Skip to main content
Top
Published in: Comparative Clinical Pathology 3/2020

01-06-2020 | Original Article

Retrospective analysis of globule leukocytes in parasite-free rumens of cattle: a histopathological research with literature review

Author: Susumu Ohfuji

Published in: Comparative Clinical Pathology | Issue 3/2020

Login to get access

Abstract

Having previously been described by several researchers, an association of globule leukocytes with helminth infestation involving the gastrointestinal tracts has been well acknowledged in humans and animals; however, the appearance of globule leukocytes is less common in those disorders which are not associated with parasitism. It has been suggested that the appearance of globule leukocytes, which are probably derived from mast cells, may indicate a significant role in immune response. The present retrospective study of archived bovine cases with postmortem diagnosis of rumen disorder that was not associated with parasitism provides a histopathological description of the appearance of globule leukocytes, in connection with a review of relevant literature. Archival histopathological analysis of 20 adult Holstein-Friesian dairy cows (5–8 years of age) revealed six cows that showed eosinophilic inflammatory changes in the lamina propria and submucosa of the rumens. In addition to eosinophils, the rumens exhibited lesser numbers of 2 cell types: the mucosal epithelium was infiltrated by globule leukocytes; the underlying lamina propria and submucosa, by mast cells admixed with eosinophils. Less frequently, there were granular cells that probably exhibited intermediate cells between mast cells and globule leukocytes. Histochemical stains failed to reveal bacteria, parasites, protozoa, or fungi. It is likely that there was a close relationship between a triad of eosinophils, mast cells, and globule leukocytes in the lesional rumens. In the present six cattle, although they appeared at glance to be asymptomatic, histopathological features were suggestive of an immune reaction involving the rumens.
Literature
go back to reference Akpavie SO, Pirie HM (1989) The globule leukocyte: morphology, origin, function and fate, a review. Anat Histol Embryol 18:87–95PubMedCrossRef Akpavie SO, Pirie HM (1989) The globule leukocyte: morphology, origin, function and fate, a review. Anat Histol Embryol 18:87–95PubMedCrossRef
go back to reference Akpavie SO, Pirie HM (1990) Morphological, histochemical and ultrastructural features of the globule leukocyte of the bovine respiratory tract. Anat Histol Embryol 19:164–180PubMedCrossRef Akpavie SO, Pirie HM (1990) Morphological, histochemical and ultrastructural features of the globule leukocyte of the bovine respiratory tract. Anat Histol Embryol 19:164–180PubMedCrossRef
go back to reference Akpavie SO, Pirie HM (1993) Globule leukocytes and bovine parasitic bronchitis. Anat Histol Embryol 22:144–150PubMedCrossRef Akpavie SO, Pirie HM (1993) Globule leukocytes and bovine parasitic bronchitis. Anat Histol Embryol 22:144–150PubMedCrossRef
go back to reference Baert J, Frederix M (1985) Globule leukocytes in the respiratory epithelium of human upper airways: an ultrastructural study. Anat Rec 212:143–152PubMedCrossRef Baert J, Frederix M (1985) Globule leukocytes in the respiratory epithelium of human upper airways: an ultrastructural study. Anat Rec 212:143–152PubMedCrossRef
go back to reference Baldwin F, Becker AB (1993) Bronchoalveolar eosinophilic cells in a canine model of asthma: two distinctive populations. Vet Pathol 30:97–103PubMedCrossRef Baldwin F, Becker AB (1993) Bronchoalveolar eosinophilic cells in a canine model of asthma: two distinctive populations. Vet Pathol 30:97–103PubMedCrossRef
go back to reference Balemba OB, Mbassa GK, Assey RJ, Kahwa CK, Makundi AE, Hay-Schmidt A, Dantzer V, Semuguruka WD (2000) Lesions of the enteric nervous system and the possible role of mast cells in the pathogenic mechanisms of migration of schistosome eggs in the small intestine of cattle during schistosoma bovis infection. Vet Parasitol 90(1–2):57–71PubMedCrossRef Balemba OB, Mbassa GK, Assey RJ, Kahwa CK, Makundi AE, Hay-Schmidt A, Dantzer V, Semuguruka WD (2000) Lesions of the enteric nervous system and the possible role of mast cells in the pathogenic mechanisms of migration of schistosome eggs in the small intestine of cattle during schistosoma bovis infection. Vet Parasitol 90(1–2):57–71PubMedCrossRef
go back to reference Balic A, Bowles VM, Meeusen EN (2000) The immunology of gastrointestinal nematode infections in ruminants. Adv Parasitol 45:181–241PubMedCrossRef Balic A, Bowles VM, Meeusen EN (2000) The immunology of gastrointestinal nematode infections in ruminants. Adv Parasitol 45:181–241PubMedCrossRef
go back to reference Balic A, Cunningham CP, Meeusen EN (2006) Eosinophil interactions with Haemonchus contortus larvae in the ovine gastrointestinal tract. Parasite Immunol 28:107–115PubMedCrossRef Balic A, Cunningham CP, Meeusen EN (2006) Eosinophil interactions with Haemonchus contortus larvae in the ovine gastrointestinal tract. Parasite Immunol 28:107–115PubMedCrossRef
go back to reference Barker IK, Van Dreumel AA, Palmer N (1993) The alimental system. In: Jubb KVF, Kennedy PC, Palmer N (eds) Pathology of domestic animals, vol. 2, 4th edn. Academic Press, San Diego, pp 1–318 Barker IK, Van Dreumel AA, Palmer N (1993) The alimental system. In: Jubb KVF, Kennedy PC, Palmer N (eds) Pathology of domestic animals, vol. 2, 4th edn. Academic Press, San Diego, pp 1–318
go back to reference Bricarello PA, Gennari SM, Oliveira-Sequeira TC et al (2002) Response of Corriedale and Crioula Lanada sheep to artificial primary infection with Haemonchus contortus. Vet Res Commun 26:447–457PubMedCrossRef Bricarello PA, Gennari SM, Oliveira-Sequeira TC et al (2002) Response of Corriedale and Crioula Lanada sheep to artificial primary infection with Haemonchus contortus. Vet Res Commun 26:447–457PubMedCrossRef
go back to reference Buergelt CD, Hall C, McEntee K et al (1978) Pathological evaluation of paratuberculosis in naturally infected cattle. Vet Pathol 15:196–207PubMedCrossRef Buergelt CD, Hall C, McEntee K et al (1978) Pathological evaluation of paratuberculosis in naturally infected cattle. Vet Pathol 15:196–207PubMedCrossRef
go back to reference Cheville NF (2009) Ultrastructural pathology: the comparative cellular basis of disease, 2nd edn. Wiley-Blackwell, Ames Cheville NF (2009) Ultrastructural pathology: the comparative cellular basis of disease, 2nd edn. Wiley-Blackwell, Ames
go back to reference Claerebout E, Vercruysse J, Dorny P et al (1998) The effect of different infection levels on acquired resistance to gastrointestinal nematodes in artificially infected cattle. Vet Parasitol 75(2–3):153–167PubMedCrossRef Claerebout E, Vercruysse J, Dorny P et al (1998) The effect of different infection levels on acquired resistance to gastrointestinal nematodes in artificially infected cattle. Vet Parasitol 75(2–3):153–167PubMedCrossRef
go back to reference Coles S, Singh A, Eyre P (1987) Morphology of globule leukocyte from bovine bronchopulmonary lavage. Acta Anat 129:155–158PubMedCrossRef Coles S, Singh A, Eyre P (1987) Morphology of globule leukocyte from bovine bronchopulmonary lavage. Acta Anat 129:155–158PubMedCrossRef
go back to reference Džaja P, Beck A, Kiš G et al (2008) Dirofilaria repens infection in a dog in Croatia- a case report. Vet Archiv 78:521–527 Džaja P, Beck A, Kiš G et al (2008) Dirofilaria repens infection in a dog in Croatia- a case report. Vet Archiv 78:521–527
go back to reference Enerbäck L, Pipkorn U, Olofsson A (1986) Intraepithelial migration of mucosal mast cells in hay fever: ultrastructural observations. Int Arch Allergy Appl Immunol 81:289–297PubMedCrossRef Enerbäck L, Pipkorn U, Olofsson A (1986) Intraepithelial migration of mucosal mast cells in hay fever: ultrastructural observations. Int Arch Allergy Appl Immunol 81:289–297PubMedCrossRef
go back to reference Ergün E, Ergun L, Asti RN (2004) Histological studies on the globule leukocytes in the small intestine of sheep. Indian Vet J 81:553–557 Ergün E, Ergun L, Asti RN (2004) Histological studies on the globule leukocytes in the small intestine of sheep. Indian Vet J 81:553–557
go back to reference Esteves MI, Schrenzel MD, Marini RP et al (2000) Helicobacter pylori gastritis in cats with long-term natural infection as a model of human disease. Am J Pathol 156:709–721PubMedPubMedCentralCrossRef Esteves MI, Schrenzel MD, Marini RP et al (2000) Helicobacter pylori gastritis in cats with long-term natural infection as a model of human disease. Am J Pathol 156:709–721PubMedPubMedCentralCrossRef
go back to reference Fan L, Iseki S (1999) Immunohistochemical localization of vascular endothelial growth factor in the globule leukocyte/mucosal mast cell of the rat respiratory and digestive tracts. Histochem Cell Biol 111:13–21PubMedCrossRef Fan L, Iseki S (1999) Immunohistochemical localization of vascular endothelial growth factor in the globule leukocyte/mucosal mast cell of the rat respiratory and digestive tracts. Histochem Cell Biol 111:13–21PubMedCrossRef
go back to reference Friedman MM, Kaliner MA (1987) Symposium on mast cells and asthma. Am Rev. Resp Dis 135:1157–1164 Friedman MM, Kaliner MA (1987) Symposium on mast cells and asthma. Am Rev. Resp Dis 135:1157–1164
go back to reference Fubini S, Divers TJ (2008) Noninfectious diseases of the gastrointestinal tract. In: Divers TJ, Peek SF (eds) Rebhun’s diseases of dairy cattle. St. Louis, Saunders Elsevier, pp 130–199CrossRef Fubini S, Divers TJ (2008) Noninfectious diseases of the gastrointestinal tract. In: Divers TJ, Peek SF (eds) Rebhun’s diseases of dairy cattle. St. Louis, Saunders Elsevier, pp 130–199CrossRef
go back to reference Fuertes M, Perez V, Benavides J et al (2015) Pathological changes in cattle naturally infected by Calicophoron daubneyi adult flukes. Vet Parasitol 209(3–4):188–196PubMedCrossRef Fuertes M, Perez V, Benavides J et al (2015) Pathological changes in cattle naturally infected by Calicophoron daubneyi adult flukes. Vet Parasitol 209(3–4):188–196PubMedCrossRef
go back to reference Galdiero MR, Varricchi G, Sesf M et al (2017) Bidirectional mast cell-eosinophil interactions in inflammatory disorders and cancer. Front Med 4:103CrossRef Galdiero MR, Varricchi G, Sesf M et al (2017) Bidirectional mast cell-eosinophil interactions in inflammatory disorders and cancer. Front Med 4:103CrossRef
go back to reference Garry FB (1996) Indigestion in ruminants. In: Smith EP (ed) Large animal internal medicine, 2nd edn. Mosby, St. Louis, pp 824–858 Garry FB (1996) Indigestion in ruminants. In: Smith EP (ed) Large animal internal medicine, 2nd edn. Mosby, St. Louis, pp 824–858
go back to reference Hajra S, Singh SV, Srivastava AK et al (2014) Pathobiology of spontaneous and experimental paratuberculosis (S-5 strain) in goats with special reference to early lesions. Asian J Anim Vet Adv 9:467–478CrossRef Hajra S, Singh SV, Srivastava AK et al (2014) Pathobiology of spontaneous and experimental paratuberculosis (S-5 strain) in goats with special reference to early lesions. Asian J Anim Vet Adv 9:467–478CrossRef
go back to reference Hargis AM (1995) Integumentary system. In: Carlton WWC, McGavin MD (eds) Thomson’s special veterinary pathology, 2nd edn. Mosby, St. Louis, pp 461–511 Hargis AM (1995) Integumentary system. In: Carlton WWC, McGavin MD (eds) Thomson’s special veterinary pathology, 2nd edn. Mosby, St. Louis, pp 461–511
go back to reference Hargis AM, Prieur DJ, Blanchard JL (1983) Prevalence, lesions, and differential diagnosis of Ollulanus tricuspis infection in cats. Vet Pathol 20:71–79PubMedCrossRef Hargis AM, Prieur DJ, Blanchard JL (1983) Prevalence, lesions, and differential diagnosis of Ollulanus tricuspis infection in cats. Vet Pathol 20:71–79PubMedCrossRef
go back to reference Horny HP, Sotlar K, Valent P (2011) Eosinophil, basophil, and mast cell infiltrates in the bone marrow: crossing the boundaries of diagnosis. J Hematop 4:101–111CrossRef Horny HP, Sotlar K, Valent P (2011) Eosinophil, basophil, and mast cell infiltrates in the bone marrow: crossing the boundaries of diagnosis. J Hematop 4:101–111CrossRef
go back to reference Huntley JF (1992) Mast cells and basophils: a review of their heterogeneity and function. J Comp Pathol 107:349–372PubMedCrossRef Huntley JF (1992) Mast cells and basophils: a review of their heterogeneity and function. J Comp Pathol 107:349–372PubMedCrossRef
go back to reference Huntley JF, Newlands G, Miller HRP (1984) The isolation and characterization of globule leukocytes: their derivation from mucosal mast cells in parasitized sheep. Parasite Immunol 6:371–390PubMedCrossRef Huntley JF, Newlands G, Miller HRP (1984) The isolation and characterization of globule leukocytes: their derivation from mucosal mast cells in parasitized sheep. Parasite Immunol 6:371–390PubMedCrossRef
go back to reference Ikeda Y, Yamashita S (1993) Developmental changes in intestinal globule leukocytes of normal rats. Cell Tissue Res 273:447–455PubMedCrossRef Ikeda Y, Yamashita S (1993) Developmental changes in intestinal globule leukocytes of normal rats. Cell Tissue Res 273:447–455PubMedCrossRef
go back to reference Jergens AE, Hostetter SJ, Andreasen CB (2016) Oral cavity, gastrointestinal tract, and associated structures. In: Raskin RE, Meyer DJ (eds) Canine and Feline Cytology: A Color Atlas and Interpretation Guide, 3rd edn. Elsevier, St. Louis, pp 220–246CrossRef Jergens AE, Hostetter SJ, Andreasen CB (2016) Oral cavity, gastrointestinal tract, and associated structures. In: Raskin RE, Meyer DJ (eds) Canine and Feline Cytology: A Color Atlas and Interpretation Guide, 3rd edn. Elsevier, St. Louis, pp 220–246CrossRef
go back to reference Kobayashi K, Kawai Y (1995) Globule leukocytes in transitional cell hyperplasia and carcinomas of aged mice. Exp Anim 44:329–331PubMedCrossRef Kobayashi K, Kawai Y (1995) Globule leukocytes in transitional cell hyperplasia and carcinomas of aged mice. Exp Anim 44:329–331PubMedCrossRef
go back to reference Konno A, Hashimoto Y, Kon Y et al (1995) Expression of gamma delta T cell receptor on caprine globule leukocytes. Vet Immunol Immunopathol 48:105–112PubMedCrossRef Konno A, Hashimoto Y, Kon Y et al (1995) Expression of gamma delta T cell receptor on caprine globule leukocytes. Vet Immunol Immunopathol 48:105–112PubMedCrossRef
go back to reference Kovalszki A, Weller PF (2014) Eosinophilia in mast cell disease. Immunol Allergy Clin N Am 34:357–364CrossRef Kovalszki A, Weller PF (2014) Eosinophilia in mast cell disease. Immunol Allergy Clin N Am 34:357–364CrossRef
go back to reference Lezmi GL, Galmiche-Rolland L, Rioux S et al (2016) Mast cells are associated with exacerbations and eosinophilia in children with severe asthma. Europ Resp J 48:1320–1328CrossRef Lezmi GL, Galmiche-Rolland L, Rioux S et al (2016) Mast cells are associated with exacerbations and eosinophilia in children with severe asthma. Europ Resp J 48:1320–1328CrossRef
go back to reference Maeda S, Tsuboi M, Sakai et al (2017) Endoscopic cytology for the diagnosis of chronic enteritis and intestinal lymphoma in digs. Vet Pathol 54:595–604PubMedCrossRef Maeda S, Tsuboi M, Sakai et al (2017) Endoscopic cytology for the diagnosis of chronic enteritis and intestinal lymphoma in digs. Vet Pathol 54:595–604PubMedCrossRef
go back to reference Mavenyengwa M, Mukaratirwa S, Obwolo M et al (2008) Bovine intestinal cellular responses following primary and challenge infections with Calicophoron microbothrium metacercariae. Onderstepoort J Vet Res 75:109–120PubMedCrossRef Mavenyengwa M, Mukaratirwa S, Obwolo M et al (2008) Bovine intestinal cellular responses following primary and challenge infections with Calicophoron microbothrium metacercariae. Onderstepoort J Vet Res 75:109–120PubMedCrossRef
go back to reference Miller HRP, Jarrett WFH (1971) Immune reactions in mucous membranes. I. Intestinal mast cell response during helminth expulsion in the rat. Immunology 20:277–288PubMedPubMedCentral Miller HRP, Jarrett WFH (1971) Immune reactions in mucous membranes. I. Intestinal mast cell response during helminth expulsion in the rat. Immunology 20:277–288PubMedPubMedCentral
go back to reference Narama I, Ozaki K, Matsushima S et al (1999) Eosinophilic gastroenterocolitis in iron lactate-overloaded rats. Toxicol Pathol 27:318–324PubMedCrossRef Narama I, Ozaki K, Matsushima S et al (1999) Eosinophilic gastroenterocolitis in iron lactate-overloaded rats. Toxicol Pathol 27:318–324PubMedCrossRef
go back to reference Nikander S (1991) Origin, morphology, histochemistry and function of the mucosal mast cell and globule leukocyte. A review. Rangifer 11:3–11CrossRef Nikander S (1991) Origin, morphology, histochemistry and function of the mucosal mast cell and globule leukocyte. A review. Rangifer 11:3–11CrossRef
go back to reference Ohfuji S (2015) Emphysematous eosinophilic lymphangitis in the ruminal submucosa of cattle. Vet Pathol 52:1163–1166PubMedCrossRef Ohfuji S (2015) Emphysematous eosinophilic lymphangitis in the ruminal submucosa of cattle. Vet Pathol 52:1163–1166PubMedCrossRef
go back to reference Pérez J, García PM, Hernández S et al (2004) Experimental haemonchosis in goats: effects of single and multiple infections in the host response. Vet Parasitol 27:333–342 Pérez J, García PM, Hernández S et al (2004) Experimental haemonchosis in goats: effects of single and multiple infections in the host response. Vet Parasitol 27:333–342
go back to reference Piliponsky AM, Pickholtz D, Gleich GJ et al (1999) Eosinophils activate mast cells to release histamine. Int Arch Allergy Immunol 118:202–203PubMedCrossRef Piliponsky AM, Pickholtz D, Gleich GJ et al (1999) Eosinophils activate mast cells to release histamine. Int Arch Allergy Immunol 118:202–203PubMedCrossRef
go back to reference Puxeddu I, Ribatti D, Crivellato E et al (2005) Mast cells and eosinophils: a novel link between inflammation and angiogenesis in allergic diseases. J Allergy Clin Immunol 116:531–536PubMedCrossRef Puxeddu I, Ribatti D, Crivellato E et al (2005) Mast cells and eosinophils: a novel link between inflammation and angiogenesis in allergic diseases. J Allergy Clin Immunol 116:531–536PubMedCrossRef
go back to reference Rahko T (1970) Globule leukocyte and mast cell in bile ducts of cattle naturally infected with liver flukes. Acta Vet Scand 11:219–217PubMed Rahko T (1970) Globule leukocyte and mast cell in bile ducts of cattle naturally infected with liver flukes. Acta Vet Scand 11:219–217PubMed
go back to reference Rahko T (1973) On the ultrastructure of mast cells and globule leucocytes in the common bile duct of cattle chronically infected with Fasciola hepatica. Acta Vet Scand 14:245–253PubMed Rahko T (1973) On the ultrastructure of mast cells and globule leucocytes in the common bile duct of cattle chronically infected with Fasciola hepatica. Acta Vet Scand 14:245–253PubMed
go back to reference Riedel RR, Schmitt A, de Jonge JPA et al (1990) Gastrointestinal type 1 hypersensitivity to azathioprine. Klin Wochenschr 68:50–52PubMedCrossRef Riedel RR, Schmitt A, de Jonge JPA et al (1990) Gastrointestinal type 1 hypersensitivity to azathioprine. Klin Wochenschr 68:50–52PubMedCrossRef
go back to reference Ritchey JW, Tompkins WAF (1998) Nonspecific immunity in the cat. In: Pastoret PP, Griebel P, Bazin H et al (eds) Handbook of veterinary immunology. Academic press, San Diego, pp 309–310 Ritchey JW, Tompkins WAF (1998) Nonspecific immunity in the cat. In: Pastoret PP, Griebel P, Bazin H et al (eds) Handbook of veterinary immunology. Academic press, San Diego, pp 309–310
go back to reference Robinson N, Piedrafita D, Snibson K et al (2010) Immune cell kinetics in the ovine abomasal mucosa following hyperimmunization and challenge with Haemonchus contortus. Vet Rec 41:37CrossRef Robinson N, Piedrafita D, Snibson K et al (2010) Immune cell kinetics in the ovine abomasal mucosa following hyperimmunization and challenge with Haemonchus contortus. Vet Rec 41:37CrossRef
go back to reference Rocha JF, Daoualibi Y, Lorenzo CD et al (2018) Emphysematous and granulomatous submucosal rumenitis in a feedlot Nellore steer. Acta Sci Vet 46(Suppl 1):266 Rocha JF, Daoualibi Y, Lorenzo CD et al (2018) Emphysematous and granulomatous submucosal rumenitis in a feedlot Nellore steer. Acta Sci Vet 46(Suppl 1):266
go back to reference Snider TG III, Williams JC, Knox JW et al (1988) Sequential histopathologic changes of typeI, pre-typeIIand type IIostertagiasis in cattle. Vet Parasitol 27:169–179PubMedCrossRef Snider TG III, Williams JC, Knox JW et al (1988) Sequential histopathologic changes of typeI, pre-typeIIand type IIostertagiasis in cattle. Vet Parasitol 27:169–179PubMedCrossRef
go back to reference Stankiewicz M, Jonas WE, Douch PCG et al (1993) Globule leukocytes in the lumen of the small intestine and the resistance status of sheep infected with parasitic nematodes. J Parasitol 79:940–945PubMedCrossRef Stankiewicz M, Jonas WE, Douch PCG et al (1993) Globule leukocytes in the lumen of the small intestine and the resistance status of sheep infected with parasitic nematodes. J Parasitol 79:940–945PubMedCrossRef
go back to reference Stear MJ, Park M, Bishop SC (1996) The key components of resistance to Ostertagia circumcincta in lambs. Parasitol Today 12:438–441PubMedCrossRef Stear MJ, Park M, Bishop SC (1996) The key components of resistance to Ostertagia circumcincta in lambs. Parasitol Today 12:438–441PubMedCrossRef
go back to reference Stromberg BE, Gasbarre LC, Waite A et al (2012) Cooperia punctate: effect on cattle productivity? Vet Parasitol 183:284–291PubMedCrossRef Stromberg BE, Gasbarre LC, Waite A et al (2012) Cooperia punctate: effect on cattle productivity? Vet Parasitol 183:284–291PubMedCrossRef
go back to reference Sutherland I, Scott I (2010) Gastrointestinal nematodes of sheep and cattle. Wiley-Blackwell, West Sussex Sutherland I, Scott I (2010) Gastrointestinal nematodes of sheep and cattle. Wiley-Blackwell, West Sussex
go back to reference Sweeney RW, Divers TJ, Gillette DM et al (1989) Mycotic omasitis and rumenitis as sequelae to sepsis in dairy cattle: six cases (1979–1986). J Am Vet Med Assoc 4:552–553 Sweeney RW, Divers TJ, Gillette DM et al (1989) Mycotic omasitis and rumenitis as sequelae to sepsis in dairy cattle: six cases (1979–1986). J Am Vet Med Assoc 4:552–553
go back to reference Tam EK, Calonico LD, McDonald DM (1988) Globule leukocytes and mast cells in the rat trachea: their number, distribution, and response to compound 48/80 and dexamethasone. Anat Embryol 178:107–118PubMedPubMedCentralCrossRef Tam EK, Calonico LD, McDonald DM (1988) Globule leukocytes and mast cells in the rat trachea: their number, distribution, and response to compound 48/80 and dexamethasone. Anat Embryol 178:107–118PubMedPubMedCentralCrossRef
go back to reference van Kruiningen HJ (1988) Morphologic considerations in the interpretation of gastrointestinal disorders. Toxicol Pathol 16:110–117PubMedCrossRef van Kruiningen HJ (1988) Morphologic considerations in the interpretation of gastrointestinal disorders. Toxicol Pathol 16:110–117PubMedCrossRef
go back to reference Vogel P, Janke L, Gravano DG et al (2018) Globule leukocytes and other mast cells in the mouse intestine. Vet Pathol 55:76–97PubMedCrossRef Vogel P, Janke L, Gravano DG et al (2018) Globule leukocytes and other mast cells in the mouse intestine. Vet Pathol 55:76–97PubMedCrossRef
go back to reference Williams AR (2012) Short communication: some observations on the role of bradykinin in immunity to Teladorsagia circumcincta in sheep. J. Parasitol Res 2012:569287 Williams AR (2012) Short communication: some observations on the role of bradykinin in immunity to Teladorsagia circumcincta in sheep. J. Parasitol Res 2012:569287
Metadata
Title
Retrospective analysis of globule leukocytes in parasite-free rumens of cattle: a histopathological research with literature review
Author
Susumu Ohfuji
Publication date
01-06-2020
Publisher
Springer London
Published in
Comparative Clinical Pathology / Issue 3/2020
Print ISSN: 1618-5641
Electronic ISSN: 1618-565X
DOI
https://doi.org/10.1007/s00580-020-03101-3

Other articles of this Issue 3/2020

Comparative Clinical Pathology 3/2020 Go to the issue