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.
Similar content being viewed by others
References
Akpavie SO, Pirie HM (1989) The globule leukocyte: morphology, origin, function and fate, a review. Anat Histol Embryol 18:87–95
Akpavie SO, Pirie HM (1990) Morphological, histochemical and ultrastructural features of the globule leukocyte of the bovine respiratory tract. Anat Histol Embryol 19:164–180
Akpavie SO, Pirie HM (1993) Globule leukocytes and bovine parasitic bronchitis. Anat Histol Embryol 22:144–150
Baert J, Frederix M (1985) Globule leukocytes in the respiratory epithelium of human upper airways: an ultrastructural study. Anat Rec 212:143–152
Baldwin F, Becker AB (1993) Bronchoalveolar eosinophilic cells in a canine model of asthma: two distinctive populations. Vet Pathol 30:97–103
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):57–71
Balic A, Bowles VM, Meeusen EN (2000) The immunology of gastrointestinal nematode infections in ruminants. Adv Parasitol 45:181–241
Balic A, Cunningham CP, Meeusen EN (2006) Eosinophil interactions with Haemonchus contortus larvae in the ovine gastrointestinal tract. Parasite Immunol 28:107–115
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
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 26:447–457
Buergelt CD, Hall C, McEntee K et al (1978) Pathological evaluation of paratuberculosis in naturally infected cattle. Vet Pathol 15:196–207
Cheville NF (2009) Ultrastructural pathology: the comparative cellular basis of disease, 2nd edn. Wiley-Blackwell, Ames
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):153–167
Coles S, Singh A, Eyre P (1987) Morphology of globule leukocyte from bovine bronchopulmonary lavage. Acta Anat 129:155–158
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
Enerbäck L, Pipkorn U, Olofsson A (1986) Intraepithelial migration of mucosal mast cells in hay fever: ultrastructural observations. Int Arch Allergy Appl Immunol 81:289–297
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
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 156:709–721
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 111:13–21
Friedman MM, Kaliner MA (1987) Symposium on mast cells and asthma. Am Rev. Resp Dis 135:1157–1164
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 130–199
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):188–196
Galdiero MR, Varricchi G, Sesf M et al (2017) Bidirectional mast cell-eosinophil interactions in inflammatory disorders and cancer. Front Med 4:103
Garry FB (1996) Indigestion in ruminants. In: Smith EP (ed) Large animal internal medicine, 2nd edn. Mosby, St. Louis, pp 824–858
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 9:467–478
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, Prieur DJ, Blanchard JL (1983) Prevalence, lesions, and differential diagnosis of Ollulanus tricuspis infection in cats. Vet Pathol 20:71–79
Horny HP, Sotlar K, Valent P (2011) Eosinophil, basophil, and mast cell infiltrates in the bone marrow: crossing the boundaries of diagnosis. J Hematop 4:101–111
Huntley JF (1992) Mast cells and basophils: a review of their heterogeneity and function. J Comp Pathol 107:349–372
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 6:371–390
Ikeda Y, Yamashita S (1993) Developmental changes in intestinal globule leukocytes of normal rats. Cell Tissue Res 273:447–455
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 220–246
Kobayashi K, Kawai Y (1995) Globule leukocytes in transitional cell hyperplasia and carcinomas of aged mice. Exp Anim 44:329–331
Konno A, Hashimoto Y, Kon Y et al (1995) Expression of gamma delta T cell receptor on caprine globule leukocytes. Vet Immunol Immunopathol 48:105–112
Kovalszki A, Weller PF (2014) Eosinophilia in mast cell disease. Immunol Allergy Clin N Am 34:357–364
Kovalszki A, Weller PF (2016) Eosinophilia. Prim Care 43:607–617
Lawrence JA (1977) The globule leucocyte in bovine schistosomiasis. Res Vet Sci 23:239–240
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 48:1320–1328
Maeda S, Tsuboi M, Sakai et al (2017) Endoscopic cytology for the diagnosis of chronic enteritis and intestinal lymphoma in digs. Vet Pathol 54:595–604
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 75:109–120
Miller HRP, Jarrett WFH (1971) Immune reactions in mucous membranes. I. Intestinal mast cell response during helminth expulsion in the rat. Immunology 20:277–288
Narama I, Ozaki K, Matsushima S et al (1999) Eosinophilic gastroenterocolitis in iron lactate-overloaded rats. Toxicol Pathol 27:318–324
Nikander S (1991) Origin, morphology, histochemistry and function of the mucosal mast cell and globule leukocyte. A review. Rangifer 11:3–11
Ohfuji S (2015) Emphysematous eosinophilic lymphangitis in the ruminal submucosa of cattle. Vet Pathol 52:1163–1166
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
Piliponsky AM, Pickholtz D, Gleich GJ et al (1999) Eosinophils activate mast cells to release histamine. Int Arch Allergy Immunol 118:202–203
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 116:531–536
Rahko T (1970) Globule leukocyte and mast cell in bile ducts of cattle naturally infected with liver flukes. Acta Vet Scand 11:219–217
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 14:245–253
Ramirez GA, Yacoub MR, Ripa M et al (2018) Eosinophils from physiology to disease: a comprehensive review. Biomed Res Int 2018:9095275 28 pages
Riedel RR, Schmitt A, de Jonge JPA et al (1990) Gastrointestinal type 1 hypersensitivity to azathioprine. Klin Wochenschr 68:50–52
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
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 41:37
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
Snider TG III, Williams JC, Knox JW et al (1988) Sequential histopathologic changes of typeI, pre-typeIIand type IIostertagiasis in cattle. Vet Parasitol 27:169–179
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 79:940–945
Stear MJ, Park M, Bishop SC (1996) The key components of resistance to Ostertagia circumcincta in lambs. Parasitol Today 12:438–441
Stone KD, Prussin C, Metcalfe DD (2010) IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol 125(2 Suppl):S73–S80
Stromberg BE, Gasbarre LC, Waite A et al (2012) Cooperia punctate: effect on cattle productivity? Vet Parasitol 183:284–291
Sutherland I, Scott I (2010) Gastrointestinal nematodes of sheep and cattle. Wiley-Blackwell, West Sussex
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
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 178:107–118
van Kruiningen HJ (1988) Morphologic considerations in the interpretation of gastrointestinal disorders. Toxicol Pathol 16:110–117
Vogel P, Janke L, Gravano DG et al (2018) Globule leukocytes and other mast cells in the mouse intestine. Vet Pathol 55:76–97
Williams AR (2012) Short communication: some observations on the role of bradykinin in immunity to Teladorsagia circumcincta in sheep. J. Parasitol Res 2012:569287
Zhao C, Liu G, Li X et al (2018) Inflammatory mechanism of rumenitis in dairy cows with subacute ruminal acidosis. BMC Vet Res 14:135
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that he has no competing interests.
Informed consent
None.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ohfuji, S. Retrospective analysis of globule leukocytes in parasite-free rumens of cattle: a histopathological research with literature review. Comp Clin Pathol 29, 645–651 (2020). https://doi.org/10.1007/s00580-020-03101-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00580-020-03101-3