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Could diet composition modulate pathological outcomes in schistosomiasis mansoni? A systematic review of in vivo preclinical evidence

Published online by Cambridge University Press:  05 February 2018

Débora Vasconcelos Bastos Marques ,
Amanda Aparecida Felizardo ,
Raquel Lopes Martins Souza ,
Alessandro Antônio Costa Pereira ,
Reggiani Vilela Gonçalves  and
Rômulo Dias Novaes
Débora Vasconcelos Bastos Marques
Affiliation:
Department Pathology and Parasitology, Federal University of Alfenas, Institute of Biomedical Sciences, Alfenas, 37130-000, Minas Gerais, Brazil
Amanda Aparecida Felizardo
Affiliation:
Department of Structural Biology, Federal University of Alfenas, Institute of Biomedical Sciences, Alfenas, 37130-000, Minas Gerais, Brazil
Raquel Lopes Martins Souza
Affiliation:
Department Pathology and Parasitology, Federal University of Alfenas, Institute of Biomedical Sciences, Alfenas, 37130-000, Minas Gerais, Brazil
Alessandro Antônio Costa Pereira
Affiliation:
Department Pathology and Parasitology, Federal University of Alfenas, Institute of Biomedical Sciences, Alfenas, 37130-000, Minas Gerais, Brazil
Reggiani Vilela Gonçalves
Affiliation:
Department of Animal Biology, Federal University of Viçosa, Viçosa, 36570-000, Minas Gerais, Brazil
Rômulo Dias Novaes*
Affiliation:
Department of Structural Biology, Federal University of Alfenas, Institute of Biomedical Sciences, Alfenas, 37130-000, Minas Gerais, Brazil
*
Author for correspondence: Rômulo Dias Novaes, E-mail: [email protected], [email protected]
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Abstract

Schistosomiasis and malnutrition are often overlapped in poor communities, resulting in disproportionately high mortality rates. Currently, fragmented data make it difficult to define the relationship between diet and schistosomiasis. Thus, we systematically review the preclinical evidence on the impact of diet in Schistosoma mansoni infection. From a structured search, we recovered 27 original articles. All studies used mice and most of them investigated hypoproteic (70.37%), hyperlipidic (22.22%) or vitamin-deficient (7.41%) diets. Diets based on carbohydrate, zinc or milk supplementation were investigated at a reduced frequency (3.70% each). Hypoproteic diets attenuated parasitic load and granulomatous inflammation, but also reduced host resistance to S. mansoni infection, determining higher mortality rates. By stimulating steatohepatitis, parasitic load and granulomatous inflammation, hyperlipidic diets increase organ damage and mortality in infected animals. Although a high-sugar diet and vitamin restriction potentiate and zinc supplementation attenuates S. mansoni infection, the current evidence for these diets remains inconclusive. Analysis of methodological quality indicated that the current evidence is at high risk of bias due to incomplete characterization of the experimental design, diet composition and treatment protocols. From the bias analysis, we report methodological limitations that should be considered to avoid systematic reproduction of inconsistent and poorly reproducible experimental designs.

Keywords

Experimental parasitologymalnutritionSchistosoma mansonischistosomiasis
Type
Review Article
Information
Parasitology , Volume 145 , Issue 9 , August 2018 , pp. 1127 - 1136
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Copyright © Cambridge University Press 2018 

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References

Abdul-ghani, RA and Hassan, AA (2010) Murine schistosomiasis as a model for human schistosomiasis mansoni: similarities and discrepancies. Parasitology Research 107, 1–8.Google Scholar
Adenowo, AF, Oyinloye, BE, Ogunyinka, BI and Kappo, AP (2015) Impact of human schistosomiasis in sub-Saharan Africa. Brazilian Journal of Infectious Diseases 19, 196–205.Google Scholar
Akpom, CA and Warren, KS (1975) Calorie and protein malnutrition in chronic murine schistosomiasis mansoni: effect on the parasite and the host. Journal of Infectious Diseases 132, 6–14.Google Scholar
Alencar, AC, Neves, RH, Águila, MB, Mandarim-de-Lacerda, CA, Gomes, DC and Machado-Silva, JR (2009) High fat diet has a prominent effect upon the course of chronic schistosomiasis mansoni in mice. Memorias do Instituto Oswaldo Cruz 104, 608–613.Google Scholar
Alencar, AC, Neves, RH, De Oliveira, AV and Machado-Silva, JR (2012) Changes in the small intestine of Schistosoma mansoni infected mice fed a high-fat diet. Parasitology 139, 716–725.Google Scholar
Alves, CC, Araujo, N, Cassali, GD and Fonseca, CT (2016) Parasitological, pathological and immunological parameters associated with Schistosoma mansoni infection and reinfection in BALB/c and C57BL/6 mice. Journal of Parasitology 102, 336–341.Google Scholar
Anderson, LA and Cheever, AW (1972) Comparison of geographical strains of Schistosoma mansoni in the mouse. Bulletin of the World Health Organization 46, 233–242.Google Scholar
Andrade, ZA and Sadigursky, M (1985) A comparative study of the Feira de Santana (Bahia) and Porto Rico strains of Schistosoma mansoni in the experimental infection of mice. Memorias do Instituto Oswaldo Cruz 80, 37–40.Google Scholar
Balen, J, Liu, Z-C, McManus, DP, Raso, G, Utzinger, J, Xiao, S-Y, Yu, D-B, Zhao, Z-Y and Li, Y-S (2013) Health access livelihood framework reveals potential barriers in the control of schistosomiasis in the Dongting Lake area of Hunan Province, China. PLoS Neglected Tropical Diseases 7, e2350.Google Scholar
Bara, M and Joffe, AR (2014) The methodological quality of animal research in critical care: the public face of science. Annals of Intensive Care 4, 41–49.Google Scholar
Barnard, DE, Lewis, SM, Teter, BB and Thigpen, JE (2009) Open- and closed-formula laboratory animal diets and their importance to research. Journal of the American Association for Laboratory Animal Science 48, 709–713.Google Scholar
Barros, AF, Oliveira, SA, Carvalho, CL, Silva, FL, de Souza, VCA, da Silva, AL, de Araujo, RE, Souza, BSF, Soares, MBP, Costa, VMA and de Coutinho, EM (2014) Low transformation growth factor-β1 production and collagen synthesis correlate with the lack of hepatic periportal fibrosis development in undernourished mice infected with Schistosoma mansoni. Memorias do Instituto Oswaldo Cruz 109, 210–219.Google Scholar
Barros, LA, Biolchini, CL and Neves, RH (2009) Effect of praziquantel administration on hepatic stereology of mice infected with Schistosoma mansoni and fed a low-protein diet. Brazilian Journal of Medical and Biological Research 42, 812–815.Google Scholar
Bhattacharyya, KK (1965) Low protein diet as a factor in the production of experimental schistosomal hepatic fibrosis. Journal of Pathology and Bacteriology 89, 13–21.Google Scholar
Burns, EA (2004) Effects of aging on immune function. Journal of Nutition Health and Aging 8, 9–18.Google Scholar
Calder, PC (2013) Feeding the immune system. Proceedings of the Nutrition Society 72, 299–309.Google Scholar
Chalvon-demersay, T, Blachier, F, Tomé, D and Blais, A (2017) Animal models for the study of the relationships between diet and obesity: a focus on dietary protein and estrogen deficiency. Frontiers in Nutrition 4, 1–13.Google Scholar
Cheever, AW, Lenzi, JA, Lenzi, HL and Andrade, ZA (2002) Experimental models of Schistosoma mansoni infection. Memorias do Instituto Oswaldo Cruz 97, 917–940.Google Scholar
Colditz, G, Watson, DL, Gray, GD and Eady, SJ (1996) Some relationships between age, immune responsiveness and resistance to parasites in ruminants. International Journal for Parasitology 26, 869–877.Google Scholar
Colley, DG, Bustinduy, AL, Secor, WE and King, CH (2014) Human schistosomiasis. Lancet 383, 2253–2264.Google Scholar
Corbett, EL, Butterworth, AE, Fulford, AJ, Ouma, JH and Sturrock, RF (1992) Nutritional status of children with schistosomiasis mansoni in two different areas of Machakos District, Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 266–273.Google Scholar
Coutinho, EM (2004) Malnutrition and hepatic fibrosis in murine schistosomiasis. Memorias do Instituto Oswaldo Cruz 99, 85–92.Google Scholar
Coutinho, EM, Abath, FG, de Freitas, LP, Salzano, AC, Lapa, MA, Campos, FS and Melo, EB (1991) Liver and serum soluble protein changes and pathomorphology in undernourished mice with acute schistosomiasis mansoni. Revista da Sociedade Brasileira de Medicina Tropical 24, 235–243.Google Scholar
Coutinho, EM, de Souza, MM, Silva, LM, Cavalcanti, CL, de Araújo, RE, Barbosa Júnior, AA, Cheever, AW and Andrade, ZA (1997) Pathogenesis of schistosomal ‘pipestem’ fibrosis: a low-protein diet inhibits the development of ‘pipestem’ fibrosis in mice. International Journal of Experimental Pathology 78, 337–342.Google Scholar
Coutinho, EM, Ferreira, HS, Assunção, ML, Carvalho, SL, Oliveira, SA and Francelino, AA (2002) The use of protein hydrolysate improves the protein intestinal absorption in undernourished mice infected with Schistosoma mansoni. Revista da Sociedade Brasileira de Medicina Tropical 35, 585–590.Google Scholar
Coutinho, EM, Barros, AF, Barbosa, A, Oliveira, SA, Silva, LM, Araújo, RE and Andrade, ZA (2003) Host nutritional status as a contributory factor to the remodeling of schistosomal hepatic fibrosis. Memorias do Instituto Oswaldo Cruz 98, 919–925.Google Scholar
Coutinho, EM, Silva, FL, Barros, AF, Araújo, RE, Oliveira, SA, Luna, CF, Barbosa, AA and Andrade, ZA (2007) Repeated infections with Schistosoma mansoni and liver fibrosis in undernourished mice. Acta Tropica 101, 15–24.Google Scholar
Coutinho, EM, de Oliveira, SA, de Barros, AF, Silva, FL and Ramos, RP (2010) Manson's schistosomiasis in the undernourished mouse: some recent findings. Memorias do Instituto Oswaldo Cruz 105, 359–366.Google Scholar
Coutinho-Abath, E, Magalhães Filho, A and Barbosa, JM (1962) Lesões hepáticas no camundongo albino experimentalmente infestado por Schistosoma mansoni e submetido a dietas de diferentes teor proteico. Revista do Instituto de Medicina Tropical de São Paulo 4, 311–322.Google Scholar
Couto, JL, Ferreira, HS, da Rocha, DB, Duarte, ME, Assuncao, ML and Coutinho, EM (2002) Structural changes in the jejunal mucosa of mice infected with Schistosoma mansoni, fed low or high protein diets. Revista da Sociedade Brasileira de Medicina Tropical 35, 601–607.Google Scholar
Crevel, RW, Friend, JV, Goodwin, BF and Parish, WE (1992) High-fat diets and the immune response of C57Bl mice. British Journal of Nutrition 67, 17–26.Google Scholar
Czerwonogrodzka-Senczyna, A, Janusz, M, Jeznach-Steinhagen, A, Demkow, U and Pyrzak, B (2016) Nutrition and immune system in children with simple obesity. Advances in Experimental Medicine and Biology – Neuroscience and Respiration 878, 49–56.Google Scholar
Dajem, SMB, Mostafa, OMS and El-said, FG (2008) Susceptibility of two strains of mice to the infection with Schistosoma mansoni: parasitological and biochemical studies. Parasitology Research 103, 1059–1063.Google Scholar
Da Silva, AM, Corrêa, CL, Neves, RH and Machado-Silva, JR (2012) A high-fat diet associated with acute schistosomiasis mansoni causes disorganization in splenic architecture in mice. Experimental Parasitology 132, 193–199.Google Scholar
Davies, CM, Fairbrother, E and Webster, JP (2002) Mixed strain schistosome infections of snails and the evolution of parasite virulence. Parasitology 124, 31–38.Google Scholar
Eloi-santos, S, Olsen, NJ, Correa-oliveira, R and Colleypw, DG (1992) Schistosoma mansoni: mortality, pathophysiology, and susceptibility differences in male and female mice. Experimental Parasitology 75, 168–175.Google Scholar
Ferreira, HS and Coutinho, EM (1999) Should nutrition be considered as a supplementary measure in schistosomiasis control? Annals of Tropical Medicine and Parasitology 93, 437–447.Google Scholar
Festing, MFW (2016) Chapter 1 genetically defined strains in drug development and toxicity testing. Methods in Molecular Biology 1438, 1–17.Google Scholar
GBD 2016 Causes of Death Collaborators (2017) Global, regional, and national age-sex specific mortality for 264 causes of death, 1980–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet 390, 1151–1210.Google Scholar
Goes, VC, Neves, RH, Alencar, AC, Oliveira, AV, Gomes, DC and Machado-Silva, JR (2012) Effects of high-fat chow on heart tissue in acute and chronic experimental murine schistosomiasis mansoni. Parasitology 139, 1462–1470.Google Scholar
Goldsworthy, ME and Potter, PK (2014) Modelling age-related metabolic disorders in the mouse. Mammalian Genome 25, 487–496.Google Scholar
Gryseels, B (2012) Schistosomiasis. Infectious Disease Clinics of North America 26, 383–397.Google Scholar
Helmy, MMF, Mahmoud, SS and Fahmy, ZH (2009) Schistosoma mansoni: effect of dietary zinc supplement on egg granuloma in Swiss mice treated with praziqantel. Experimental Parasitology 122, 310–317.Google Scholar
Hooijmans, CR, Tillema, A, Leenaars, M and Ritskes-Hoitinga, M (2010) Enhancing search efficiency by means of a search filter for finding all studies on animal experimentation in PubMed. Laboratory Animals 44, 170–175.Google Scholar
Incani, RN and Cesari, IM (2001) Parasite and vertebrate host genetic heterogeneity determine the outcome of infection by Schistosoma mansoni. Parasitology Research 87, 131–137.Google Scholar
Inobaya, MT, Olveda, RM, Chau, TNP, Olveda, DU and Ross, AGP (2014) Prevention and control of schistosomiasis: a current perspective. Research and Reports in Tropical Medicine 5, 65–75.Google Scholar
Jackson, SJ, Andrews, N, Ball, D, Bellantuono, I, Gray, J, Hachoumi, L, Holmes, A, Latcham, J, Petrie, A, Potter, P, Rice, A, Ritchie, A, Stewart, M, Strepka, C, Yeoman, M and Chapman, K (2017) Does age matter? The impact of rodent age on study outcomes. Laboratory Animals 51, 160–169.Google Scholar
Jenkins, M (2004) Evaluation of methodological search filters – a review. Health Information & Libraries Journal 21, 148–163.Google Scholar
Katona, P and Katona-Apte, J (2008) The interaction between nutrition and infection. Clinical Infectious Disease 46, 1582–1588.Google Scholar
Kilkenny, C, Parsons, N, Kadyszewski, E, Festing, MFW, Cuthill, IC, Fry, D, Hutton, J and Altman, DG (2009) Survey of the quality of experimental design, statistical analysis and reporting of research using animals. PLoS ONE 4, e7824.Google Scholar
Kilkenny, C, Browne, WJ, Cuthill, IC, Emerson, M and Altman, DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biology 8, e1000412.Google Scholar
Knauft, RF and Warren, KS (1969) The effect of calorie and protein malnutrition on both the parasite and the host in acute murine schistosomiasis mansoni. Journal of Infectious Diseases 120, 560–575.Google Scholar
Korou, LA, Doulamis, IP, Tzanetakou, IP, Mikhailidis, DP and Perrea, DN (2013) The effect of biological age on the metabolic responsiveness of mice fed a high-fat diet. Laboratory Animals 47, 241–247.Google Scholar
Krawinkel, MB (2012) Interaction of nutrition and infections globally: an overview. Annals of Nutrition and Metabolism 61, 39–45.Google Scholar
Landis, SC, Amara, SG, Asadullah, K, Austin, CP, Bradley, EW, Crystal, RG, Darnell, RB and Robert, J (2013) A call for transparent reporting to optimize the predictive value of preclinical research. Nature 490, 187–191.Google Scholar
Lapchak, PA, Zhang, JH and Noble-haeusslein, LJ (2013) RIGOR guidelines: escalating STAIR and STEPS for effective translational research. Translational Stroke Research 4, 279–285.Google Scholar
Leidy, HJ and Campbell, WW (2011) The effect of eating frequency on appetite control and food intake: brief synopsis of controlled feeding studies. Journal of Nutrition 141, 154–157.Google Scholar
Lopes, IC, Santos, VRC, Souza, VLRB and Rodrigues, IRC (2006) Histopathological study of Schistosoma mansoni infection in the murine model using the PC (Pará) and LILA (Maranhão) strains. Memorias do Instituto Oswaldo Cruz 101, 273–277.Google Scholar
Machado-silva, JR, Heisler, R, Ormond, L, Maria, R, De Oliveira, F and Carlos, A (2005) Do mice genetically selected for resistance to oral tolerance provide selective advantage for Schistosoma mansoni infection? Experimental Parasitology 111, 1–7.Google Scholar
Machado-silva, JR, Neves, RH and Cerqueira, E (2010) Hepatic stereology of acute schistosomiasis mansoni infection in C57BL/ 10 and CBA mice. Revista de Patologia Tropical 39, 211–219.Google Scholar
Magalhães, LA, Guaraldo, AM, de Carvalho Bastos, O, Boschero, AC, Piedrabuena, AE and Dottaviano, EJ (1978) Influência da dieta hiperglicêmica e do diabetes aloxânico sobre a vitalidade do Schistosoma mansoni Sambon, 1907, em camundongos experimentalmente infectados. Revista de Saude Publica 12, 267–276.Google Scholar
Maghraby, AS, Mohamed, MA and Abdel-Salam, AM (2005) Anti-schistosomal activity of colostral and mature camel milk on Schistosoma mansoni infected mice. Asia Pacific Journal of Clinical Nutrition 14, 432–438.Google Scholar
Mekonnen, Z, Meka, S, Zeynudin, A and Suleman, S (2014) Schistosoma mansoni infection and undernutrition among school age children in Fincha'a sugar estate, rural part of West Ethiopia. BMC Research Notes 7, 763.Google Scholar
Mitra, AK and Mawson, AR (2017) Neglected tropical diseases: epidemiology and global burden. Tropical Medicine and Infectious Disease 2, 36.Google Scholar
Moher, D, Liberati, A, Tetzlaff, J and Altman, DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLos Medicine 6, e1000097.Google Scholar
Moraal, M, Leenaars, PPAM, Arnts, H, Smeets, K, Savenije, BS and Curfs, JHAJ (2012) The influence of food restriction versus ad libitum feeding of chow and purified diets on variation in body weight, growth and physiology of female Wistar rats. Laboratory Animals 46, 101–107.Google Scholar
Moran, CJ, Ramesh, A, Brama, PAJ, Byrne, JMO, Brien, FJO and Levingstone, TJ (2016) The benefits and limitations of animal models for translational research in cartilage repair. Journal of Experimental Orthopaedics 3, 1.Google Scholar
Munisi, DZ, Buza, J, Mpolya, EA and Kinung'hi, SM (2016) Schistosoma mansoni infections, undernutrition and anaemia among primary schoolchildren in two onshore villages in Rorya District, North-Western Tanzania. PLoS ONE 11, e0167122.Google Scholar
Nakazawa, M, Fantappie, MR, Freeman, GL Jr., Eloi-Santos, S, Olsen, NJ, Kovacs, WJ, Secor, WE and Colley, DG (1997) Schistosoma mansoni: susceptibility differences between male and female mice can be mediated by testosterone during early infection. Experimental Parasitology 85, 233–240.Google Scholar
Negrão-Corrêa, D, Fittipaldi, JF, Lambertucci, JR, Teixeira, MM, De Figueiredo Antunes, CM and Carneiro, M (2014) Association of Schistosoma mansoni-specific IgG and IgE antibody production and clinical schistosomiasis status in a rural area of Minas Gerais, Brazil. PLoS ONE 9, e88042.Google Scholar
Neves, RH, Alencar, AC, Aguila, MB, Mandarim-de-Lacerda, CA, Machado-Silva, JR and Gomes, DC (2006) Hepatic stereology of schistosomiasis mansoni infected-mice fed a high-fat diet. Memorias do Instituto Oswaldo Cruz 101, 253–260.Google Scholar
Neves, RH, Alencar, AC, Costa-Silva, M, Águila, MB, Mandarim-de-Lacerda, CA, Machado-Silva, JR and Gomes, DC (2007) Long-term feeding a high-fat diet causes histological and parasitological effects on murine schistosomiasis mansoni outcome. Experimental Parasitology 115, 324–332.Google Scholar
Oliveira, SA, Silva, LM, Barbosa, AA, Ribeiro-dos-Santos, R, Coutinho, EM, Andrade, ZA and Soares, MBP (2004) Decreased humoral and pathologic responses in undernourished mice infected with Schistosoma mansoni. Parasitology Research 93, 30–35.Google Scholar
Pereira, RM, Greco, GM, Moreira, AM, Chagas, PF, Caldas, IS, Gonçalves, RV and Novaes, RD (2017) Applicability of plant-based products in the treatment of Trypanosoma cruzi and Trypanosoma brucei infections: a systematic review of preclinical in vivo evidence. Parasitology 144, 1275–1287.Google Scholar
Pérez, L, Vicente, B, Blanco-gómez, A, Castellanos, A, Pérez-losada, J and Muro, A (2014) Identifying phenotypes involved in susceptibility to Schistosoma mansoni infection in F1B6CBA mice. Acta Parasitologica 59, 529–539.Google Scholar
Pettersson, US, Waldén, TB, Carlsson, PO, Jansson, L and Phillipson, M (2012) Female mice are protected against high-fat diet induced metabolic syndrome and increase the regulatory T cell population in adipose tissue. PLoS ONE 7, e46057.Google Scholar
Picchi, MG, Mattos, AM, Barbosa, MR, Duarte, CP, Gandini, MA, Portari, GV and Jordão, AA (2011) A high-fat diet as a model of fatty liver disease in rats. Acta Cirúrgica Brasileira 26, 25–30.Google Scholar
Pinto-Almeida, A, Mendes, T, de Oliveira, RN, Corrêa, SAP, Allegretti, SM, Belo, S, Tomás, A, Anibal, FF, Carrilho, E and Afonso, A (2016) Morphological characteristics of Schistosoma mansoni PZQ-resistant and -susceptible strains are different in presence of Praziquantel. Frontiers in Microbiology 7, 1–11.Google Scholar
Ramos, RP, Costa, VMA, Melo, CF, Souza, VMO, Malagueño, E, Coutinho, EM, Abath, FGC and Montenegro, SML (2006) Preliminary results on interleukin-4 and interleukin-10 cytokine production in malnourished, inducible nitric oxide synthase-deficient mice with schistosomiasis mansoni infection. Memorias do Instituto Oswaldo Cruz 101, 331–332.Google Scholar
Reeves, PG, Nielsen, FH and Fahey, GC (1993) AIN- 93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc Writing Committee on the reformulation of the AIN-76A rodent diet. Journal of Nutrition 123, 1939–1951.Google Scholar
Saoud, MFA (1966) The infectivity and pathogenicity of geographical strains of Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 60, 585–600.Google Scholar
Sena, E, Bart van der Worp, H, Howells, D and Macleod, M (2007) How can we improve the pre-clinical development of drugs for stroke? Trends in Neurosciences 30, 433–439.Google Scholar
Shalaby, I, Gherbawy, Y and Banaja, A (2011) Genetic diversity among Schistosoma mansoni population in the western region of Saudi Arabia. Tropical Biomedicine 28, 90–101.Google Scholar
Speziali, E, Aranha, CHM, Santiago, AF and Oliveira, RP (2010) Ageing down-modulates liver inflammatory immune responses to schistosome infection in mice. Scandinavian Journal of Immunology 71, 240–248.Google Scholar
Strandberg, L, Verdrengh, M, Enge, M, Andersson, N, Amu, S, Onnheim, K, Benrick, A, Brisslert, M, Bylund, J, Bokarewa, M, Nilsson, S and Jansson, JO (2009) Mice chronically fed high-fat diet have increased mortality and disturbed immune response in sepsis. PLoS ONE 4, e7605.Google Scholar
Svendsen, C, Alexander, J, Paulsen, JE, Knutsen, HK, Hjertholm, H, Brantsæter, AL and Husøy, T (2012) The impact of commercial rodent diets on the induction of tumours and flat aberrant crypt foci in the intestine of multiple intestinal neoplasia mice. Laboratory Animals 46, 207–214.Google Scholar
Theron, A, Rognon, A, Gourbal, B and Mitta, G (2014) Infection, genetics and evolution multi-parasite host susceptibility and multi-host parasite infectivity: a new approach of the Biomphalaria glabrata/Schistosoma mansoni compatibility polymorphism. Infection, Genetics And Evolution 26, 80–88.Google Scholar
Vandamme, TF (2015) Rodent models for human diseases. European Journal of Pharmacology 759, 84–89.Google Scholar
Van de Vijver, KK, Colpaert, CG, Jacobs, W, Kuypers, K, Hokke, CH, Deelder, M and Van Marck, EA (2006) The host's genetic background determines the extent of angiogenesis induced by schistosome egg antigens. Acta Tropica 99, 243–251.Google Scholar
Weisstaub, G, Aguilar, AM and Uauy, R (2014) Treatment and prevention of malnutrition in Latin America: focus on Chile and Bolivia. Food and Nutrition Bulletin 35, S39–S46.Google Scholar
Wilson, RA (1990) Leaky livers, portal shunting and immunity to schistosomes. Parasitology Today 6(11), 354–358.Google Scholar
Wilson, RA (2009) The saga of schistosome migration and attrition. Parasitology 136(12), 1581–1592.Google Scholar
WHO, World Health Organization (2017) Schistosomiasis. Updated October 2017. Available at http://www.who.int/mediacentre/factsheets/fs115/en/.Google Scholar
Yole, DS, Gikuru, SK, Wango, EO, Kithome, K and Kiarie, S (2006) Influence of age of mice on the susceptibility to murine schistosomiasis infection. African Journal of Health Sciences 13, 47–54.Google Scholar
Zapatera, B, Prados, A, Gómez-Martínez, S and Marcos, A (2015) Immunonutrition: methodology and applications. Nutricion Hospitalaria 31, 145–154.Google Scholar
Zoni, AC, Catalá, L and Ault, SK (2016) Schistosomiasis prevalence and intensity of infection in Latin America and the Caribbean countries, 1942–2014: a systematic review in the context of a regional elimination goal. PLoS Neglected Tropical Diseases 10, e0004493.Google Scholar
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