.1097/COH.0b013e328351b9e3.CrossRefPubMed Secor WE: The effects of schistosomiasis on HIV/AIDS infection, progression and transmission. Curr Opin HIV AIDS. 2012, 7 (3): 254-259. 10.1097/COH.0b013e328351b9e3.CrossRefPubMed
32.
go back to reference Webb EL, Ekii AO, Pala P: Epidemiology and immunology of helminth-HIV interactions. Curr Opin HIV AIDS. 2012, 7 (3): 245-253. 10.1097/COH.0b013e32835210cd.CrossRefPubMed Webb EL, Ekii AO, Pala P: Epidemiology and immunology of helminth-HIV interactions. Curr Opin HIV AIDS. 2012, 7 (3): 245-253. 10.1097/COH.0b013e32835210cd.CrossRefPubMed
33.
go back to reference Knopp S, Becker S, Ingram K, Keiser J, Utzinger J: Diagnosis and treatment of schistosomiasis in children in the era of intensified control. Expert Rev Anti Infect Ther. 2013, 11 (11): 1237-1258. 10.1586/14787210.2013.844066.CrossRefPubMed Knopp S, Becker S, Ingram K, Keiser J, Utzinger J: Diagnosis and treatment of schistosomiasis in children in the era of intensified control. Expert Rev Anti Infect Ther. 2013, 11 (11): 1237-1258. 10.1586/14787210.2013.844066.CrossRefPubMed
34.
go back to reference Moreau E, Chauvin A: Immunity against helminths: interactions with the host and the intercurrent infections. J Biomed Biotechnol. 2010, 2010: 428593-10.1155/2010/428593.CrossRefPubMedPubMedCentral Moreau E, Chauvin A: Immunity against helminths: interactions with the host and the intercurrent infections. J Biomed Biotechnol. 2010, 2010: 428593-10.1155/2010/428593.CrossRefPubMedPubMedCentral
35.
go back to reference McSorley HJ, Hewitson JP, Maizels RM: Immunomodulation by helminth parasites: defining mechanisms and mediators. Int J Parasitol. 2013, 43 (3–4): 301-310. 10.1016/j.ijpara.2012.11.011.CrossRefPubMed McSorley HJ, Hewitson JP, Maizels RM: Immunomodulation by helminth parasites: defining mechanisms and mediators. Int J Parasitol. 2013, 43 (3–4): 301-310. 10.1016/j.ijpara.2012.11.011.CrossRefPubMed
36.
go back to reference Kinung'hi SM, Magnussen P, Kaatano GM, Kishamawe C, Vennervald BJ: Malaria and helminth co-infections in school and preschool children: a cross-sectional study in Magu district, north-western Tanzania. PLoS One. 2014, 9 (1): e86510-10.1371/journal.pone.0086510.CrossRefPubMedPubMedCentral Kinung'hi SM, Magnussen P, Kaatano GM, Kishamawe C, Vennervald BJ: Malaria and helminth co-infections in school and preschool children: a cross-sectional study in Magu district, north-western Tanzania. PLoS One. 2014, 9 (1): e86510-10.1371/journal.pone.0086510.CrossRefPubMedPubMedCentral
37.
go back to reference Salgame P, Yap GS, Gause WC: Effect of helminth-induced immunity on infections with microbial pathogens. Nat Immunol. 2013, 14 (11): 1118-1126. 10.1038/ni.2736.CrossRefPubMed Salgame P, Yap GS, Gause WC: Effect of helminth-induced immunity on infections with microbial pathogens. Nat Immunol. 2013, 14 (11): 1118-1126. 10.1038/ni.2736.CrossRefPubMed
38.
go back to reference Righetti AA, Glinz D, Adiossan LG, Koua AY, Niamke S, Hurrell RF, Wegmuller R, N'Goran EK, Utzinger J: Interactions and potential implications of Plasmodium falciparum-hookworm coinfection in different age groups in south-central Côte d'Ivoire. PLoS Negl Trop Dis. 2012, 6 (11): e1889-10.1371/journal.pntd.0001889.CrossRefPubMedPubMedCentral Righetti AA, Glinz D, Adiossan LG, Koua AY, Niamke S, Hurrell RF, Wegmuller R, N'Goran EK, Utzinger J: Interactions and potential implications of Plasmodium falciparum-hookworm coinfection in different age groups in south-central Côte d'Ivoire. PLoS Negl Trop Dis. 2012, 6 (11): e1889-10.1371/journal.pntd.0001889.CrossRefPubMedPubMedCentral
39.
go back to reference Mwangi TW, Bethony JM, Brooker S: Malaria and helminth interactions in humans: an epidemiological viewpoint. Ann Trop Med Parasitol. 2006, 100 (7): 551-570. 10.1179/136485906X118468.CrossRefPubMedPubMedCentral Mwangi TW, Bethony JM, Brooker S: Malaria and helminth interactions in humans: an epidemiological viewpoint. Ann Trop Med Parasitol. 2006, 100 (7): 551-570. 10.1179/136485906X118468.CrossRefPubMedPubMedCentral
40.
go back to reference NBS & OCGS: 2012 Population and Housing Survey of the United Republic of Tanzania. Population Distribution by Administrative Areas. 2013, United Republic of Tanzania: National Bureau of Statistics, Ministry of Finance, and Zanzibar, United Republic of Tanzania: Office of Chief Government Statistician, President’s Office, Finance, Economy and Development Planning, Dar es Salaam NBS & OCGS: 2012 Population and Housing Survey of the United Republic of Tanzania. Population Distribution by Administrative Areas. 2013, United Republic of Tanzania: National Bureau of Statistics, Ministry of Finance, and Zanzibar, United Republic of Tanzania: Office of Chief Government Statistician, President’s Office, Finance, Economy and Development Planning, Dar es Salaam
41.
go back to reference NBS & CRCO: United Republic of Tanzania Coast Region Socio-Economic Profile. 2007, United Republic of Tanzania: National Bureau of Statistics and Coast Regional Commissioner’s Office, coordinated by Ministry of Planning, Economy and Empowerment, Dar es Salaam NBS & CRCO: United Republic of Tanzania Coast Region Socio-Economic Profile. 2007, United Republic of Tanzania: National Bureau of Statistics and Coast Regional Commissioner’s Office, coordinated by Ministry of Planning, Economy and Empowerment, Dar es Salaam
42.
go back to reference Greenwood BM, Armstrong JR: Comparison of two simple methods for determining malaria parasite density. Trans R Soc Trop Med Hyg. 1991, 85 (2): 186-188. 10.1016/0035-9203(91)90015-Q.CrossRefPubMed Greenwood BM, Armstrong JR: Comparison of two simple methods for determining malaria parasite density. Trans R Soc Trop Med Hyg. 1991, 85 (2): 186-188. 10.1016/0035-9203(91)90015-Q.CrossRefPubMed
43.
go back to reference NMCP, WHO, IHI, KEMRI: An Epidemiological Profile of Malaria and its Control in Mainland Tanzania. Report Funded by Roll Back Malaria and Department for International Development-UK. 2013, United Republic of Tanzania: National Malaria Control Programme, WHO, Ifakara Health Institute, and Nairobi, Kenya: KEMRI-Wellcome Trust, Dar es Salaam NMCP, WHO, IHI, KEMRI: An Epidemiological Profile of Malaria and its Control in Mainland Tanzania. Report Funded by Roll Back Malaria and Department for International Development-UK. 2013, United Republic of Tanzania: National Malaria Control Programme, WHO, Ifakara Health Institute, and Nairobi, Kenya: KEMRI-Wellcome Trust, Dar es Salaam
44.
go back to reference García LS, Bruckner DA: Diagnostic Medical Parasitology. 2001, American Society for Microbiology, Washington DC, 4 García LS, Bruckner DA: Diagnostic Medical Parasitology. 2001, American Society for Microbiology, Washington DC, 4
45.
go back to reference Katz N, Chaves A, Pellegrino J: A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo. 1972, 14 (6): 397-400.PubMed Katz N, Chaves A, Pellegrino J: A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo. 1972, 14 (6): 397-400.PubMed
46.
go back to reference Peters PA, Mahmoud AA, Warren KS, Ouma JH, Siongok TK: Field studies of a rapid, accurate means of quantifying Schistosoma haematobium eggs in urine samples. Bull World Health Organ. 1976, 54 (2): 159-162.PubMedPubMedCentral Peters PA, Mahmoud AA, Warren KS, Ouma JH, Siongok TK: Field studies of a rapid, accurate means of quantifying Schistosoma haematobium eggs in urine samples. Bull World Health Organ. 1976, 54 (2): 159-162.PubMedPubMedCentral
47.
go back to reference Cringoli G, Rinaldi L, Maurelli MP, Utzinger J: FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc. 2010, 5: 503-515. 10.1038/nprot.2009.235.CrossRefPubMed Cringoli G, Rinaldi L, Maurelli MP, Utzinger J: FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc. 2010, 5: 503-515. 10.1038/nprot.2009.235.CrossRefPubMed
48.
go back to reference Mogeni P, Twahir H, Bandika V, Mwalekwa L, Thitiri J, Ngari M, Toromo C, Maitland K, Berkley JA: Diagnostic performance of visible severe wasting for identifying severe acute malnutrition in children admitted to hospital in Kenya. Bull World Health Organ. 2011, 89 (12): 900-906. 10.2471/BLT.11.091280.CrossRefPubMedPubMedCentral Mogeni P, Twahir H, Bandika V, Mwalekwa L, Thitiri J, Ngari M, Toromo C, Maitland K, Berkley JA: Diagnostic performance of visible severe wasting for identifying severe acute malnutrition in children admitted to hospital in Kenya. Bull World Health Organ. 2011, 89 (12): 900-906. 10.2471/BLT.11.091280.CrossRefPubMedPubMedCentral
49.
go back to reference WHO & UNICEF: WHO Child Growth Standards and the Identification of Severe Acute Malnutrition in Infants and Children. 2009, A Joint Statement by the World Health Organization and the United Nations Children’s Fund, Geneva, Switzerland WHO & UNICEF: WHO Child Growth Standards and the Identification of Severe Acute Malnutrition in Infants and Children. 2009, A Joint Statement by the World Health Organization and the United Nations Children’s Fund, Geneva, Switzerland
50.
go back to reference WHO: Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. 2011, World Health Organization, Geneva, Switzerland WHO: Haemoglobin Concentrations for the Diagnosis of Anaemia and Assessment of Severity. 2011, World Health Organization, Geneva, Switzerland
51.
go back to reference Buchanan AM, Muro FJ, Gratz J, Crump JA, Musyoka AM, Sichangi MW, Morrissey AB, M'Rimberia JK, Njau BN, Msuya LJ, Bartlett JA, Cunningham CK: Establishment of haematological and immunological reference values for healthy Tanzanian children in Kilimanjaro Region. Trop Med Int Health. 2010, 15 (9): 1011-1021.PubMedPubMedCentral Buchanan AM, Muro FJ, Gratz J, Crump JA, Musyoka AM, Sichangi MW, Morrissey AB, M'Rimberia JK, Njau BN, Msuya LJ, Bartlett JA, Cunningham CK: Establishment of haematological and immunological reference values for healthy Tanzanian children in Kilimanjaro Region. Trop Med Int Health. 2010, 15 (9): 1011-1021.PubMedPubMedCentral
52.
go back to reference Kohl KS, Marcy SM, Blum M, Connell Jones M, Dagan R, Hansen J, Nalin D, Rothstein E: Brighton Collaboration Fever Working G: fever after immunization: current concepts and improved future scientific understanding. Clin Infect Dis. 2004, 39 (3): 389-394. 10.1086/422454.CrossRefPubMed Kohl KS, Marcy SM, Blum M, Connell Jones M, Dagan R, Hansen J, Nalin D, Rothstein E: Brighton Collaboration Fever Working G: fever after immunization: current concepts and improved future scientific understanding. Clin Infect Dis. 2004, 39 (3): 389-394. 10.1086/422454.CrossRefPubMed
53.
go back to reference Montresor A, Crompton DWT, Hall A, Bundy DAP, Savioli L: Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level. 1998, World Health Organization, Geneva, Switzerland Montresor A, Crompton DWT, Hall A, Bundy DAP, Savioli L: Guidelines for the Evaluation of Soil-Transmitted Helminthiasis and Schistosomiasis at Community Level. 1998, World Health Organization, Geneva, Switzerland
54.
go back to reference Raso G, Vounatsou P, Singer BH, N'Goran EK, Tanner M, Utzinger J: An integrated approach for risk profiling and spatial prediction of Schistosoma mansoni-hookworm coinfection. Proc Natl Acad Sci U S A. 2006, 103 (18): 6934-6939. 10.1073/pnas.0601559103.CrossRefPubMedPubMedCentral Raso G, Vounatsou P, Singer BH, N'Goran EK, Tanner M, Utzinger J: An integrated approach for risk profiling and spatial prediction of Schistosoma mansoni-hookworm coinfection. Proc Natl Acad Sci U S A. 2006, 103 (18): 6934-6939. 10.1073/pnas.0601559103.CrossRefPubMedPubMedCentral
55.
go back to reference Knopp S, Mohammed KA, Stothard JR, Khamis IS, Rollinson D, Marti H, Utzinger J: Patterns and risk factors of helminthiasis and anemia in a rural and a peri-urban community in Zanzibar, in the context of helminth control programs. PLoS Negl Trop Dis. 2010, 4 (5): e681-10.1371/journal.pntd.0000681.CrossRefPubMedPubMedCentral Knopp S, Mohammed KA, Stothard JR, Khamis IS, Rollinson D, Marti H, Utzinger J: Patterns and risk factors of helminthiasis and anemia in a rural and a peri-urban community in Zanzibar, in the context of helminth control programs. PLoS Negl Trop Dis. 2010, 4 (5): e681-10.1371/journal.pntd.0000681.CrossRefPubMedPubMedCentral
56.
go back to reference Tatala SR, Kihamia CM, Kyungu LH, Svanberg U: Risk factors for anaemia in schoolchildren in Tanga Region. Tanzania Tanzan J Health Res. 2008, 10 (4): 189-202.PubMed Tatala SR, Kihamia CM, Kyungu LH, Svanberg U: Risk factors for anaemia in schoolchildren in Tanga Region. Tanzania Tanzan J Health Res. 2008, 10 (4): 189-202.PubMed
57.
go back to reference Nyhus Dhillon C, Subramaniam H, Mulokozi G, Rambeloson Z, Klemm R: Overestimation of vitamin a supplementation coverage from district tally sheets demonstrates importance of population-based surveys for program improvement: lessons from Tanzania. PLoS One. 2013, 8 (3): e58629-10.1371/journal.pone.0058629.CrossRefPubMedPubMedCentral Nyhus Dhillon C, Subramaniam H, Mulokozi G, Rambeloson Z, Klemm R: Overestimation of vitamin a supplementation coverage from district tally sheets demonstrates importance of population-based surveys for program improvement: lessons from Tanzania. PLoS One. 2013, 8 (3): e58629-10.1371/journal.pone.0058629.CrossRefPubMedPubMedCentral
58.
go back to reference Mwakitalu ME, Malecela MN, Mosha FW, Simonsen PE: Urban schistosomiasis and soil transmitted helminthiases in young school children in Dar es Salaam and Tanga, Tanzania, after a decade of anthelminthic intervention. Acta Trop. 2014, 133: 35-41. 10.1016/j.actatropica.2014.01.012.CrossRefPubMed Mwakitalu ME, Malecela MN, Mosha FW, Simonsen PE: Urban schistosomiasis and soil transmitted helminthiases in young school children in Dar es Salaam and Tanga, Tanzania, after a decade of anthelminthic intervention. Acta Trop. 2014, 133: 35-41. 10.1016/j.actatropica.2014.01.012.CrossRefPubMed
59.
go back to reference Gryseels B: Schistosomiasis. Infect Dis Clin North Am. 2012, 26 (2): 383-397. 10.1016/j.idc.2012.03.004.CrossRefPubMed Gryseels B: Schistosomiasis. Infect Dis Clin North Am. 2012, 26 (2): 383-397. 10.1016/j.idc.2012.03.004.CrossRefPubMed
60.
go back to reference Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, 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 (11): e331-10.1371/journal.pntd.0000331.CrossRefPubMedPubMedCentral Knopp S, Mgeni AF, Khamis IS, Steinmann P, Stothard JR, 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 (11): e331-10.1371/journal.pntd.0000331.CrossRefPubMedPubMedCentral
61.
go back to reference Jeandron A, Abdyldaieva G, Usubalieva J, Ensink JH, Cox J, Matthys B, Rinaldi L, Cringoli G, Utzinger J: Accuracy of the Kato-Katz, adhesive tape and FLOTAC techniques for helminth diagnosis among children in Kyrgyzstan. Acta Trop. 2010, 116 (3): 185-192. 10.1016/j.actatropica.2010.08.010.CrossRefPubMed Jeandron A, Abdyldaieva G, Usubalieva J, Ensink JH, Cox J, Matthys B, Rinaldi L, Cringoli G, Utzinger J: Accuracy of the Kato-Katz, adhesive tape and FLOTAC techniques for helminth diagnosis among children in Kyrgyzstan. Acta Trop. 2010, 116 (3): 185-192. 10.1016/j.actatropica.2010.08.010.CrossRefPubMed
62.
go back to reference Hillier SD, Booth M, Muhangi L, Nkurunziza P, Khihembo M, Kakande M, Sewankambo M, Kizindo R, Kizza M, Muwanga M, Elliott AM: Plasmodium falciparum and helminth coinfection in a semi urban population of pregnant women in Uganda. J Infect Dis. 2008, 198 (6): 920-927. 10.1086/591183.CrossRefPubMedPubMedCentral Hillier SD, Booth M, Muhangi L, Nkurunziza P, Khihembo M, Kakande M, Sewankambo M, Kizindo R, Kizza M, Muwanga M, Elliott AM: Plasmodium falciparum and helminth coinfection in a semi urban population of pregnant women in Uganda. J Infect Dis. 2008, 198 (6): 920-927. 10.1086/591183.CrossRefPubMedPubMedCentral
63.
go back to reference Stothard JR, Pleasant J, Oguttu D, Adriko M, Galimaka R, Ruggiana A, Kazibwe F, Kabatereine NB: Strongyloides stercoralis: a field-based survey of mothers and their preschool children using ELISA, Baermann and Koga plate methods reveals low endemicity in western Uganda. J Helminthol. 2008, 82 (3): 263-269. 10.1017/S0022149X08971996.CrossRefPubMed Stothard JR, Pleasant J, Oguttu D, Adriko M, Galimaka R, Ruggiana A, Kazibwe F, Kabatereine NB: Strongyloides stercoralis: a field-based survey of mothers and their preschool children using ELISA, Baermann and Koga plate methods reveals low endemicity in western Uganda. J Helminthol. 2008, 82 (3): 263-269. 10.1017/S0022149X08971996.CrossRefPubMed
64.
go back to reference Joyce T, McGuigan KG, Elmore-Meegan M, Conroy RM: Prevalence of enteropathogens in stools of rural Maasai children under five years of age in the Maasailand region of the Kenyan Rift Valley. East Afr Med J. 1996, 73 (1): 59-62.PubMed Joyce T, McGuigan KG, Elmore-Meegan M, Conroy RM: Prevalence of enteropathogens in stools of rural Maasai children under five years of age in the Maasailand region of the Kenyan Rift Valley. East Afr Med J. 1996, 73 (1): 59-62.PubMed
65.
go back to reference Tanner M, Burnier E, Mayombana C, Betschart B, de Savigny D, Marti HP, Suter R, Aellen M, Lüdin E, Degrémont AA: Longitudinal study on the health status of children in a rural Tanzanian community: parasitoses and nutrition following control measures against intestinal parasites. Acta Trop. 1987, 44 (2): 137-174.PubMed Tanner M, Burnier E, Mayombana C, Betschart B, de Savigny D, Marti HP, Suter R, Aellen M, Lüdin E, Degrémont AA: Longitudinal study on the health status of children in a rural Tanzanian community: parasitoses and nutrition following control measures against intestinal parasites. Acta Trop. 1987, 44 (2): 137-174.PubMed
66.
go back to reference Keiser J, Utzinger J: Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA. 2008, 299 (16): 1937-1948. 10.1001/jama.299.16.1937.CrossRefPubMed Keiser J, Utzinger J: Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA. 2008, 299 (16): 1937-1948. 10.1001/jama.299.16.1937.CrossRefPubMed
67.
go back to reference Mazigo HD, Kidenya BR, Ambrose EE, Zinga M, Waihenya R: Association of intestinal helminths and P. falciparum infections in co-infected school children in northwest Tanzania. Tanzan J Health Res. 2010, 12 (4): 283-285.CrossRef Mazigo HD, Kidenya BR, Ambrose EE, Zinga M, Waihenya R: Association of intestinal helminths and P. falciparum infections in co-infected school children in northwest Tanzania. Tanzan J Health Res. 2010, 12 (4): 283-285.CrossRef
68.
go back to reference Shapiro AE, Tukahebwa EM, Kasten J, Clarke SE, Magnussen P, Olsen A, Kabatereine NB, Ndyomugyenyi R, Brooker S: Epidemiology of helminth infections and their relationship to clinical malaria in southwest Uganda. Trans R Soc Trop Med Hyg. 2005, 99 (1): 18-24. 10.1016/j.trstmh.2004.02.006.CrossRefPubMed Shapiro AE, Tukahebwa EM, Kasten J, Clarke SE, Magnussen P, Olsen A, Kabatereine NB, Ndyomugyenyi R, Brooker S: Epidemiology of helminth infections and their relationship to clinical malaria in southwest Uganda. Trans R Soc Trop Med Hyg. 2005, 99 (1): 18-24. 10.1016/j.trstmh.2004.02.006.CrossRefPubMed
69.
go back to reference Boel M, Carrara VI, Rijken M, Proux S, Nacher M, Pimanpanarak M, Paw MK, Moo O, Gay H, Bailey W, Singhasivanon P, White NJ, Nosten F, McGready R: Complex interactions between soil-transmitted helminths and malaria in pregnant women on the Thai-Burmese border. PLoS Negl Trop Dis. 2010, 4 (11): e887-10.1371/journal.pntd.0000887.CrossRefPubMedPubMedCentral Boel M, Carrara VI, Rijken M, Proux S, Nacher M, Pimanpanarak M, Paw MK, Moo O, Gay H, Bailey W, Singhasivanon P, White NJ, Nosten F, McGready R: Complex interactions between soil-transmitted helminths and malaria in pregnant women on the Thai-Burmese border. PLoS Negl Trop Dis. 2010, 4 (11): e887-10.1371/journal.pntd.0000887.CrossRefPubMedPubMedCentral
70.
go back to reference Tanner M, Lukmanji Z: Food consumption patterns in a rural Tanzanian community (Kikwawila village, Kilombero District, Morogoro Region) during lean and post-harvest season. Acta Trop. 1987, 44 (2): 229-244.PubMed Tanner M, Lukmanji Z: Food consumption patterns in a rural Tanzanian community (Kikwawila village, Kilombero District, Morogoro Region) during lean and post-harvest season. Acta Trop. 1987, 44 (2): 229-244.PubMed
71.
go back to reference Tanner M, de Savigny D: Monitoring of community health status: experience from a case study in Tanzania. Acta Trop. 1987, 44 (2): 261-270.PubMed Tanner M, de Savigny D: Monitoring of community health status: experience from a case study in Tanzania. Acta Trop. 1987, 44 (2): 261-270.PubMed
72.
go back to reference MUCHALI: Comprehensive Food Security and Nutrition Assessment Report of the April, 2012 Main (Masika) Season. 2012, United Republic of Tanzania: Report coordinated by the Disaster Management Department - Prime Minister’s Office and The National Food Security Division - Ministry of Agriculture Food Security and Co-operatives and prepared by the Tanzania Food Security and Nutrition Analysis System - MUCHALI, Dar es Salaam MUCHALI: Comprehensive Food Security and Nutrition Assessment Report of the April, 2012 Main (Masika) Season. 2012, United Republic of Tanzania: Report coordinated by the Disaster Management Department - Prime Minister’s Office and The National Food Security Division - Ministry of Agriculture Food Security and Co-operatives and prepared by the Tanzania Food Security and Nutrition Analysis System - MUCHALI, Dar es Salaam
73.
go back to reference Gyorkos TW, Maheu-Giroux M, Casapia M, Joseph SA, Creed-Kanashiro H: Stunting and helminth infection in early preschool-age children in a resource-poor community in the Amazon lowlands of Peru. Trans R Soc Trop Med Hyg. 2011, 105 (4): 204-208. 10.1016/j.trstmh.2010.12.003.CrossRefPubMed Gyorkos TW, Maheu-Giroux M, Casapia M, Joseph SA, Creed-Kanashiro H: Stunting and helminth infection in early preschool-age children in a resource-poor community in the Amazon lowlands of Peru. Trans R Soc Trop Med Hyg. 2011, 105 (4): 204-208. 10.1016/j.trstmh.2010.12.003.CrossRefPubMed
74.
go back to reference Sanchez AL, Gabrie JA, Usuanlele MT, Rueda MM, Canales M, Gyorkos TW: Soil-transmitted helminth infections and nutritional status in school-age children from rural communities in Honduras. PLoS Negl Trop Dis. 2013, 7 (8): e2378-10.1371/journal.pntd.0002378.CrossRefPubMedPubMedCentral Sanchez AL, Gabrie JA, Usuanlele MT, Rueda MM, Canales M, Gyorkos TW: Soil-transmitted helminth infections and nutritional status in school-age children from rural communities in Honduras. PLoS Negl Trop Dis. 2013, 7 (8): e2378-10.1371/journal.pntd.0002378.CrossRefPubMedPubMedCentral
75.
go back to reference Shang Y, Tang LH, Zhou SS, Chen YD, Yang YC, Lin SX: Stunting and soil-transmitted-helminth infections among school-age pupils in rural areas of southern China. Parasit Vectors. 2010, 3: 97-10.1186/1756-3305-3-97.CrossRefPubMedPubMedCentral Shang Y, Tang LH, Zhou SS, Chen YD, Yang YC, Lin SX: Stunting and soil-transmitted-helminth infections among school-age pupils in rural areas of southern China. Parasit Vectors. 2010, 3: 97-10.1186/1756-3305-3-97.CrossRefPubMedPubMedCentral
76.
go back to reference Kurtzhals JA, Addae MM, Akanmori BD, Dunyo S, Koram KA, Appawu MA, Nkrumah FK, Hviid L: Anaemia caused by asymptomatic Plasmodium falciparum infection in semi-immune African schoolchildren. Trans R Soc Trop Med Hyg. 1999, 93 (6): 623-627. 10.1016/S0035-9203(99)90073-1.CrossRefPubMed Kurtzhals JA, Addae MM, Akanmori BD, Dunyo S, Koram KA, Appawu MA, Nkrumah FK, Hviid L: Anaemia caused by asymptomatic Plasmodium falciparum infection in semi-immune African schoolchildren. Trans R Soc Trop Med Hyg. 1999, 93 (6): 623-627. 10.1016/S0035-9203(99)90073-1.CrossRefPubMed
77.
go back to reference Smith JL, Brooker S: Impact of hookworm infection and deworming on anaemia in non-pregnant populations: a systematic review. Trop Med Int Health. 2010, 15 (7): 776-795. 10.1111/j.1365-3156.2010.02542.x.CrossRefPubMedPubMedCentral Smith JL, Brooker S: Impact of hookworm infection and deworming on anaemia in non-pregnant populations: a systematic review. Trop Med Int Health. 2010, 15 (7): 776-795. 10.1111/j.1365-3156.2010.02542.x.CrossRefPubMedPubMedCentral
78.
go back to reference Brooker S, Hotez PJ, Bundy DAP: Hookworm-related anaemia among pregnant women: a systematic review. PLoS Negl Trop Dis. 2008, 2 (9): e291-10.1371/journal.pntd.0000291.CrossRefPubMedPubMedCentral Brooker S, Hotez PJ, Bundy DAP: Hookworm-related anaemia among pregnant women: a systematic review. PLoS Negl Trop Dis. 2008, 2 (9): e291-10.1371/journal.pntd.0000291.CrossRefPubMedPubMedCentral
79.
go back to reference Dreyfuss ML, Stoltzfus RJ, Shrestha JB, Pradhan EK, LeClerq SC, Khatry SK, Shrestha SR, Katz J, Albonico M, West KP: Hookworms, malaria and vitamin A deficiency contribute to anemia and iron deficiency among pregnant women in the plains of Nepal. J Nutr. 2000, 130 (10): 2527-2536.PubMed Dreyfuss ML, Stoltzfus RJ, Shrestha JB, Pradhan EK, LeClerq SC, Khatry SK, Shrestha SR, Katz J, Albonico M, West KP: Hookworms, malaria and vitamin A deficiency contribute to anemia and iron deficiency among pregnant women in the plains of Nepal. J Nutr. 2000, 130 (10): 2527-2536.PubMed
80.
go back to reference Stoltzfus RJ, Chwaya HM, Montresor A, Albonico M, Savioli L, Tielsch JM: Malaria, hookworms and recent fever are related to anemia and iron status indicators in 0- to 5-y old Zanzibari children and these relationships change with age. J Nutr. 2000, 130 (7): 1724-1733.PubMed Stoltzfus RJ, Chwaya HM, Montresor A, Albonico M, Savioli L, Tielsch JM: Malaria, hookworms and recent fever are related to anemia and iron status indicators in 0- to 5-y old Zanzibari children and these relationships change with age. J Nutr. 2000, 130 (7): 1724-1733.PubMed
81.
go back to reference Antonelli LR, Leoratti FM, Costa PA, Rocha BC, Diniz SQ, Tada MS, Pereira DB, Teixeira-Carvalho A, Golenbock DT, Goncalves R, Gazzinelli RT: The CD14 + CD16+ inflammatory monocyte subset displays increased mitochondrial activity and effector function during acute Plasmodium vivax malaria. PLoS Pathog. 2014, 10 (9): e1004393-10.1371/journal.ppat.1004393.CrossRefPubMedPubMedCentral Antonelli LR, Leoratti FM, Costa PA, Rocha BC, Diniz SQ, Tada MS, Pereira DB, Teixeira-Carvalho A, Golenbock DT, Goncalves R, Gazzinelli RT: The CD14 + CD16+ inflammatory monocyte subset displays increased mitochondrial activity and effector function during acute Plasmodium vivax malaria. PLoS Pathog. 2014, 10 (9): e1004393-10.1371/journal.ppat.1004393.CrossRefPubMedPubMedCentral
82.
go back to reference Halim NKD, Ajayi OI, Oluwafemi F: Monocytosis in acute malaria infection. Niger J Clin Pract. 2002, 5 (2): 106-108. Halim NKD, Ajayi OI, Oluwafemi F: Monocytosis in acute malaria infection. Niger J Clin Pract. 2002, 5 (2): 106-108.
83.
go back to reference Schulte C, Krebs B, Jelinek T, Nothdurft HD, von Sonnenburg F, Loscher T: Diagnostic significance of blood eosinophilia in returning travelers. Clin Infect Dis. 2002, 34 (3): 407-411. 10.1086/338026.CrossRefPubMed Schulte C, Krebs B, Jelinek T, Nothdurft HD, von Sonnenburg F, Loscher T: Diagnostic significance of blood eosinophilia in returning travelers. Clin Infect Dis. 2002, 34 (3): 407-411. 10.1086/338026.CrossRefPubMed
84.
go back to reference Mitre E, Nutman TB: Lack of basophilia in human parasitic infections. Am J Trop Med Hyg. 2003, 69 (1): 87-91.PubMed Mitre E, Nutman TB: Lack of basophilia in human parasitic infections. Am J Trop Med Hyg. 2003, 69 (1): 87-91.PubMed
85.
go back to reference Lugada ES, Mermin J, Kaharuza F, Ulvestad E, Were W, Langeland N, Asjo B, Malamba S, Downing R: Population-based hematologic and immunologic reference values for a healthy Ugandan population. Clin Diagn Lab Immunol. 2004, 11 (1): 29-34.PubMedPubMedCentral Lugada ES, Mermin J, Kaharuza F, Ulvestad E, Were W, Langeland N, Asjo B, Malamba S, Downing R: Population-based hematologic and immunologic reference values for a healthy Ugandan population. Clin Diagn Lab Immunol. 2004, 11 (1): 29-34.PubMedPubMedCentral
Metadata
Title
Enterobiasis and strongyloidiasis and associated co-infections and morbidity markers in infants, preschool- and school-aged children from rural coastal Tanzania: a cross-sectional study
Authors
Nahya Salim
Tobias Schindler
Ummi Abdul
Julian Rothen
Blaise Genton
Omar Lweno
Alisa S Mohammed
John Masimba
Denis Kwaba
Salim Abdulla
Marcel Tanner
Claudia Daubenberger
Stefanie Knopp
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2014
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-014-0644-7

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