Schistosoma haematobium infection is associated with alterations in energy and purine-related metabolism in preschool-aged children
Open accessAbstract
Helminths are parasitic worms that infect over a billion people worldwide. The pathological consequences from infection are due in part, to parasite-induced changes in host metabolic pathways. Here, we analyse the changes in host metabolic profiles, in response to the first Schistosoma haematobium infection and treatment in Zimbabwean children. A cohort of 83 schistosome-negative children (2-5 years old) as determined by parasitological examination, guardian interviews and examination of medical records, was recruited at baseline. Children were followed up after three months for parasitological diagnosis of their first S. haematobium infection, by detection of parasite eggs excreted in urine. Children positive for infection were treated with the antihelminthic drug praziquantel, and treatment efficacy checked three months after treatment. Blood samples were taken at each time point, and capillary electrophoresis mass spectrometry in conjunction with multivariate analysis were used to compare the change in serum metabolite profiles in schistosome-infected versus uninfected children. Following baseline at the three-month follow up, 11 children had become infected with S. haematobium (incidence = 13.3%). Our results showed that infection with S. haematobium was associated with significant increases (>2-fold) in discriminatory metabolites, linked primarily with energy (G6P, 3-PG, AMP, ADP) and purine (AMP, ADP) metabolism. These observed changes were commensurate with schistosome infection intensity, and levels of the affected metabolites were reduced following treatment, albeit not significantly. This study demonstrates that early infection with S. haematobium is associated with alterations in host energy and purine metabolism. Taken together, these changes are consistent with parasite-related clinical manifestations of malnutrition, poor growth and poor physical and cognitive performance observed in schistosome-infected children.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Early childhood infections with schistosomes affect metabolism in children aged 5 years and below.
“We have recently reported that early childhood infections with schistosomes affect metabolism in children aged 5 years and below, [39]”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
PLS-regression: a basic tool of chemometrics
Wold, S., Sjöström, M., & Eriksson, L. (2001) · Chemometrics and Intelligent Laboratory Systems · doi:10.1016/s0169-7439(01)00155-1 · Cited by 10,084 · see citing works
AMPK: a nutrient and energy sensor that maintains energy homeostasis
Hardie, D. G., Ross, F. A., & Hawley, S. A. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3311 · Cited by 4,602 · see citing works
MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis
Chong, J., Soufan, O., Li, C., Caraus, I., Li, S., Bourque, G., Wishart, D. S., & Xia, J. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky310 · Cited by 3,577 · see citing works
van den Berg, R. A., Hoefsloot, H. C., Westerhuis, J. A., Smilde, A. K., & van der Werf, M. J. (2006) · BMC Genomics · doi:10.1186/1471-2164-7-142 · Cited by 2,450 · see citing works
A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni.
Katz, N., Chaves, A. C., & Pellegrino, J. (1973) · PubMed · Cited by 2,414 · see citing works
MetaboAnalyst: a web server for metabolomic data analysis and interpretation
Xia, J., Psychogios, N., Young, N., & Wishart, D. S. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp356 · Cited by 2,238 · see citing works
Steinmann, P., Keiser, J., Bos, R., Tanner, M., & Utzinger, J. (2006) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(06)70521-7 · Cited by 2,146 · see citing works
Nrf2 Redirects Glucose and Glutamine into Anabolic Pathways in Metabolic Reprogramming
Mitsuishi, Y., Taguchi, K., Kawatani, Y., Shibata, T., Nukiwa, T., Aburatani, H., Yamamoto, M., & Motohashi, H. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.05.016 · Cited by 1,395 · cited 1× · see citing works
“Sample preparation and metabolite analysis was carried out by HMT using the capillary electrophoresis time-of-flight mass spectrometry (CE–TOF–MS)-based metabolomics technique [53,54].”
MethodA simple, device for quantita tive stool thick-smear technique in schistosomiasis mansoni
Katz, N., Chaves, A., & Pellegrino, J. (1972) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) · Cited by 1,338 · see citing works
Xia, J., & Wishart, D. S. (2011) · Nature Protocols · doi:10.1038/nprot.2011.319 · Cited by 1,332 · see citing works
Prevention and control of schistosomiasis and soil-transmitted helminthiasis.
(2002) · PubMed · Cited by 1,315 · see citing works
Wiklund, S., Johansson, E., Sjöström, L., Mellerowicz, E. J., Edlund, U. G., Shockcor, J. P., Gottfries, J., Möritz, T., & Trygg, J. (2007) · Analytical Chemistry · doi:10.1021/ac0713510 · Cited by 1,234 · see citing works
McManus, D. P., Dunne, D. W., Sacko, M., Utzinger, J., Vennervald, B. J., & Zhou, X. (2018) · Nature Reviews Disease Primers · doi:10.1038/s41572-018-0013-8 · Cited by 1,202 · see citing works
Soil-transmitted helminth infections: updating the global picture
de Silva, N. R., Brooker, S. J., Hotez, P. J., Montresor, A., Engels, D., & Savioli, L. (2003) · Trends in Parasitology · doi:10.1016/j.pt.2003.10.002 · Cited by 1,162 · see citing works
The immunobiology of schistosomiasis
Pearce, E. J., & MacDonald, A. S. (2002) · Nature reviews. Immunology · doi:10.1038/nri843 · Cited by 1,151 · see citing works
Orthogonal signal correction of near-infrared spectra
Wold, S., Antti, H., Lindgren, F., & Öhman, J. (1998) · Chemometrics and Intelligent Laboratory Systems · doi:10.1016/s0169-7439(98)00109-9 · Cited by 1,090 · see citing works
Hotez, P. J., Alvarado, M., Basáñez, M.-G., Bolliger, I. W., Bourne, R., Boussinesq, M., Brooker, S. J., Brown, A. S., Buckle, G. C., Budke, C. M., et al. (2014) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0002865 · Cited by 1,089 · see citing works
Bours, M. J. L., Swennen, E. L. R., Di Virgilio, F., Cronstein, B. N., & Dagnelie, P. C. (2006) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2005.04.013 · Cited by 1,030 · see citing works
Quantitative Metabolome Analysis Using Capillary Electrophoresis Mass Spectrometry
Soga, T., Ohashi, Y., Ueno, Y., Naraoka, H., Tomita, M., & Nishioka, T. (2003) · Journal of Proteome Research · doi:10.1021/pr034020m · Cited by 975 · see citing works
Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa
van der Werf, M. J., de Vlas, S. J., BROOKER, S. J., Looman, C. W. N., Nagelkerke, N. J. D., Habbema, J. D. F., & Engels, D. (2003) · Acta Tropica · doi:10.1016/s0001-706x(03)00029-9 · Cited by 951 · see citing works
Double-check: validation of diagnostic statistics for PLS-DA models in metabolomics studies
Szymańska, E., Saccenti, E., Smilde, A. K., & Westerhuis, J. A. (2011) · Metabolomics · doi:10.1007/s11306-011-0330-3 · Cited by 913 · see citing works
Adenosine: an endogenous regulator of innate immunity
Haskó, G. (2003) · Trends in Immunology · doi:10.1016/j.it.2003.11.003 · Cited by 900 · see citing works
A Novel Host-Parasite Lipid Cross-talk
van der Kleij, D., Latz, E., Brouwers, J. F. H. M., Kruize, Y. C. M., Schmitz, M., Kurt-Jones, E. A., Espevik, T., de Jong, E. C., Kapsenberg, M. L., Golenbock, D. T., et al. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m206941200 · Cited by 587 · see citing works
Amino Acid Analysis by Capillary Electrophoresis Electrospray Ionization Mass Spectrometry
Soga, T., & Heiger, D. N. (2000) · Analytical Chemistry · doi:10.1021/ac990976y · Cited by 520 · see citing works
Immune Regulation of Metabolic Homeostasis in Health and Disease
Brestoff, J. R., & Artis, D. (2015) · Cell · doi:10.1016/j.cell.2015.02.022 · Cited by 498 · see citing works
Patterson, T. A., Lobenhofer, E. K., Fulmer-Smentek, S., Collins, P. J., Chu, T., Bao, W., Fang, H., Kawasaki, E. S., Hager, J., Tikhonova, I. R., et al. (2006) · Nature Biotechnology · doi:10.1038/nbt1242 · Cited by 489 · see citing works
Soga, T., Ueno, Y., Naraoka, H., Ohashi, Y., Tomita, M., & Nishioka, T. (2002) · Analytical Chemistry · doi:10.1021/ac020064n · Cited by 473 · see citing works
Regulation of the pentose phosphate cycle
Eggleston, L. V., & Krebs, H. A. (1974) · Biochemical Journal · doi:10.1042/bj1380425 · Cited by 445 · see citing works
Amiri, P., Locksley, R. M., Parslow, T. G., Sadickt, M., Rector, E., Ritter, D. M., & McKerrow, J. H. (1992) · Nature · doi:10.1038/356604a0 · Cited by 419 · see citing works
Chronic helminth infections induce immunomodulation: Consequences and mechanisms
van Riet, E., Hartgers, F. C., & Yazdanbakhsh, M. (2007) · Immunobiology · doi:10.1016/j.imbio.2007.03.009 · Cited by 393 · see citing works
AMP-activated protein kinase: new regulation, new roles?
Carling, D., Thornton, C., Woods, A., & Sanders, M. J. (2012) · Biochemical Journal · doi:10.1042/bj20120546 · Cited by 375 · see citing works
Wheelock, Å. M., & Wheelock, C. E. (2013) · Molecular BioSystems · doi:10.1039/c3mb70194h · Cited by 338 · see citing works
Zaccone, P., Fehervari, Z. T., Jones, F. M., Sidobre, S., Kronenberg, M., Dunne, D. W., & Cooke, A. (2003) · European Journal of Immunology · doi:10.1002/eji.200323910 · Cited by 317 · see citing works
Depiction of metabolome changes in histidine-starved Escherichia coli by CE-TOFMS
Ohashi, Y., Hirayama, A., Ishikawa, T., Nakamura, S., Shimizu, K., Ueno, Y., Tomita, M., & Soga, T. (2007) · Molecular BioSystems · doi:10.1039/b714176a · Cited by 291 · see citing works
Immunology of human schistosomiasis
Colley, D. G., & Secor, W. E. (2013) · Parasite Immunology · doi:10.1111/pim.12087 · Cited by 289 · see citing works
CARBOHYDRATE METABOLISM OF SCHISTOSOMA MANSONI
Bueding, E. (1950) · The Journal of General Physiology · doi:10.1085/jgp.33.5.475 · Cited by 282 · see citing works
Effects of pre-analytical processes on blood samples used in metabolomics studies
Yin, P., Lehmann, R., & Xu, G. (2015) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-015-8565-x · Cited by 278 · see citing works
Mondal, D., Minak, J., Alam, M., Liu, Y., Dai, J., Korpe, P. S., Liu, L., Haque, R., & Petri, W. A. (2011) · Clinical Infectious Diseases · doi:10.1093/cid/cir807 · Cited by 277 · see citing works
Wang, Y., Holmes, E. C., Nicholson, J. K., Cloarec, O., Chollet, J., Tanner, M., Singer, B. H., & Utzinger, J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404878101 · Cited by 272 · see citing works
Komiya, S., Mitsuzono, R., & Ube, M. (1995) · 体力科學 · doi:10.7600/jspfsm1949.44.211 · Cited by 256 · see citing works
Meyer, F., Meyer, H., & Bueding, E. (1970) · Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism · doi:10.1016/0005-2760(70)90170-0 · Cited by 214 · see citing works
Rollinson, D. (2009) · Parasitology · doi:10.1017/s0031182009990552 · Cited by 140 · see citing works
Modulation of Blood Fluke Development in the Liver by Hepatic CD4 + Lymphocytes
Davies, S. J. A., Grogan, J. L., Blank, R. B., Lim, K. C., Locksley, R. M., & McKerrow, J. H. (2001) · Science · doi:10.1126/science.1064462 · Cited by 137 · see citing works
When Too Much ATP Is Bad for Protein Synthesis
Pontes, M. H., Sevostyanova, A., & Groisman, E. A. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.06.021 · Cited by 134 · see citing works
Chen, Y., Lu, J., Huang, Y., Wang, T., Xu, Y., Xu, M., Li, M., Wang, W., Li, D., Bi, Y., et al. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2517 · Cited by 122 · see citing works
Midzi, N., Mduluza, T., Chimbari, M. J., Tshuma, C., Charimari, L., Mhlanga, G., Manangazira, P., Munyati, S. M., Phiri, I., Mutambu, S. L., et al. (2014) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0003014 · Cited by 102 · see citing works
Recent progress in integrated neglected tropical disease control
Hotez, P. J., Raff, S., Fenwick, A., Richards, F., & Molyneux, D. H. (2007) · Trends in Parasitology · doi:10.1016/j.pt.2007.08.015 · Cited by 99 · see citing works
Kim, K., Minnar, C. M., Taylor, S. L., Hitchcock, S., Zhang, C., Wettersten, H. I., Jones, A. D., Chapman, A. B., & Weiss, R. H. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086223 · Cited by 92 · see citing works
RELATION BETWEEN CARCINOMA OF THE BLADDER AND INFESTATION WITH SCHISTOSOMA HqMATOBIUM
Gelfand, M. (1967) · The Lancet · doi:10.1016/s0140-6736(67)92714-6 · Cited by 87 · see citing works
Adenosine and lymphocyte regulation
Gessi, S., Varani, K., Merighi, S., Fogli, E., Sacchetto, V., Benini, A., Leung, E., MacLennan, S., & Borea, P. A. (2007) · Purinergic Signalling · doi:10.1007/s11302-006-9042-y · Cited by 86 · see citing works
Mott, K. E., Baltes, R., Bambagha, J., & Baldassini, B. (1982) · PubMed · Cited by 84 · see citing works
The incorporation, modification and turnover of fatty acids in adult Schistosoma mansoni
Brouwers, J. F. H. M., Smeenk, I. M. B., GOLDE, L. M. G. V., & Tielens, A. G. M. (1997) · Molecular and Biochemical Parasitology · doi:10.1016/s0166-6851(97)00091-1 · Cited by 80 · see citing works
The significance of proteinuria and haematuria in Schistosoma haematobium infection
Wilkins, H. A., Goll, P. H., Marshall, T., & Moore, P. J. (1979) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(79)90134-2 · Cited by 80 · see citing works
Hormones and Nuclear Receptors in Schistosome Development
de Mendonça, R. L., Escrivá, H., Bouton, D., Laudet, V., & Pierce, R. J. (2000) · Parasitology Today · doi:10.1016/s0169-4758(00)01641-0 · Cited by 76 · see citing works
Metabolic Changes Reveal the Development of Schistosomiasis in Mice
Wu, J., Xu, W., Ming, Z., Dong, H., Tang, H., & Wang, Y. (2010) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0000807 · Cited by 75 · see citing works
Schistosomiasis in the first 1000 days
Freer, J., Bourke, C. D., Durhuus, G. H., Kjetland, E. F., & Prendergast, A. J. (2017) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(17)30490-5 · Cited by 73 · see citing works
Cesari, I. M., Simpson, A. J. G., & Evans, W. H. (1981) · Biochemical Journal · doi:10.1042/bj1980467 · Cited by 70 · see citing works
Li, J. V., Holmes, E. C., Saric, J., Keiser, J., Dirnhofer, S., Utzinger, J., & Wang, Y. (2008) · International Journal for Parasitology · doi:10.1016/j.ijpara.2008.10.010 · Cited by 65 · see citing works
Metabonomic investigation of human Schistosoma mansoni infection
Balog, C. I. A., Meissner, A., Göraler, S., Bladergroen, M. R., Vennervald, B. J., Mayboroda, O. A., & Deelder, A. M. (2011) · Molecular BioSystems · doi:10.1039/c0mb00262c · Cited by 64 · see citing works
Characterization of Schistosome Tegumental Alkaline Phosphatase (SmAP)
Bhardwaj, R., & Skelly, P. J. (2011) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0001011 · Cited by 62 · see citing works
Davies, S. J. A., Lim, K. C., Blank, R. B., Kim, J.-H., Lucas, K. D., Hernandez, D. C., Sedgwick, J. D., & McKerrow, J. H. (2003) · International Journal for Parasitology · doi:10.1016/j.ijpara.2003.10.010 · Cited by 61 · see citing works
Effects of Schistosoma mansoni worms and eggs on circulating cholesterol and liver lipids in mice
Stanley, R. G., Jackson, C. L., Griffiths, K., & Doenhoff, M. J. (2009) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2009.04.037 · Cited by 59 · see citing works
The Schistosoma mansoni lipidome: Leads for immunomodulation
Giera, M. A., Kaisar, M. M. M., Derks, R. J. E., Steenvoorden, E., Kruize, Y. C. M., Hokke, C. H., Yazdanbakhsh, M., & Everts, B. (2017) · Analytica Chimica Acta · doi:10.1016/j.aca.2017.11.058 · Cited by 58 · see citing works
Aerobic and Anaerobic Carbohydrate Metabolism and Egg Production of Schistosoma mansoni In vitro
Schiller, E. L., Bueding, E., Turner, V. M., & Fisher, J. (1975) · Journal of Parasitology · doi:10.2307/3279308 · Cited by 57 · see citing works
Purine and Pyrimidine Transport in Schistosoma mansoni
Levy, M. G., & Read, C. P. (1975) · Journal of Parasitology · doi:10.2307/3279455 · Cited by 56 · see citing works
Protein metabolism in women and men: Similarities and disparities
Markofski, M. M., & Volpi, E. (2011) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/mco.0b013e3283412343 · Cited by 54 · see citing works
Metabolic Requirements of Schistosomes
Bueding, E., & Fisher, J. (1982) · Journal of Parasitology · doi:10.2307/3281177 · Cited by 54 · see citing works
Exposure, infection and immune responses to Schistosoma haematobium in young children
Woolhouse, M. E. J., Mutapi, F., Ndhlovu, P. D., Chandiwana, S. K., & Hagan, P. (2000) · Parasitology · doi:10.1017/s0031182099005156 · Cited by 50 · see citing works
You, H., Gobert, G. N., Cai, P., Mou, R., Nawaratna, S. S. K., Fang, G., Villinger, F. J., & McManus, D. P. (2015) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0003730 · Cited by 48 · see citing works
Immune Regulation of Metabolic Homeostasis by Helminths and Their Molecules
van der Zande, H. J. P., Zawistowska‐Deniziak, A., & Guigas, B. (2019) · Trends in Parasitology · doi:10.1016/j.pt.2019.07.014 · Cited by 48 · see citing works
García‐Pérez, I., Whitfield, P. J., Bartlett, A., Angulo, S., Legido‐Quigley, C., Hanna‐Brown, M., & Barbas, C. (2008) · Electrophoresis · doi:10.1002/elps.200800031 · Cited by 47 · see citing works
Gurarie, D., Wang, X., Bustinduy, A. L., & King, C. H. (2011) · The American Society of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2011.10-0642 · Cited by 43 · see citing works
Osakunor, D. N. M., Mduluza, T., Midzi, N., Chase-Topping, M. E., Mutsaka‐Makuvaza, M. J., Chimponda, T. N., Eyoh, E., Mduluza-Jokonya, T. L., Pfavayi, L. T., Wami, W. M., et al. (2018) · BMJ Global Health · doi:10.1136/bmjgh-2017-000661 · Cited by 41 · see citing works
Self-citationMutsaka‐Makuvaza, M. J., Zingoni, Z. M., Katsidzira, A., Tshuma, C., Chin’ombe, N., Zhou, X., Webster, B. L., & Midzi, N. (2019) · Parasites & Vectors · doi:10.1186/s13071-019-3667-5 · Cited by 40 · see citing works
Blood Fluke Exploitation of Non-Cognate CD4+ T Cell Help to Facilitate Parasite Development
Lamb, E. W., Walls, C. D., Pesce, J. T., Riner, D. K., Maynard, S. K., Crow, E. T., Wynn, T. A., Schaefer, B. C., & Davies, S. J. A. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000892 · Cited by 37 · see citing works
EARLY VARIATIONS OF HOST THYROXINE AND INTERLEUKIN-7 FAVOR SCHISTOSOMA MANSONI DEVELOPMENT
Saule, P., Adriaenssens, É., Delacre, M., Chassande, O., Bossu, M., Auriault, C., & Wolowczuk, I. (2002) · Journal of Parasitology · doi:10.1645/0022-3395(2002)088[0849:evohta]2.0.co;2 · Cited by 37 · see citing works
Cheng, Y., Wen-jian, S., Liu, W., Lei, J., Mo, H.-M., Ruppel, A., & Li, Y. (2008) · Parasitology Research · doi:10.1007/s00436-008-0880-0 · Cited by 35 · see citing works
p values for pathogens: statistical inference from infectious-disease data
Mutapi, F., & Roddam, A. (2002) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(02)00240-2 · Cited by 35 · see citing works
Wami, W. M., Nausch, N., Midzi, N., Gwisai, R., Mduluza, T., Woolhouse, M. E. J., & Mutapi, F. (2015) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0003649 · Cited by 31 · see citing works
Wami, W. M., Nausch, N., Bauer, K., Midzi, N., Gwisai, R., Peter Simmonds, K., Mduluza, T., Woolhouse, M. E. J., & Mutapi, F. (2014) · Parasitology · doi:10.1017/s0031182014000213 · Cited by 31 · see citing works
A Comparison of Two Geographical Strains of Schistosoma haematobium
Webbe, G., & James, C. (1971) · Journal of Helminthology · doi:10.1017/s0022149x0000715x · Cited by 31 · see citing works
Relation of Tegumentary Phosphohydrolase to Purine and Pyrimidine Transport in Schistosoma mansoni
Levy, M. G., & Read, C. P. (1975) · Journal of Parasitology · doi:10.2307/3279457 · Cited by 31 · see citing works
Ahmed, S. A. A., & Gad, M. Z. (1995) · PubMed · Cited by 31 · see citing works
Culture ofSchistosoma haematobium in vivoandin vitro
Smith, M. A., Clegg, J. A., & Webbe, G. (1976) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1976.11687100 · Cited by 28 · see citing works
Wolde, M., Berhe, N., Medhin, G., Challa, F., van Die, I., & Tsegaye, A. (2019) · Microbiology Insights · doi:10.1177/1178636119849934 · Cited by 27 · see citing works
Tang, H., Ming, Z., Liu, R., Xiong, T., Grevelding, C. G., Dong, H., & Jiang, M.-S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054432 · Cited by 24 · see citing works
Mutsaka‐Makuvaza, M. J., Zingoni, Z. M., Tshuma, C., Ray, S. C., Zhou, X., Webster, B. L., & Midzi, N. (2018) · Infectious Diseases of Poverty · doi:10.1186/s40249-018-0483-7 · Cited by 24 · see citing works
Liu, R., Cheng, W., Tang, H., Zhong, Q., Ming, Z., & Dong, H. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.00440 · Cited by 20 · see citing works
Wami, W. M., Nausch, N., Midzi, N., Gwisai, R., Mduluza, T., Woolhouse, M. E. J., & Mutapi, F. (2016) · BioMed Research International · doi:10.1155/2016/9162631 · Cited by 16 · see citing works
Schistosoma Egg Antigen Induces Oncogenic Alterations in Human Prostate Cells
Tuffour, I., Ayi, I., Gwira, T. M., Dumashie, E., Ashong, Y. A., & Appiah‐Opong, R. (2018) · Analytical Cellular Pathology · doi:10.1155/2018/4675380 · Cited by 15 · see citing works
Schistosomiasis as a worldwide problem: Pathology
von Lichtenberg, F. (1975) · Journal of Toxicology and Environmental Health · doi:10.1080/15287397509529319 · Cited by 14 · see citing works
Rujeni, N., Nausch, N., Midzi, N., Cowan, G. J. M., Burchmore, R., Cavanagh, D. R., Taylor, D. W., Mduluza, T., & Mutapi, F. (2013) · Journal of Tropical Medicine · doi:10.1155/2013/283619 · Cited by 11 · see citing works
Exploiting the Potential of Metabonomics in Large Population Studies: Three Venues
Singer, B. H., Utzinger, J., Ryff, C. D., Wang, Y., & Holmes, E. C. (2007) · Elsevier eBooks · doi:10.1016/b978-044452841-4/50012-6 · Cited by 11 · see citing works
Abdel-Rahim, I. M., Kaiser, C., Homeida, M., Elsheikh, M., Schmidt, E. M., Ehrich, J. H. H., & Doehring-Schwerdfeger, E. (1990) · PubMed · Cited by 10 · see citing works
Panić, G., Coulibaly, J. T., Harvey, N. E., Keiser, J., & Swann, J. R. (2018) · Journal of Proteome Research · doi:10.1021/acs.jproteome.7b00910 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mutapi, F., Pfavayi, L., Osakunor, D., Lim, R., Kasambala, M., Mutemeri, A., Rusakaniko, S., Chibanda, D., & Mduluza, T. (2021) · PLOS Neglected Tropical Diseases · doi:10.1371/journal.pntd.0009660 · Cited by 25 · see citing works
“We have recently reported that early childhood infections with schistosomes affect metabolism in children aged 5 years and below, [39], which may have a subsequent impact on ECD.”
BackgroundSelf-citationZhu, P., Wu, K., Zhang, C., Batool, S. S., Li, A., Yu, Z., & Huang, J. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011498 · Cited by 17 · see citing works
Untargeted serum metabolomics analysis of Trichinella spiralis-infected mouse
Chienwichai, P., Thiangtrongjit, T., Tipthara, P., Tärning, J., Adisakwattana, P., & Reamtong, O. (2023) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0011119 · Cited by 12 · see citing works
Chienwichai, P., Nogrado, K. S., Tipthara, P., Tärning, J., Limpanont, Y., Chusongsang, P., Chusongsang, Y., Tanasarnprasert, K., Adisakwattana, P., & Reamtong, O. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.910177 · Cited by 10 · see citing works
Zdesenko, G., Mduluza, T., & Mutapi, F. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.914372 · Cited by 10 · see citing works
Prevalence Mapping of Schistosoma mansoni Among Pre-school Age Children in Rwanda
Rujeni, N., Bayingana, J. B., Nyandwi, E., Ntakarutimana, A., Kagabo, J., Rutayisire, R., Shema, E., Kanimba, P., Mbonigaba, J. B., & Ruberanziza, E. (2022) · Frontiers in Pediatrics · doi:10.3389/fped.2022.906177 · Cited by 9 · see citing works
Osakunor, D. N. M., Ishida, K., Lamanna, O. K., Rossi, M., Dwomoh, L., & Hsieh, M. H. (2022) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0010176 · Cited by 8 · see citing works
Self-citationMetabolomics for biomarker discovery in schistosomiasis: A systematic scoping review
Midzi, H., Vengesai, A., Muleya, V., Kasambala, M., Mduluza-Jokonya, T. L., Chipako, I., Siamayuwa, C. E., Mutapi, F., Naicker, T., & Mduluza, T. (2023) · Frontiers in Tropical Diseases · doi:10.3389/fitd.2023.1108317 · Cited by 6 · see citing works
Ghezellou, P., von Bülow, V., Luh, D., Badin, E., Albuquerque, W. W. C., Roderfeld, M., Roeb, E., Grevelding, C. G., & Spengler, B. (2024) · PNAS Nexus · doi:10.1093/pnasnexus/pgae104 · Cited by 4 · see citing works
Paediatric schistosomiasis: last mile preparations for deploying paediatric praziquantel
Mutapi, F., Garba, A., Woolhouse, M. E. J., & Kazyoba, P. E. (2024) · Trends in Parasitology · doi:10.1016/j.pt.2024.06.011 · Cited by 4 · see citing works
Mireille, K. P., Musaigwa, F., Kamguia, L. M., Kamdem, S. D., Mbanya, M. G., Lamberton, P. H. L., & Nono, J. K. (2024) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0012009 · Cited by 4 · see citing works
Ndolo, S. M., Zachariah, M., Molefi, L., Phaladze, N., & Sichilongo, K. (2021) · Expert Review of Proteomics · doi:10.1080/14789450.2021.2012454 · Cited by 2 · see citing works
Ola, E. M., Balogun, T. H., Isijola, R. O., & Ajakaye, O. G. (2025) · PLoS ONE · doi:10.1371/journal.pone.0329740 · Cited by 1 · see citing works
Roy, S., & Lyndem, L. M. (2026) · Acta Tropica · doi:10.1016/j.actatropica.2026.108151 · Cited by 1 · see citing works
Gene expression changes in mammalian hosts during schistosomiasis: a review
Namulondo, J., Mulindwa, J., Nyangiri, O. A., Egesa, M., Noyes, H. A., & Matovu, E. (2021) · Open Research Africa · doi:10.12688/aasopenres.13312.1 · Cited by 1 · see citing works
Midzi, H., Naicker, T., Vengesai, A., Choto, E. T., Muchesa, P., Kasambala, M., Mduluza-Jokonya, T. L., Muleya, V., Nyagumbo, E., Kapanga, D. T., et al. (2024) · Frontiers in Tropical Diseases · doi:10.3389/fitd.2024.1358514 · Cited by 1 · see citing works
Fok, L., Dai, H. D., Brett‐Major, D. M., Animut, A., Erko, B., Linville, J., Negash, Y., & Degarege, A. (2025) · Pathogens · doi:10.3390/pathogens14020123
Ali, H. A., Khadar, A., Nuh, A. M., Abdi, H. A., Osman, O. M., Muse, A. H., & Muse, M. S. (2026) · Discover Public Health · doi:10.1186/s12982-026-01891-5
Schistosomiasis and stunting: microbial and metabolic mechanisms in early childhood
Osakunor, D. N. M., Pfavayi, L. T., Mduluza, T., & Mutapi, F. (2026) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2025.0094
Self-citationChienwichai, P., Tipthara, P., Tärning, J., Limpanont, Y., Tanasanprasert, K., Kiangkoo, N., Thiangtrongjit, T., Adisakwattana, P., & Reamtong, O. (2026) · Current Research in Parasitology and Vector-Borne Diseases · doi:10.1016/j.crpvbd.2026.100398
- Authors
- Osakunor, D. N. M., Mduluza, T., Osei-Hyiaman, D., Burgess, K., Woolhouse, M. E. J., & Mutapi, F.
- Affiliations
- University of Edinburgh (GB)
- University of Zimbabwe (ZW)
- Corresponding author
- Osakunor, Derick N. M.
- Mduluza, Takafira
- Burgess, Karl
- Woolhouse, Mark E. J.
- Mutapi, Francisca
- ORCID
- Venue
- PLoS neglected tropical diseases
- Publisher
- Public Library of Science (PLoS)
- Published
- 2020-12-14
- Volume
- 14
- Issue
- 12
- Pages
- e0008866
- ISSN
- 1935-2727 (ISSN-L)
- 1935-2735
- PMC
- PMC7735607
- OpenAlex
- W3111718474
- Cited by
- 20
- References
- 96
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 4 · 2023: 3 · 2022: 4 · 2021: 3
- FWCI
- 1.87
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS neglected tropical diseases (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
- Funders
- Thrasher Research Fund (12440)
- Wellcome Trust (108061/Z/15/Z)
- Oak Foundation
- Darwin Trust of Edinburgh
- National Institute for Health Research (16/136/33)
- Topics
- Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Mollusks and Parasites Studies
- Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
- Keywords
- Schistosoma haematobium, schistosomiasis, energy metabolism, purine metabolism, serum metabolite profiles, praziquantel treatment, preschool children, infection intensity, malnutrition, host-parasite interactions
- MeSH terms
- Animals, Anthelmintics, Child, Preschool, Energy Metabolism, Female, Humans, Male, Praziquantel, Purines, Schistosoma haematobium, Schistosomiasis haematobia
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review