Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-24T03:42:19.901Z Has data issue: false hasContentIssue false
  • English
  • Français

Changes in the small intestine of Schistosoma mansoni-infected mice fed a high-fat diet

Published online by Cambridge University Press:  06 February 2012

ALBA CRISTINA MIRANDA DE BARROS ALENCAR ,
RENATA HEISLER NEVES ,
ALBANITA VIANA DE OLIVEIRA  and
JOSÉ ROBERTO MACHADO-SILVA
ALBA CRISTINA MIRANDA DE BARROS ALENCAR
Affiliation:
Department of Microbiology, Immunology and Parasitology, Faculty of Medical Sciences, State University of Rio de Janeiro, Brazil Department of Pathology and Laboratories, Faculty of Medical Science, State University of Rio de Janeiro, Brazil
RENATA HEISLER NEVES
Affiliation:
Laboratory of Helminth Parasites of Vertebrates, Oswaldo Cruz Institute, Rio de Janeiro, Brazil
ALBANITA VIANA DE OLIVEIRA
Affiliation:
Department of Pathology and Laboratories, Faculty of Medical Science, State University of Rio de Janeiro, Brazil
JOSÉ ROBERTO MACHADO-SILVA*
Affiliation:
Department of Microbiology, Immunology and Parasitology, Faculty of Medical Sciences, State University of Rio de Janeiro, Brazil
*
*Corresponding author: Laboratório de Helmintologia Romero Lascasas Porto, Departamento de Microbiologia, Imunologia e Parasitologia, Faculdade de Ciências Médicas, Centro Biomédico, Universidade do Estado do Rio de Janeiro, Rua Prof. Manoel de Abreu, 444, 5° andar, CEP: 20511- 070, Rio de Janeiro, Brasil. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The consumption of a high-fat diet modifies both the morphology of the small intestine and experimentally tested effects of schistosomiasis mansoni. However, whether a schistosomiasis infection associated with a high-fat diet causes injury to the small intestine has never been investigated. Mice were fed either a high-fat or a standard-fat diet for 6 months and were then infected with Schistosoma mansoni cercariae. Physical characteristics of the intestinal tissue (mucosal thickness, small intestinal villi length and height, and abundance of goblet cells and enterocytes on the villous surface) and the distribution of granulomas along the intestinal segments and their developmental stage were measured at the time of sacrifice (9 or 17 weeks post-infection). The group fed a high-fat diet exhibited different granuloma stages, whereas the control group possessed only exudative granulomas. The chronically infected mice fed a high-fat diet exhibited higher granuloma and egg numbers than the acutely infected group. Exudative, exudative/exudative-productive and exudative-productive granulomas were present irrespective of diet. Computer-aided morphometric analysis confirmed that villus length, villus width, muscular height and submucosal height of the duodenal and jejunal segments were affected by diet and infection. In conclusion, a high-fat diet and infection had a significant impact on the small intestine morphology and morphometry among the animals tested.

Keywords

Schistosoma mansoniexperimental infectiongutcholesterolhistopathologymorphometrymorphology
Type
Research Article
Information
Parasitology , Volume 139 , Issue 6 , May 2012 , pp. 716 - 725
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alencar, A. C. M. B., Neves, R. H., Aguila, M. B., Mandarim-de-Lacerda, C. A., Corrêa, D. G. and Machado-Silva, J. R. (2009). High fat diet has a prominent effect upon the course of chronic schistosomiasis mansoni in mice. Memórias do Instituto Oswaldo Cruz 104, 608–613.CrossRefGoogle Scholar
Andrade, Z. A. (2009). Schistosomiasis and liver fibrosis. Parasite Immunology 31, 656–663.CrossRefGoogle ScholarPubMed
Backhed, F., Ding, H., Wang, T., Hooper, L. V., Koh, G. Y., Nagy, A., Semenkovich, C. F. and Gordon, J. I. (2004). The gut microbiota as an environmental factor that regulates fat storage. Proceedings of the National Academy of Sciences, USA 101, 15718–15723.CrossRefGoogle ScholarPubMed
Backhed, F., Manchester, J. K., Semenkovich, C. F. and Gordon, J. I. (2007). Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proceedings of the National Academy of Sciences, USA 104, 979–984.CrossRefGoogle ScholarPubMed
Balint, J. A., Fried, M. B. and Imai, C. (1980). Ileal uptake of oleic acid: evidence for adaptive response to high fat feeding. American Journal of Clinical Nutrition 33, 2276–2280.CrossRefGoogle ScholarPubMed
Barth, L. R., Fernandes, A. P. and Rodrigues, V. (1996). Oviposition by Schistosoma mansoni during in vitro cultivation. Revista do Instituto de Medicina Tropical de São Paulo 38, 423–426.CrossRefGoogle ScholarPubMed
Borgers, J., Moreels, T., De Man, J., Vrolix, G., Jacobs, W., Pelckmans, P. and Van Marck, E. (2000). Schistosoma mansoni infection causing diffuse enteric inflammation and damage of the enteric nervous system in the mouse small intestine. Neurogastroenterogy and Motility 12, 431–440.CrossRefGoogle Scholar
Cani, P. D., Amar, J. and Iglesias, M. A. (2007). Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56, 1761–1772.CrossRefGoogle ScholarPubMed
Cass, C. L, Johnson, J. R., Califf, L. L., Xu, T., Hernadez, H. J., Yates, 3rd, Jr. 3rd, Jr. and Williams, D. L. (2007). Proteomic analysis of Schistosoma mansoni egg secretions. Molecular and Biochemical Parasitology 155, 84–93.CrossRefGoogle ScholarPubMed
Cheever, A. W., Kamel, I. A., Elwi, A. M., Mosimann, J. E. and Danner, R. (1977). Schistosoma mansoni and S. haematobium infections in Egypt. Quantitative parasitological findings at necropsy. The American Journal of Tropical Medicine and Hygiene 26, 702–716.CrossRefGoogle ScholarPubMed
Cheever, A., Mosimann, J. E., Deb, S., Cheever, E. A. and Duvall, R. H. (1994). Natural history of Schistosoma mansoni infection in mice: egg production, egg passage in the feces, and contribution of host and parasite death to changes in worm numbers. The American Journal of Tropical Medicine and Hygiene 50, 269–280.CrossRefGoogle ScholarPubMed
Coutinho, E. M., Ferreira, H. S., Assunção, M. L., Carvalho, S. L., Oliveira, S. A. and Francelino, A. A. (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.CrossRefGoogle ScholarPubMed
Couto, J. L., Ferreira, H. S., Rocha, D. B., Duarte, M. E., Assunção, M. L. and Coutinho, E. M. (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.CrossRefGoogle ScholarPubMed
de Lima e Costa, M. F. and Katz, N. (1982). Comparative study of Schistosoma mansoni strains isolated from patients with toxemic or intestinal forms of schistosomiasis. The American Journal of Tropical Medicine and Hygiene 31, 499–504.CrossRefGoogle ScholarPubMed
de Wit, N. J., Bosch-Vermeulen, H., de Groot, P. J., Hooiveld, G. J., Bromhaar, M. M., Jansen, J., Müller, M. and van der Meer, R. (2008). The role of the small intestine in the development of dietary fat-induced obesity and insulin resistance in C57BL/6J mice. BioMed Central Medical Genomics 6, 1–14.Google Scholar
Ding, S., Chi, M. M., Scull, B. P., Rigby, R., Schwerbrock, N. M., Magness, S., Jobin, C. and Lund, P. K. (2010). High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. Plos One Journal Information 16, 5:e12191.CrossRefGoogle Scholar
Doenhoff, M. J., Hassounah, O., Murare, H., Bain, J. and Lucas, S. (1986). The schistosome egg granuloma: immunopathology in the cause of host protection or parasite survival? The American Journal of Tropical Medicine and Hygiene 80, 503–514.CrossRefGoogle ScholarPubMed
Doenhoff, M. J., Stanley, R. G., Griffiths, K. and Jackson, C. L. (2002). An anti-atherogenic effect of Schistosoma mansoni infections in mice associated with a parasite-induced lowering of blood total cholesterol. Parasitology 125, 415–421.CrossRefGoogle ScholarPubMed
Domingo, E. O. and Warren, K. S. (1969). Pathology and pathophysiology of the small intestine in murine schistosomiasis mansoni, including a review of the literature. Gastroenterology 56, 231–240.CrossRefGoogle ScholarPubMed
Feuerer, M., Herrero, L., Cipolletta, D., Naaz, A., Wong, J., Nayer, A., Lee, J., Goldfine, A. B., Benoist, C., Shoelson, S. and Mathis, D. (2009). Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nature Medicine 15, 930–939.CrossRefGoogle Scholar
Freire, N., Rodrigues-Silva, R., Machado-Silva, J. R. and Rey, L. A. (2003). A comparative parasitologic study on Biomphalaria glabrata snail and C3H/He mice infected with human and murine isolates of Schistosoma mansoni derived from Sumidouro, Rio de Janeiro, Brazil. Memórias do Instituto Oswaldo Cruz 98, 783–787.CrossRefGoogle Scholar
Galloway, S., Pallebage-Gamarallage, M. M., Takechi, R., Jian, L., Johnsen, R. D., Dhaliwal, S. S. and Mamo, J. C. (2008). Synergistic effects of high fat feeding and apolipoprotein E deletion on enterocytic amyloid-beta abundance. Lipids in Health and Disease 22, 7–15.Google Scholar
Holmes, J. C. (1990). Competition, contacts, and other factors restricting niches of parasitic helminths. Annales de Parasitologie Humaine et Comparée 65, 69–72.CrossRefGoogle ScholarPubMed
Kanuft, R. F. and Warren, K. S. J. (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 ScholarPubMed
Kintscher, U., Hartge, M., Hess, K., Foryst-Ludwig, A., Clemenz, M., Wabitsch, M., Fischer-Posovszky, P., Barth, T. F., Dragun, D., Skurk, T., Hauner, H., Blüher, M., Unger, T., Wolf, A. M., Knippschild, U., Hombach, V. and Marx, N. (2008). T lymphocyte Infiltration in visceral adipose tissue. A primary event in adipose tissue inflammation and the development of obesity-mediated insulin resistance. Ateriosclerosis, Thrombosis, and Vascular Biology 28, 1304–1310.CrossRefGoogle ScholarPubMed
Kvietys, P. R., Specian, R. D., Grisham, M. B. and Tso, P. (1991). Jejunal mucosal injury andrestitution: role of hydrolytic products of food digestion. American Journal of Physiology Gastrointestinal and Liver Physiology 261, 384–391.CrossRefGoogle ScholarPubMed
Lenzi, H. L., Kimmel, E., Schechtman, H., Pelajo-Machado, M., Romanha, W. S., Pacheco, R. G., Mariano, M. and Lenzi, J. A. (1998). Histoarchitecture of schistosomal granuloma development and involution: morphogenetic and biomechanical approaches. Memórias do Instituto Oswaldo Cruz 93, 141–151.CrossRefGoogle ScholarPubMed
Li Hsü, S. Y., Hsü, H. F., Davis, J. R. and Lust, G. L. (1972). Comparative studies on the lesions caused by eggs of Schistosoma mansoni in livers of albino mice and rhesus monkeys. Annals of Tropical Medicine and Parasitology 66, 89–97.CrossRefGoogle Scholar
Little, T. J., Horowitz, M. and Feinle-Bisset, C. (2007). Modulation by high-fat diets of gastrointestinal function and hormones associated with the regulation of energy intake: implications for the pathophysiology of obesity. The American Journal of Clinical Nutrition 86, 531–541.CrossRefGoogle ScholarPubMed
Little, T. J., Feltrin, K. L., Horowitz, M., Meyer, J. H., Wishart, J., Chapman, I. M. and Feinle-Bisset, C. (2008). A high-fat diet raises fasting plasma CCK but does not affect upper gut motility, PYY, and ghrelin, or energy intake during CCK-8 infusion in lean men. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 294, 45–51.CrossRefGoogle ScholarPubMed
Machado-Silva, J. R., Neves, R. H. and Rodrigues-Silva, R. (2010). Do schistosomes grow old? A confocal laser scanning microscopy study. Journal of Helminthology 84, 305–311.CrossRefGoogle Scholar
Martinez, E. M., Neves, R. H., de Oliveira, R. M., Machado-Silva, J. R. and Rey, L. (2003). Parasitological and morphological characteristics of Brazilian strains of Schistosoma mansoni in Mus musculus. Revista da Sociedade Brasileira de Medicina Tropical 36, 557–564.CrossRefGoogle ScholarPubMed
Matyash, V., Geier, C., Henske, A., Mukherjee, S., Hirsh, D., Thiele, C., Grant, B., Maxfield, F. R. and Kurzchalia, T. V. (2001). Distribution and transport of cholesterol in Caenorhabditis elegans. Molecular Biology of the Cell. 12, 1725–1736.CrossRefGoogle ScholarPubMed
Moreels, T. G., De Man, J. G., Bogers, J. J., De Winter, B. Y., Vrolix, G., Herman, A. G., Van Marck, E. A. and Pelckmans, P. A. (2001). Effect of Schistosoma mansoni-induced granulomatous inflammation on murine gastrointestinal motility. American Journal of Physiology – Gastrointestinal and Liver Physiology 280, 1030–1042.CrossRefGoogle ScholarPubMed
Neves, R. H., Alencar, A. C., Aguila, M. B., Mandarim-de-Lacerda, C. A., Corrêa, D. G. and Machado-Silva, J. R. (2006). Hepatic stereology of Schistosomiasis mansoni infected-mice fed a high-fat diet. Memórias do Instituto Oswaldo Cruz 101, 253–260.CrossRefGoogle ScholarPubMed
Neves, R. H., Alencar, A. C. M. B., Aguila, M. B., Mandarim-de-Lacerda, C. A., Corrêa, D. G. and Machado-Silva, J. R. (2007). Light and confocal microscopic observations of adult Schistosoma mansoni from mice fed on a high-fat diet. Journal of Helminthology 81, 361–368.CrossRefGoogle ScholarPubMed
Neves, R. H., Machado-Silva, J. R., Pelajo-Machado, M., Oliveira, S. A., Coutinho, E. M., Lenzi, H. L. and Gomes, D. C. (2001). Morphological aspects of Schistosoma mansoni adult worms isolated from nourished and undernourished mice: a comparative analysis by confocal laser scanning microscopy. Memórias do Instituto Oswaldo Cruz 96, 1013–1016.CrossRefGoogle ScholarPubMed
Nishimura, S., Manabe, I., Nagasaki, M., Eto, K., Yamashita, H., Ohsugi, M., Otsu, M., Hara, K., Ueki, K., Sugiura, S., Yoshimura, K., Kadowaki, T. and Nagai, R. (2009). CD8+ effector T cells contribute to macrophage recruitment and adipose tissue inflammation in obesity. Nature Medicine 15, 914–920.CrossRefGoogle ScholarPubMed
Nyindo, M. and Farah, I. O. (1999). The baboon as a non-human primate model of human schistosome infection. Parasitology Today 15, 478–82.CrossRefGoogle ScholarPubMed
Paraense, W. L. and Corrêa, L. R. (1989). A potential vector of Schistosoma mansoni in Uruguay. Memórias do Instituto Oswaldo Cruz 84, 281–288.CrossRefGoogle ScholarPubMed
Park, S. W., Chen, S. W., Kim, M., Brown, K. M., Kolls, J. K., D'Agati, V. D. and Lee, H. T. (2011). Cytokines induce small intestine and liver injury after renal ischemia or nephrectomy. Laboratory Investigation 91, 63–84.CrossRefGoogle ScholarPubMed
Platt, T. R. and Brooks, D. R. (1997). Evolution of the schistosomes (Digenea: Schistosomatoidea): the origin of dioecy and colonization of the venous system. Journal of Parasitology 83, 1035–1044.CrossRefGoogle ScholarPubMed
Rocha, R. L., Rocha, M. O., Pedroso, E. R., Colosimo, E. A. and Coelho, P. M. (1995). Egg excretion in the initial phase of experimental murine schistosomiasis mansoni: stability and association with worm burden. Revista do Instituto de Medicina Tropical de São Paulo 37, 325–329.CrossRefGoogle ScholarPubMed
Rumjanek, F. D. and Simpson, A. J. (1980). The incorporation and utilization of radiolabelled lipids by adult Schistosoma mansoni in vitro. Molecular and Biochemical Parasitology 1, 31–44.CrossRefGoogle ScholarPubMed
Silva, L. M., Fernandes, A. L., Barbosa, A. Jr., Oliveira, I. R. and Andrade, Z. A. (2000). Significance of schistosomal granuloma modulation. Memórias do Instituto Oswaldo Cruz 95, 353–361.CrossRefGoogle ScholarPubMed
Siqueira, L. T., Ferraz, A. A., Campos, J. M., De Lima Filho, J. L., Albuquerque, M. C., de Lima Aires, A., Ribeiro, M. H., Cavalcanti, M. T., De Lima, B., Cavalcanti, C. and Ferraz, E. M. (2010). Analysis of plasma citrulline and intestinal morphometry in mice with hepatosplenic schistosomiasis. Surgical Infections 11, 419–426.CrossRefGoogle ScholarPubMed
Stanley, R. G., Jackson, C. L., Griffiths, K. and Doenhoff, M. J. (2009). Effects of Schistosoma mansoni worms and eggs on circulating cholesterol and liver lipids in mice. Atherosclerosis 207, 131–138.CrossRefGoogle ScholarPubMed
Stavitsky, A. B. (2004). Regulation of granulomatous inflammation in experimental models of schistosomiasis. Infection and Immunity 72, 1–12.CrossRefGoogle ScholarPubMed
Tallima, H. and El Ridi, R. (2005). Methyl-beta-Cyclodextrin treatment and filipin staining reveal the role of cholesterol in surface membrane antigen sequestration of Schistosoma mansoni and S. haematobium lung-stage larvae. The Journal of Parasitology 91, 720–725.CrossRefGoogle ScholarPubMed
Trobojević-Stanković, J. B., Milićević, N. M., Milosević, D. P., Despotović, N., Davidović, M., Erceg, P., Bojić, B., Bojić, D., Svorcan, P., Protić, M., Dapcević, B., Miljković, M. D. and Milićević, Z. (2010). Morphometric study of healthy jejunal and ileal mucosa in adult and aged subjects. Histology and Histopathology 25, 153–158.Google Scholar
Xu, H., Barnes, G. T., Yang, Q., Tan, G., Yang, D., Chou, C. J., Sole, J., Nichols, A., Ross, J. S., Tartaglia, L. A. and Chen, H. (2003). Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. The Journal of Clinical Investigation 112, 1821–1830.CrossRefGoogle Scholar
Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L. and Ferrante, A. W. Jr. (2003). Obesity is associated with macrophage accumulation in adipose tissue. The Journal of Clinical Investigation 112, 1796–1808.CrossRefGoogle ScholarPubMed
Winer, S., Chan, Y., Paltser, G., Truong, D., Tsui, H., Bahrami, J., Dorfman, R., Wang, Y., Zielenski, J., Mastronardi, F., Maezawa, Y., Drucker, D. J., Engleman, E., Winer, D. and Dosch, H. M. (2009). Normalization of obesity-associated insulin resistance through immunotherapy. Nature Medicine 15, 921–929.CrossRefGoogle ScholarPubMed