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A key mechanism of pathogenesis in sheep infected with the nematode Teladorsagia circumcincta

Published online by Cambridge University Press:  28 February 2007

M. J. Stear ,
S. C. Bishop ,
N. G. Henderson  and
I. Scott
M. J. Stear*
Affiliation:
Department of Veterinary Clinical Studies, Glasgow University Veterinary School, Glasgow, UK
S. C. Bishop
Affiliation:
Department of Biometrical Genetics, Roslin Institute, Roslin, UK
N. G. Henderson
Affiliation:
Department of Veterinary Clinical Studies, Glasgow University Veterinary School, Glasgow, UK
I. Scott
Affiliation:
Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand
*
*Department of Veterinary Clinical Studies, Glasgow University Veterinary School, Bearsden Road, Glasgow G61 1QH, UK E-mail: [email protected] Fax: +44 (0)1419 427215
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Abstract

Infection of sheep with the abomasal nematode Teladorsagia circumcincta can cause a relative protein deficiency and reduce growth rate in growing lambs. A key event appears to be the destruction of junctions between epithelial cells. If the infection is heavy or prolonged, this leads to increased mucus production, hyperplasia, decreased acid production, gastrinemia, inappetance and pepsinogenemia. The severity of the infection depends upon the extent of concurrent infection, the nutritional status of the host and genetically controlled variation in the ability to mount protective immune responses.

Keywords

Teladorsagia circumcinctapathogenesissheepparasitic diseasesparasitic nematodes
Type
Research Article
Information
Animal Health Research Reviews , Volume 4 , Issue 1 , June 2003 , pp. 45 - 52
Copyright
Copyright © CAB International 2003

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References

Abbott, EM, Parkins, JJ and Holmes, PH (1984). Studies on the pathophysiology of chronic ovine haemonchosis in Merino and Scottish Blackface lambs. Parasitology 89: 585–596.CrossRefGoogle ScholarPubMed
Abbott, EM, Parkins, JJ and Holmes, PH (1986). The effect of dietary protein on the pathophysiology of acute ovine haemonchosis. Veterinary Parasitology 20: 291–306.CrossRefGoogle ScholarPubMed
Abbott, EM, Parkins, JJ and Holmes, PH (1988). Influence of dietary protein on the patho-physiology of haemonchosis in lambs given continuous infections. Research in Veterinary Science 45: 41–49.CrossRefGoogle Scholar
Albers, GAA, Gray, GD, Piper, LR, Barker, JSF, Lejambre, L and Barger, IA (1987). The genetics of resistance and resilience to Haemonchus contortus infection in young merino sheep. International Journal for Parasitology 17: 1355–1363.CrossRefGoogle ScholarPubMed
Armour, J, Jarrett, WFH and Jennings, FW (1966). Experimental Ostertagia circumcincta infections in sheep: development and pathogenesis of a single infection. American Journal of Veterinary Research 27: 1267–1278.Google Scholar
Bado, A, Levasseur, S, Attoub, S, Kermorgant, S, Laigneau, J-P, Bortoluzzi, M-N, Moizo, I, Lehy, T, Guerre-Millo, M, Le Marchand-Brustel, Y and Lewin, MJM (1998). The stomach is a source of leptin. Nature 394: 790–793.CrossRefGoogle ScholarPubMed
Baker, DG, Bruss, ML and Gershwin, LJ (1993). Abomasal interstitial fluid-to-blood concentrations gradient of pepsinogen in calves with type-1 and type-2 ostertagiosis. American Journal of Veterinary Research 54: 1294–1298.CrossRefGoogle ScholarPubMed
Balic, A, Bowles, VM and Mewson, ENT (2000). The immunology of gastrointestinal nematode infections in ruminants. Advances in Parasitology 45: 181–241.CrossRefGoogle ScholarPubMed
Beales, ILP (2000). Acid secretion in H. pylori associated enlarged fold gastritis. Gut 47: 313–315.CrossRefGoogle Scholar
Behm, CA and Ovington, KS (2000). The role of eosinophils in parasitic helminth infections: insights from genetically modified mice. Parasitology Today 16: 202–209.CrossRefGoogle ScholarPubMed
Bishop, SC and Stear, MJ (1999). Genetic and epidemiological relationships between productivity and disease resistance: gastro-intestinal parasite infection in growing lambs. Animal Science 69: 515–524.CrossRefGoogle Scholar
Bishop, SC and Stear, MJ (2000). Genetic control of resistance to gastrointestinal parasites in hill sheep. Report to MAFF on project LS2204.Google Scholar
Bishop, SC and Stear, MJ (2001). Genetic improvement of resistance to nematodes in terminal sire sheep. Report to LINK on project LK0610.Google Scholar
Bishop, SC, Bairden, K, McKellar, QA, Park, M and Stear, MJ (1996). Genetic parameters for faecal egg count following mixed, natural, predominantly Ostertagia circumcincta infection and relationships with liveweight in young lambs. Animal Science 63: 423–428.CrossRefGoogle Scholar
Bisset, SA, Morris, CA, McEwan, JA and Vlassoff, A (2001). Breeding sheep in New Zealand that are less reliant on anthelmintics to maintain health and productivity. New Zealand Veterinary Journal 49: 236–246.CrossRefGoogle ScholarPubMed
Bisset, SA, Vlassoff, A, Morris, CA, Southey, BR, Baker, RL and Parker, AGH (1992). Heritability of and genetic correlations among faecal egg counts and productivity traits in Romney sheep. New Zealand Journal of Agricultural Research 35: 51–58.CrossRefGoogle Scholar
Bouix, J, Krupinski, J, Rzepecki, R, Nowosad, B, Skrzyzala, I, Roborzynski, M, Fudalewicz-Niemczyk, W, Skalska, M, Malczewski, A and Gruner, L (1998). Genetic resistance to gastrointestinal nematode parasites in Polish long-wool sheep. International Journal for Parasitology 28: 1797–1804.CrossRefGoogle ScholarPubMed
Bown, MD, Poppi, DP and Sykes, AR (1991). The effect of post-ruminal infusion of protein or energy on the pathophysiology of Trichostrongylus colubriformis infection and body composition in lambs. Australian Journal of Agricultural Research 42: 253–267.Google Scholar
Coltman, DW, Pilkington, J, Kruuk, LEB, Wilson, K and Pemberton, JM (2001). Positive genetic correlation between parasite resistance and body size in a free-living ungulate population. Evolution 55: 2116–2125.Google Scholar
Coltman, DW, Wilson, K, Pilkington, JG, Stear, MJ and Pemberton, JM (2001). A microsatellite polymorphism in the gamma interferon gene is associated with resistance to gastrointestinal nematodes in a naturally-parasitized population of Soay sheep. Parasitology 122: 571–582.CrossRefGoogle Scholar
Coop, RL and Holmes, PH (1996). Nutrition and parasite interaction. International Journal for Parasitology 26: 951–962.CrossRefGoogle ScholarPubMed
Coop, RL and Kyriazakis, I (1999). Nutrition–parasite interaction. Veterinary Parasitology 84: 187–204.CrossRefGoogle ScholarPubMed
Coop, RL and Kyriazakis, I (2000). Influence of host nutrition on the development and consequences of parasitism in livestock. Parasitology Today 17: 325–330.Google Scholar
Coop, RL, Sykes, AR and Angus, KW (1982). The effect of three levels of Ostertagia circumcincta larvae on growth rate, food intake and body composition of growing lambs. Journal of Agricultural Science (Cambridge) 98: 247–255.CrossRefGoogle Scholar
Coop, RL, Graham, RB, Jackson, F, Wright, SE and Angus, KW (1985). Effect of experimental Ostertagia circumcincta infection on the performance of grazing lambs. Research in Veterinary Science 38: 282–287.CrossRefGoogle ScholarPubMed
Coop, RL, Huntley, JF and Smith, WD (1995). Effect of dietary-protein supplementation on the development of immunity to Ostertagia circumcincta in growing lambs. Research in Veterinary Science 59: 24–29.CrossRefGoogle ScholarPubMed
Douch, PGC, Green, RS, Morris, CA, Bisset, SA, Vlassoff, A, Baker, RL, Watson, TG, Hurford, AP and Wheeler, M (1995). Genetic and phenotypic relationships among anti-Trichostrongylus colubriformis antibody level, faecal egg count and body weight traits in grazing Romney sheep. Livestock Production Science 41: 121–132.CrossRefGoogle Scholar
Eady, SJ, Woolaston, RR, Lewer, RP, Raadsma, HW, Swan, AA and Ponzoni, RW (1998). Resistance to nematode parasites in Merino sheep: correlation with production traits. Australian Journal of Agricultural Science 49: 1201–1211.CrossRefGoogle Scholar
Eiler, H, Baber, W, Lyke, WA and Scholtens, R (1981). Inhibition of gastric hydrochloric acid secretions in the rat given Ostertagia ostertagi (a gastric parasite of cattle) extract. American Journal of Veterinary Research 42: 498–502.Google ScholarPubMed
Else, KJ and Finkelman, FD (1998). Intestinal nematode parasites, cytokines and effector mechanisms. International Journal for Parasitology 28: 1145–1158.CrossRefGoogle ScholarPubMed
Filmer, DB and McClure, TJ (1951) Absorption of anti-nematode antibodies from ewe's colostrum by the new-born lamb. Nature 168: 170.CrossRefGoogle ScholarPubMed
Finkelman, FD, Shea-Donohue, T, Goldhill, J, Sullivan, CA, Morris, SC, Madden, KB, Gause, WC and Urban, JF (1997). Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annual Review of Immunology 15: 505–533.CrossRefGoogle ScholarPubMed
Fox, MT (1997). Pathophysiology of infection with gastrointestinal nematodes in domestic ruminants: recent developments. Veterinary Parasitology 72: 285–308.CrossRefGoogle ScholarPubMed
Fox, MT, Gerrelli, D, Shivalkar, P and Jacobs, DE (1989). Effect of omeprazole treatment on feed intake and blood gastrin and pepsinogen levels in the calf. Research in Veterinary Science 46: 280–282.CrossRefGoogle ScholarPubMed
Gasbarre, LC, Leighton, EA and Sonstegard, T (2001). Role of the bovine immune system and genome in resistance to gastrointestinal nematodes. Veterinary Parasitology 98: 51–64.CrossRefGoogle ScholarPubMed
Grencis, RK (1997). Th2-mediated host protective immunity to intestinal nematode infections. Philosophical Transactions of the Royal Society of London Series B Biological Sciences 352: 1377–1384.CrossRefGoogle ScholarPubMed
Grenfell, BT, Wilson, K, Isham, VS, Boyd, HEG and Dietz, K (1996) Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode–ruminant interactions as a case study. Parasitology 111, s135-s151.Google Scholar
Gulland, FM, Albon, SD, Pemberton, JM, Moorcroft, PR and Clutton-Brock, TH (1993). Parasite-associated polymorphisms in a cyclic ungulate population. Proceedings of the Royal Society of London B Biological Sciences 254: 7–13.Google Scholar
Harris, PR, Mobley, HLT, Perez, GI, Blaser, MJ and Smith, PD (1996). Helicobacter pylori urease is a potent stimulus of mononuclear phagocyte activation and inflammatory cytokine production. Gastroenterology 111: 419–425.CrossRefGoogle ScholarPubMed
Holmes, PH (1987) Pathophysiology of parasitic infections. Parasitology 94: s29–s51.CrossRefGoogle ScholarPubMed
Heath, MF and Connon, RM (1991). Interaction of Ostertagia and Nematodirus species and the potential of serum fructosamine determination in monitoring gastrointestinal parasitism. Research in Veterinary Science 51: 322–326.CrossRefGoogle ScholarPubMed
Huntley, JF, Newlands, G and Miller, HRP (1984). The isolation and characterization of globule leukocytes—their derivation from mucosal mast-cells in parasitized sheep. Parasite Immunology 6: 371–390.CrossRefGoogle ScholarPubMed
Israf, DA, Coop, RL, Stevenson, LM, Jones, DG, Jackson, F, Jackson, E, Mackellar, A and Huntley, JF (1996). Dietary protein influences upon immunity to Nematodirus battus infection in lambs. Veterinary Parasitology 61: 273–286.CrossRefGoogle ScholarPubMed
Kambara, T, McFarlane, RG, Abell, TJ, McAnulty, RW and Sykes, AR (1993) The effect of age and dietary protein on immunity and resistance in lambs vaccinated with Trichostrongylus colubriformis. International Journal for Parasitology 23: 471–476.CrossRefGoogle ScholarPubMed
Knox, MR and Steel, JW (1999). The effects of urea supplementation on production and parasitological responses of sheep infected with Haemonchus contortus and Trichostrongylus colubriformis. Veterinary Parasitology 83: 123–135.CrossRefGoogle ScholarPubMed
Kyriazakis, I, Anderson, DH, Coop, RL and Jackson, F (1996). The pathophysiology and development of immunity during long-term subclinical infection with Trichostrongylus colubriformis of sheep receiving different nutritional treatments. Veterinary Parasitology 65: 41–54.CrossRefGoogle ScholarPubMed
Kyriazakis, I, Tolkamp, BJ and Hutchings, MR (1998). Towards a functional explanation for the occurrence of anorexia during parasitic infections. Animal Behaviour 56: 265–274.CrossRefGoogle ScholarPubMed
Larsen, JWA, Anderson, N, Vizard, AL, Anderson, GA and Hoste, H (1994). Diarrhoea in Merino ewes during winter: association with trichostrongylid larvae. Australian Veterinary Journal 71: 365–372.CrossRefGoogle ScholarPubMed
Lawrence, CE, Kennedy, MW and Garside, P (2001) Gut immunopathology in helminth infections—paradigm lost? In: Kennedy, MW and Harnett, W (editors). Parasitic Nematodes. Molecular Biology, Biochemistry and Immunology. Wallingford: CABI Publishing, pp 373–397.CrossRefGoogle Scholar
Lord, PCW, Wilmoth, LMG, Mizel, SB and McCall, CE (1991). Expression of interleukin-1α and β genes by human blood polymorphonuclear leukocytes. Journal of Clinical Investigation 87: 1312–1321.CrossRefGoogle Scholar
McAnulty, RW, Clark, VR and Sykes, AR (1982). The effect of clean pasture and anthelmintic frequency on growth rates of lambs on irrigated pasture. Proceedings of the New Zealand Society of Animal Production 42: 187–188.Google Scholar
McClure, SJ, Emery, DL, Bendixsen, T and Davey, RJ (1998). Attempts to generate immunity against Trichostrongylus colubriformis and Haemonchus contortus in young lambs by vaccination with viable parasites. International Journal for Parasitology 28: 739–746.CrossRefGoogle ScholarPubMed
McEwan, JC, Mason, P, Baker, RL, Clarke, JN, Hickey, SM and Turner, K (1992). Effect of selection for productive traits on internal parasite resistance in sheep. Proceedings of the New Zealand Society of Animal Production 52: 53–56.Google Scholar
McEwan, JC, Dodds, KG, Greer, GJ, Bain, WE, Duncan, SJ, Wheeler, R, Knowler, KJ, Reid, PJ, Green, RS and Douch, PGC (1995). Genetic estimates for parasite resistance traits in sheep and their correlations with production traits. New Zealand Journal of Zoology 22: pp 177.Google Scholar
McKellar, QA (1993). Interactions of Ostertagia species with their bovine and ovine hosts. International Journal for Parasitology 23: 451–462.CrossRefGoogle ScholarPubMed
McKellar, QA, Duncan, JL, Armour, J and McWilliam, P (1986). Response to transplanted adult Ostertagia ostertagi in calves. Research in Veterinary Science 40: 367–371.CrossRefGoogle ScholarPubMed
McKellar, QA, Duncan, JL, Armour, J, Lindsay, FEF and McWilliam, P (1987). Further studies on the response to transplanted adult Ostertagia ostertagi in calves. Research in Veterinary Science 42: 29–34.CrossRefGoogle ScholarPubMed
Miller, HRP (1996). Mucosal mast cells and the allergic response against nematode parasites. Veterinary Immunology and Immunopathology 54: 331–336.CrossRefGoogle ScholarPubMed
Miller, FM, Blair, HT, Reynolds, GW and Revell, DK (1998). The role of cysteine in the increased parasite susceptibility of Romney sheep selected for hogget fleece weight. Proceedings of the New Zealand Society of Animal Production 58: 153–158.Google Scholar
Murray, M, Miller, HRP and Jarrett, WFH (1968). The globule leukocyte and its derivation from the subepithelial mast cell. Laboratory Investigation 19: 222–234.Google Scholar
Murray, M, Jennings, FW and Armour, J (1970). Bovine ostertagiasis: structure, function and mode of differentiation of bovine gastric mucosa and kinetics of the worm loss. Research in Veterinary Science 11: 417–427.CrossRefGoogle ScholarPubMed
Parkins, JJ and Holmes, PH (1989). Effects of gastrointestinal helminth parasites on ruminant nutrition. Nutrition Research Reviews 2: 227–246.CrossRefGoogle ScholarPubMed
Parkins, JJ, Holmes, PH and Bremner, KC (1973). The pathophysiology of ovine ostertagiasis: some nitrogen balance and digestibility studies. Research in Veterinary Science 14: 21–28.CrossRefGoogle ScholarPubMed
Pernthaner, A, Cabaj, W, Stankiewicz, M, Davies, J and Maass, D (1997). Cytokine mRNA expression and IFN-gamma production of immunised nematode resistant and susceptible lambs against natural poly-generic challenge Acta Parasitologica 42: 180–186.Google Scholar
Playford, RJ (1995). Peptides and gastrointestinal mucosal integrity. Gut 37: 595–597.CrossRefGoogle ScholarPubMed
Schubert, ML (1997). Regulation of gastrin secretion. Current Opinion in Gastroenterology 13: 441–450.CrossRefGoogle Scholar
Schwaiger, F-W, Gostomski, D, Stear, MJ, Duncan, JL, McKellar, QA, Epplen, JT and Buitkamp, J (1995). An ovine major histocompatibility complex DRB1 allele is associated with low faecal egg counts following natural, predominantly Ostertagia circumcincta infection. International Journal for Parasitology 25: 815–822.CrossRefGoogle ScholarPubMed
Scott, I (1996). Biochemical and structural changes in response to abomasal nematode infections in ruminants. PhD thesis, University of Glasgow, UK.Google Scholar
Scott, I, Khalaf, S, Simcock, DC, Knight, CG, Reynolds, GW, Pomroy, WE and Simpson, HV (2000) A sequential study of the pathology associated with the infection of sheep with adult and larval Ostertagia circumcincta. Veterinary Parasitology 89: 79–84.CrossRefGoogle ScholarPubMed
Scudamore, CL, Thornton, EM, Mcmillan, L, Newlands, GFJ and Miller, HRP (1995). Release of the mucosal mast cell granule chymase, rat mast cell protease ii during anaphylaxis is associated with the rapid development of paracellular permeability to macromolecules in rat jejunum. Journal of Experimental Medicine 182: 1871–1881.CrossRefGoogle ScholarPubMed
Simpson, HV (2000). Pathophysiology of abomasal parasitism: is the host or parasite responsible? Veterinary Journal 160: 177–191.CrossRefGoogle ScholarPubMed
Simpson, HV, Simpson, BH, Simcock, DC, Reynolds, GW and Pomroy, WE (1999). Abomasal secretion in sheep receiving adult Ostertagia circumcincta that are prevented from contact with the mucosa. New Zealand Veterinary Journal 47: 20–24.CrossRefGoogle ScholarPubMed
Stear, MJ and Bishop, SC (1999) The curvilinear relationship between worm length and fecundity of Teladorsagia circumcincta. International Journal for Parasitology 29: 777–780.CrossRefGoogle ScholarPubMed
Stear, MJ, Bishop, SC, Doligalska, M, Duncan, JL, Holmes, PH, Irvine, J, McCririe, L, McKellar, QA, Sinski, E and Murray, M (1995). Regulation of egg production, worm burden, worm length and worm fecundity by host responses in sheep infected with Ostertagia circumcincta. Parasite Immunology 17: 643–652.CrossRefGoogle ScholarPubMed
Stear, MJ, Bairden, K, Bishop, SC, Buitkamp, J, Duncan, JL, Gettinby, G, McKellar, QA, Park, M, Parkins, JJ, Reid, SWJ, Strain, S and Murray, M (1997 a). The genetic basis of resistance to Ostertagia circumcincta in lambs. Veterinary Journal 154: 111–119.CrossRefGoogle ScholarPubMed
Stear, MJ, Bairden, K, Duncan, JL, Holmes, PH, McKellar, QA, Park, M, Strain, S and Murray, M (1997 b) How hosts control worms. Nature 389: 27.CrossRefGoogle ScholarPubMed
Stear, MJ, Bairden, K, McKellar, QA, Scott, I and Strain, S (1999). The relationship between the number and size of nematodes in the abomasum and the concentration of pepsinogen in ovine plasma. Research in Veterinary Science 67: 89–92.CrossRefGoogle ScholarPubMed
Stear, MJ, Bairden, K, Duncan, JL, Eckersall, PD, Fishwick, G, Graham, PA, Holmes, PH, McKellar, QA, Mitchell, S, Murray, M, Parkins, JJ and Wallace, DS (2000 a). The influence of relative resistance and urea-supplementation on deliberate infection with Teladorsagia circumcincta during winter. Veterinary Parasitology 94: 45–54.CrossRefGoogle ScholarPubMed
Stear, MJ, Mitchell, S, Strain, S, Bishop, SC and Mckellar, QA (2000 b). The influence of age on the variation among sheep in susceptibility to natural nematode infection. Veterinary Parasitology 89: 31–36.CrossRefGoogle ScholarPubMed
Stear, MJ, Eckersall, PD, Graham, PA, McKellar, QA, Mitchell, S and Bishop, SC (2001). Fructosamine concentration and resistance to natural, predominantly Teladorsagia circumcincta infection. Parasitology 123: 211–218.CrossRefGoogle ScholarPubMed
Stear, MJ, Henderson, NG, Kerr, A, McKellar, QA, Mitchell, S, Seeley, C and Bishop, SC (2002). Eosinophilia as a marker of resistance to Teladorsagia circumcincta in Scottish Blackface lambs. Parasitology 124: 545–552.CrossRefGoogle ScholarPubMed
Strain, SAJ and Stear, MJ (2001). The influence of protein supplementation on the immune response to Haemonchus contortus. Parasite Immunology 23: 527–531.CrossRefGoogle ScholarPubMed
Sykes, AR (1994). Parasitism and production in farm animals. Animal Production 59: 155–172.Google Scholar
Urquhart, GM, Armour, J, Duncan, JL, Dunn, AM and Jennings, FW (1987). Veterinary Parasitology. Avon: Longman Scientific and Technical.Google Scholar
van Houtert, MFJ, Barger, IA, Steel, JW, Windon, RG and Emery, DL (1995) Effects of dietary protein intake on responses of young sheep to infection with Trichostrongylus colubriformis. Veterinary Parasitology 56: 163–180.CrossRefGoogle ScholarPubMed
Wallace, DS, Bairden, K, Duncan, JL, Eckersall, PD, Fishwick, G, Gill, M, Holmes, PH, McKellar, QA, Murray, M, Parkins, JJ and Stear, MJ (1998) The influence of dietary supplementation with urea on resilience and resistance to infection with Haemonchus contortus. Parasitology 116: 67–72.CrossRefGoogle ScholarPubMed
Wallace, DS, Bairden, K, Duncan, JL, Eckersall, PD, Fishwick, G, Holmes, PH, McKellar, QA, Mitchell, S, Murray, M, Parkins, JJ and Stear, MJ (1999). The influence of increased feeding on the susceptibility of sheep to infection with Haemonchus contortus. Animal Science 69: 457–463.CrossRefGoogle Scholar
Williamson, JF, Blair, HT, Garrick, DJ, Pomroy, WE, Douch, PGC, Green, RS and Simpson, HV (1995). Parasitism and production in fleece-weight selected and control sheep. New Zealand Journal of Agricultural Research 38: 381–387.CrossRefGoogle Scholar
Yakoob, A, Holmes, PH and Armour, J (1983). Patho-physiology of gastrointestinal trichostrongyles in sheep—plasma losses and changes in plasma pepsinogen levels associated with parasite challenge of immune animals. Research in Veterinary Science 34: 305–309.CrossRefGoogle Scholar
Yasunaga, Y, Shinomura, Y, Kanayama, S, Higashimoto, Y, Yabu, M, Miyazaki, Y, Murayama, Y, Nishibayashi, H, Kitamura, S and Matsuzawa, Y (1997). Mucosal interleukin-1 beta production and acid secretion in enlarged fold gastritis. Alimentary Pharmacology and Therapeutics 11: 801–809.CrossRefGoogle ScholarPubMed