Pancreatic acinar atrophy in German shepherd dogs and rough-coated Collies. Etiopathogenesis, diagnosis and treatment. A review

Veterinary Quarterly

Volumn 26, Issue 2, 2004, Pages 61-75

  Wiberg, M E ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Autoimmune diseases; Dog diseases; Exocrine pancreatic insufficiency; German shepherd dogs; Hereditary diseases; Maldigestion; Pancreatic acinar atrophy; Pancreatic diseases; Review; Rough coated collies

Indexed keywords

ANTIBIOTIC AGENT; CIMETIDINE; COBALAMIN; ENZYME; HISTAMINE H2 RECEPTOR ANTAGONIST; METRONIDAZOLE; OXYTETRACYCLINE; TRIACYLGLYCEROL LIPASE; TYLOSIN;

ACINAR CELL; ANIMAL DISEASE; CLINICAL FEATURE; DIAGNOSTIC PROCEDURE; DIGESTIVE SYSTEM FUNCTION DISORDER; DOG; DRUG DEGRADATION; GENETIC PREDISPOSITION; IMMUNOPATHOGENESIS; NONHUMAN; PANCREAS ACINUS; PANCREAS DISEASE; PANCREAS EXOCRINE INSUFFICIENCY; PROGNOSIS; REVIEW;

ANIMALS; ATROPHY; DOG DISEASES; DOGS; PANCREAS; PANCREATITIS; PEDIGREE;

ANIMALIA; CANIS FAMILIARIS; PAA;

EID: 3042842291     PISSN: 01652176     EISSN: 18755941     Source Type: Journal    
DOI: 10.1080/01652176.2004.9695169     Document Type: Review

References (131)

1. Adrian TE. Plasma trypsin-like immunoreactivity in normal subjects and in patients with pancreatic diseases. Scandinavian Journal of Gastroenterology. Supplement 1980; 15: 15–20.
2. Anderson RC, Rackis JJ and Tallent WH. Biologically active substances in soy products. In: Soy protein and human nutrition, 1979. Edited by R.C. Anderson, J.J. Rackis and W.H. Tallent. Academic Press, New York. pp 209–233.
3. Andriulli A, Masoero G, Felder M, Vantini I, Petrillo M, Cavallini G, Bianchi Porro G, Dobrilla G and Verme G. Circulating trypsin-like immunoreactivity in chronic pancreatitis. Digestive Diseases and Sciences 1981; 26: 532–537.
4. Archer FJ, Kerr ME and Houston DM. Evaluation of three pancreas specific protein assays, TLI (trypsin-like immunoreactivity), PASP (pancreas specific protein) and CA 19-9 (glycoprotein) for use in the diagnosis of canine pancreatitis. Journal of Veterinary Medicine. Series A 1997; 44: 109–113.
5. Batt RM, Bush BM and Peters TJ. A new test for the diagnosis of exocrine pancreatic insufficiency in the dog. Journal of Small Animal Practice 1979; 20: 185–192.
6. Batt RM and Mann LC. Specificity of the BT-PABA test for the diagnosis of exocrine pancreatic insufficiency in the dog. Veterinary Record 1981; 108: 303–307.
7. Batt RM and Morgan JO. Role of serum folate and vitamin B12 consentrations in the differentiation of small intestinal abnormalities in the dog. Research in Veterinary Science 1982; 32: 17–22.
8. Batt RM. Bacterial overgrowth associated with a naturally occurring enteropathy in the German shepherd dog. Research in Veterinary Science 1983; 35: 42–46.
9. Batt RM, Horadagoda NU, McLean L, Morton DB and Simpson KW. Identification and characterization of a pancreatic intrinsic factor in the dog. American Journal of Physiology 1989; 256: 517–523.
10. Batt RM. Relationships between diet and malabsorption in dogs. Journal of Small Animal Practice 1990; 31: 489–493.
11. Beg linger C, Grossman MI and Solomon TR. Interaction between stimulants of exocrine pancreatic secretion in dogs. American Journal of Physiology 1984; 246: G173-G179.
12. Boari A, Williams DA and Famigli-Bergamini P. Observations on exocrine pancreatic insufficiency in a family of English Setter dogs. Journal of Small Animal Practice 1994; 35: 247–250.
13. Boari A, Williams DA and Bergamini PF. Diagnosis and management of concurrent exocrine pancreatic insufficiency (EPI) and diabetes mellitus (DM), in a young Rottweiler dog. European Journal of Comparative Gastroenterology 1997; 1: 29–31.
14. Boden G, Shore LS, Wilson N, Essa-Koumar N and Landor JR. Effects of pentobarbital anesthesia on serum secretin and exocrine pancreatic secretions. Hormone and Metabolic Research 1977; 9: 123–127.
15. Bonora G, Tomassetti P, Sternini C, Bagnoli L, Agostini D and Vezzadini P. Basal and stimulated serum immunoreactive trypsin in normal subjects. Scandinavian Journal of Gastroenterology. Supplement 1980; 62: 11–14.
16. Borgstrom A. The fate of intravenously injected trypsinogens in dogs. Scandinavian Journal of Gastroenterology 1981; 16: 281–287.
17. Burrows CF, Merritt AM and Chiapella AM. Determination of fecal fat and trypsin output in the evaluation of chronic canine diarrhea. Journal of the American Veterinary Medical Association 1979; 174: 62–66.
18. Carnaud C and Bach JF. Cellular basis of Trcell autoreactivity in autoimmune diseases. Immunologic Research 1993; 12: 131–148.
19. Chari ST and Singer MV. The problem of classification and staging of chronic pancreatitis. Proposals based on current knowledge of its natural history. Scandinavian Journal of Gastroenterology 1994; 29: 949–960.
20. Clark CH. Pancreatic atrophy and absorption failure in a Boxer. Journal of the American Veterinary Medical Association 1960; 136: 174–177.
21. Delles EK, Williard MD, Simpson RB, Fossum TW, Slater M, Kolp D, Lees GE, Helman R and Reinhart G. Comparison of species and numbers of bacteria in concurrently cultured samples of proximal small intestinal fluid and endoscopically obtained duodenal mucosa in dogs with intestinal bacterial overgrowth. American Journal of Veterinary Research 1994; 55: 957–964.
22. Dimagno EP, Go VLW and Summerskill WHJ. Relations between pancreatic enzyme outputs and malabsorption of severe pancreatic insufficiency. New England Journal of Medicine 1973; 288: 813–815.
23. Dominguez-Munoz JE, Hieronymus C, Sauerbruch T and Malfertheiner P. Fecal elastase test: Evaluation of a new non-invasive pancreatic function test. American Journal of Gastroenterology 1995; 90: 1834–1837.
24. Durie PR. Inherited causes of exocrine dysfunction. Canadian Journal of Gastroenterology 1997; 11: 145–152.
25. Dutta SK and Hlasko J. Dietary fiber in pancreatic disease: Effect of high fiber on fat malabsorption in insufficiency and in vitro study of the of dietary fiber with pancreatic enzymes. Journal of Clinical Nutrition 1985; 41: pancreatic pancreatic interaction American 517–525.
26. Eppig JJ and Leiter EH. Exocrine pancreatic insufficiency syndrome in CBA/J mice. I. Ultrastructural study. American Journal of Pathology 1977; 86: 17–30.
27. Fell BF, King TP and Davies N.T. Pancreatic atrophy in copper-deficient rats: Histochemical and ultrastructural evidence of a selective effect on acinar cells. Histochemical Journal 1982; 14: 665–680.
28. Florholmen J, Burhol PG and Jorde response and diurnal variation of trypsin-like immunorecativity in man. Scandinavian Journal of Gastroenterology 1984; 19: 622–625.
29. Freudiger U. Diseases of the exocrine pancreas in dogs. Kleintierpraxis 1971; 16: 201-228 (in German).
30. Geokas MC, Reidelberg R, O’Rourke M, Passaro E. Jr. and Largman C. Plasma pancreatic trypsinogens in chronic renal failure and after nephrectomy. American Journal of Physiology 1982; 242: G177–182.
31. Geyer S, Bibrack BR and Hänichen T. Clinics and pathology of pancreatic diseases in dogs. Kleintierpraxis 1968; 13: 17-24 (in German)
32. Glasbrenner B, Schön A, Klatt S, Beckh K and Adler G. Clinical evaluation of the faecal elastase test in the diagnosis and staging of chronic pancreatitis. European Journal of Gastroenterology and Hepatology 1996; 8: 1117–1120.
33. Gullo L, Ventrucci G, Bonora G, Gori G and Vezzadini P. Comparative study of serum trypsin levels and pancreatic exocrine function in chronic pancreatitis. Scandinavian Journal of Gastroenterology. Supplement 1980; 62: 27–28.
34. Hall EJ, Bond PM, McLean C, Batt RM and McLean L. A survey of the diagnosis and treatment of canine exocrine pancreatic insufficiency. Journal of Small Animal Practice 1991; 32: 613–619.
35. Hashimoto A, Kita I, Okada K and Fujimoto Y. Juvenile acinar atrophy of the pancreas of a dog. Veterinary Pathology 1979; 16: 74–80.
36. Hellman J and Loppnow H. Hyperplasia of somatostatin and pancreatic polypeptide immunoreactive cells in dogs with idiopathic atrophy of the exocrine pancreas. Journal of Veterinary Medicine. Series A 1991; 38: 80–89.
37. Herman L and Fitzgerald PJ. The degenerative changes in pancreatic acinar cells caused by dl-ethionine. Journal of Cell Biology 1962; 12: 277–296.
38. Hill FWG and Kidder DE. The estimation of daily fecal trypsin levels in dogs as an indicator of gross pancreatic exocrine insufficiency. Journal of Small Animal Practice 1970; 11: 191–195.
39. Hill FWG, Osborne AD and Kidder DE. Pancreatic degenerative atrophy in dogs. Journal of Comparative Pathology 1971; 81: 321–330.
40. Holroyd JB. Canine exocrine pancreatic disease. Journal of Small Animal Practice 1968; 9: 269–281.
41. Hänichen T and Minkus G. Retrospective study op the pathology of diseases of the exocrine pancreas in dogs and cats. Tierärztliche Umschau 1990; 45: 363-368 (in German).
42. Ito T, Nakano I, Koyanagi S. Miyahara T, Migita Y, Ogoshi K, Sakai H, Matsunaga S, Yasuda O, Sumii T and Nawata H. Autoimmune pancreatitis as a new clinical entity. Three cases of autoimmune pancreatitis with effective steroid therapy. Digestive Diseases and Sciences 1997; 42: 1458–1468.
43. Janeway CA, Travers P. Walport M and Capra DJ. In: Immunobiology: The immune system in health and disease, 4th ed., 1999. Edited by C.A. Janeway, P. Travers, M. Walport and D.J. Capra. Elsevier Science Ltd/Garland Publishing, London, England. pp. 262 -303 and 489–509.
44. Jo YH, Lee KY, Chang TM and Chey WH. Role of cholecystokinin in pancreatic bicarbonate secretion in dogs. Pancreas 1991; 6: 197–201.
45. Johnston KL. Small intestinal bacterial overgrowth. Veterinary Clinics of North America. Small Animal Practice 1999; 2: 523–550.
46. Jubb JC. Juvenile pancreatic atrophy (pancreatic hypoplasia) in dogs. Veterinary Medicine 1983: 1841–1842.
47. Keller ET. High serum trypsin-like immunoreactivity secondary to pancreatitis in a dog with exocrine pancreatic insufficiency. Journal of the American Veterinary Medical Association 1990; 196: 623–626.
48. Lankisch PG, Koop H, Seeling R and Seeling HP. Antinuclear and pancreatic cell antibodies in pancreatic diseases. Digestion 1981; 21: 65–68.
49. Lankisch PG. Function test in diagnosis of chronic pancreatitis. International Journal of Pancreatology 1993; 14: 9–20.
50. Leiter EH and Cunliffe-Beamer T. Exocrine pancreatic insufficiency in CBA/J mice. HI. Pathological and genetic analysis. Gastroenterology 1977; 73: 260–266.
51. Lendrum R and Walker G. Serum autoantibodies in human pancreatic disease. Gut 1975; 16: 365–371.
52. Loser C, Molgaard A and FOlsch UR. Faecal elastase: a novel, highly sensitive and specific tubeless pancreatic function test. Gut 1996; 39: 580–586.
53. Marvola M, Heinmäki J and Westermarck E. The fate of single-unit enteric-coated drug products in the stomach of a dog. Acta Pharmaceutica Fennica 1986; 95: 59–70.
54. Melgarejo T, Williams DA, O’Connell NC and Setchell KDR. Serum unconjugated bile acids as a test for intestinal bacterial overgrowth in dogs. Digestive Diseases and Sciences 2000; 45: 407–414.
55. Mizunuma T, Kawamura S and Kishino Y. Effects of injecting excess arginine on rat pancreas. Journal of Nutrition 1984; 114: 467–471.
56. Moeller ME, Steiner JM, Clark LA, Murphy KE, Famula TR, Williams DA, Stankovics ME and Vose AS. Inheritance of pancreatic acinar atrophy in German shpherd dogs. American Journal of Veterinary Research 2002; 10: 1429–1434.
57. Neiger R, Bornand Jaunin VB and Boujon CE. Exocrine pancreatic insufficiency combined with insulin-dependent diabetes mellitus in a juvenile German Shepherd Dog. Journal of Small Animal Practice 1996; 37: 344–349.
58. Nevalainen TJ and Janigan DT. Degeneration of mouse pancreatic acinar cells during fasting. Virchows Archiv, Abteilung B, Zellpathologie 1974; 15: 107–118.
59. Oates PS, Morgan RGH and Light AM. Cell death (apoptosis) during pancreatic involution after soya flour feeding in the rat. American Journal of Physiology 1986; 250: G9-G14.
60. Okazaki K, Uchida K, Ohana M, Nakase H, Uose S, Inai M, Matsushima Y, Katamura K, Ohmori K and Chiba T. Autoimmune-related pancreatitis is associated with autoantibodies and a Thl/Th2-type cellular immune response. Gastroenterology 2000; 118: 573–581.
61. Patten JR, Richards EA and Pope H 2nd. The effect of raw soybean on the pancreas of adult dog. Proceedings of the Society for Experimental Biology and Medicine 1971; 137: 59–63.
62. Pfister K, Rossi GL, Freudiger U and Bigler B. Morphological studies in dogs with chronic pancreatic insufficiency. Virchows Archiv A. Pathology, Anatomy and Histology 1980; 386: 91–105.
63. Pidgeon G. Effect of diet on exocrine pancreatic insufficiency in dogs. Journal of the American Veterinary Medical Association 1982; 181: 232–235.
64. Pidgeon G and Strombeck DR. Evaluation of treatment for pancreatic exocrine insufficiency in dogs with ligated pancreatic ducts. American Journal of Veterinary Research 1982; 43: 461–464.
65. Prentice DE, James RW and Wadsworth PF. Pancreatic atrophy in young Beagle dogs. Veterinary Pathology 1980; 17: 575–580.
66. Reidelberg RD, O’Rourke M, Durie PR, Geokas MC and Largman C. Effect of food intake and cholecystokinin on plasma trypsinogen levels in dogs. American Journal of Physiology 1984; 246: G543-G549.
67. Rimaila-Pärnänen E and Westermarck E. Pancreatic degenerative atrophy and chronic pancreatitis in dogs. A comparative study of 60 cases. Acta Veterinaria Scandinavica 1982; 23: 400–406.
68. Roep BO and De Vries RRP. T-lymphocytes and the pathogenesis of type 1 (insulin-dependent) diabetes mellitus. European Journal of Clinical Investigation 1992; 22: 697–711.
69. Roep BO. T-cell responses to autoantigens in IDDM: The search for the Holy Grail. Diabetes 1996; 45: 1147–1156.
70. Roitt I, Brostoff J and Male D. In: Immunology, 4th edition, 1998. Edited by I. Roitt, J. Brostoff and D. Male. Mosby, London.
71. Rose NR. Pathogenic mechanisms in autoimmune diseases. Clinical Immunology and Immunopatholology 1989; 53: S7-S16.
72. Rose NR and Bona C. Defining criteria for autoimmune diseases (Witebsky’s postulates revisited). Immunology Today 1993; 14: 426–430.
73. Ruddell WS, Mitchell CJ, Hamilton I, Leek JP and Kelleher J. Clinical value of serum immunoreactive trypsin concentration. British Medical Journal (Clinical Research Edition) 1981; 283: 1429–1432.
74. Rumenssen JJ, Marner B, Thorsgaard Pedersen T Permin H. Autoantibodies in chronic pancreatitis. Scandinavian Journal of Gastroenterology 1985; 20: 966–970.
75. Rutgers HC, Batt RM, Elwood CM and Lamport A. Small intestinal bacterial overgrowth in dogs with chronic intestinal disease. Journal of the American Veterinary Medical Association 1995; 206: 187.
76. Rutz GM, Steiner JM, Bauer JE and Williams DA. The effect of dietary medium chain triglycerides on dogs with exocrine pancreatic insufficiency. Journal of Veterinary Internal Medicine 2001; 15: 319 (abstract).
77. Räihd M and Westermarck E. The signs of pancreatic degenerative atrophy in dogs and the role of external factors in the etiology of the disease. Acta Veterinaria Scandinavica 1989; 30: 447–452.
78. Schattner A and Rager-Zisman B. Virus-induced autoimmunity. Reviews on Infectious Diseases 1990; 12: 204–222.
79. Sidhu SS and Tandon RK. The pathogenesis of chronic pancreatitis. Postgraduate Medical Journal 1995; 71: 67–70.
80. Simpson JW and Doxey DL. Evaluation of faecal analysis as an aid to the detection of exocrine pancreatic insufficiency. British Veterinary Journal 1988; 144: 174–178.
81. Simpson JW, Maskell IE, Quigg J and Markwell PJ. The long-term management of canine exocrine pancreatic insufficiency. Journal of Small Animal Practice 1994; 35: 133–138.
82. Simpson KW, Batt RM, McLean L and Morton DB. Circulating concentrations of trypsin-like immunoreactivity and activities of lipase and amylase after pancreatic duct ligation in dogs. American Journal of Veterinary Research 1989; 50: 629–632.
83. Simpson KW, Morton DB and Batt RM. Effect of exocrine pancreatic insufficiency on cobalamin absorption in dogs. American Journal of Veterinary Research 1989; 50: 1233–1236.
84. Simpson KW, Batt RM, Jones D and Morton DB. Effects of exocrine pancreatic insufficiency and replacement therapy on the bacterial flora of the duodenum in dogs. American Journal of Veterinary Research 1990; 51: 203–206.
85. Simpson KW, Johnstone JMS, Bell PRF, Morton DB and Batt RM. Pancreatic function following partial pancreatectomy and anastomosis of the pancreatic duct to the stomach or duodenum in dogs. Research in Veterinary Science 1992; 52: 97–104.
86. Simpson KW and Cobb MA. Investigation of the relationship of circulating anti-pancreatic antibodies to exocrine pancreatic insufficiency in dogs. European Journal of Comparative Gastroenterology 1998; 3: 37–42.
87. Sinha AX, Lopez MT and Mc Dewitt HO. Autoimmune diseases: The failure of self tolerance. Science 1990; 248: 1380–1388.
88. Spillmann T. Diagnosis of exocrine pancreatic insufficiency in dogs. Thesis, Giessen, 1995. 213 p. 89.
89. Spillmann T, Steiner JM, Williams DA and Failing K. Serum feline trypsin-like immunoreactivity following administration of ceruletide to healthy cats. American Journal of Veterinary Research 2000; 61: 925–927.
90. Spillmann T, Wiberg ME, Teigelkamp S, Failing K, Chaundhry YS, Kirsch A, Eifler R, Westermarck E, Eigenbrodt E and Sziegoleit A. Canine faecal pancreatic elastase (cE1) in dogs with clinical exocrine pancreatic insufficiency, normal dogs and dogs with chronic enteropathies. European Journal of Comparative Gastroenterology 2001; 2: 5–10.
91. Spillmann T, Wittker A, Teigelkamp S, Eim C, Burkhardt E, Eigenbrodt E and Sziegoleit A. An immunoassay for canine pancreatic elastase 1 as an indicator for exocrine pancreatic insufficiency in dogs. Journal of Veterinary Diagnostic Investigation 2001; 13: 468–474.
92. Steer ML, Waxman I and Freedman S. Chronic pancreatitis. New England Journal of Medicine 1995; 332: 1482–1490.
93. Stein J, Jung M, Sziegoleit A, Zeuzem S, Caspary WF and Lembcke B. Immunoreactive elastase 1: clinical evaluation of a new non-invasive test of pancreatic function. Clinical Chemistry 1996: 42: 222–226.
94. Steiner JM and Williams DA. Feline exocrine pancreatic disorders: Insufficiency, neoplasia, and uncommon conditions. Compendium on Continuing Education for the Practicing Veterinarian 1997; 19: 836–848.
95. Strad ley RP, Stern RJ and Heinhold NB. A method for the simultaneous evaluation of exocrine pancreatic function and intestinal absorptive function in dogs. American Journal of Veterinary Research 1979; 40: 1201–1205.
96. Säteri H. Investigations on the exocrine pancreatic function in dogs suffering from chronic exocrine pancreatic insufficiency. Acta Veterinaria Scandinavica 1975; 53: 1–86.
97. Tanaka T, Ichiba Y, Miura Y, Ito H and Dohi K. Canine model of chronic pancreatitis due to chronic ischemia. Digestion 1994; 55: 86–89.
98. Thordal-Christensen AA and Coffin DL. Pancreatic disease in the dog. Nordisk Veterinary Medicine 1956; 8: 89–114.
99. Tiscornia OM, Brasca AF, Hage G, Palasciano G, Devaux MA and Sarles H. The effects of atropine pentolinium, vagotomy and fluothane anaesthesia on canine exocrine pancreatic secretion. Biologie et Gastro-Enterologie 1972; 5: 249–256.
100. Walker NI, Winterford CM, Williamson RM and Kerr JF. Ethionine-induced atrophy of rat pancreas involves apoptosis of acinar cells. Pancreas 1993; 8: 443–449.
101. Washabau RI, Callan MB and Williams DA. Cholecystokinin secretion is preserved in canine pancreatic insufficiency. Journal of Veterinary Internal Medicine 1995; 9: 193 (abstract).
102. Watanabe S, Abe K, Anbo Y and Katoh H. Changes in the mouse exocrine pancreas after pancreatic duct ligation: A qualitative and quantitative histological study. Archives of Histology and Cytology 1995; 58: 365–374.
103. Weber W and Freudiger U. Heritability of the chronic exocrine pancreatic insufficiency in German shepherd dogs. Schweizer Archiv’ fiir Tierheilkunde 1977; 119: 257-263 (in German).
104. Westermarck E. Hereditary nature of canine pancreatic degenerative atrophy in the German shepherd dog. Acta Veterinaria Scandinavica 1980; 21: 389–394.
105. Westermarck E and Sandholm M. Faecal hydrolyse activity as determined by radial enzyme diffusion: A new method for detecting pancreatic dysfunction in the dog. Research in Veterinary Science 1980; 28: 341–346.
106. Westermarck E. The diagnosis of pancreatic degenerative atrophy in dogs. A practical method. Acta Veterinaria Scandinavica 1982; 23: 197–203.
107. Westermarck E. Treatment of pancreatic degenerative atrophy with raw pancreas homogenate and various enzyme preparations. Zentralblatt file Veterinarmedizin. Reihe A 1987; 34: 728–733.
108. Westermarck E, Pamilo P and Wiberg M. Pancreatic degenerative atrophy in the Collie breed: A hereditary disease. Journal of Veterinary Medicine 1989; 36: 549–554.
109. Westermarck E and Rimaila-Parnanen E. Mesenteric torsion in dogs with exocrine pancreatic insufficiency: 21 cases (1978-1987). Journal of the American Veterinary Medical Association 1989; 195: 1404–1406.
110. Westermarck E and Rimaila-Parnanen E. Two unusual cases ‘of canine exocrine pancreatic insufficiency. Journal of Small Animal Practice 1989; 30: 2–34.
111. Westermarck E, Wiberg M and Junttila J. Role of feeding in the treatment of the dogs with pancreatic degenerative atrophy. Acta Veterinaria Scandinavica 1990; 31: 325–331.
112. Westermarck E, Batt RM, Vaillant C and Wiberg M. Sequential study of pancreatic structure and function during development of pancreatic acinar atrophy in a German shepherd dog. American Journal of Veterinary Research 1993; 54: 1088–1094.
113. Westermarck E, Myllys V and Aho M. Effect of treatment on the jejunal and colonic bacterial flora of dogs with exocrine pancreatic insufficiency. Pancreas 1993; 8: 559–562.
114. Westermarck E, Junttila J and Wiberg M. The role of low dietary fat in the treatment of dogs with exocrine pancreatic insufficiency. American Journal of Veterinary Research 1995; 56: 600–605.
115. Vezzadini P, Gullo L, Sternini C, Bonora G, Ferri GL and Labo G. Serum immunoreactive trypsin after secretin stimulation in chronic pancreatitis. Scandinavian Journal of Gastroenterology. Supplement 1980; 62: 29–34.
116. Wiberg ME. Pancreatic acinar atrophy in German shepherd dogs and rough-coated Collies. Etiopathogenesis and response to long-term enzyme replacement treatment. Thesis, Helsinki, 2003. 130 p.
117. Wiberg ME, Lautala HM and Westermarck E. Response to long-term enzyme replacement treatment in dogs with exocrine pancreatic insufficiency. Journal of the American Veterinary Medical Association 1998: 213: 86–90.
118. Wiberg ME, Nurmi AK and Westermarck E. Serum trypsin-like immunoreactivity measurement for the diagnosis of subclinical exocrine pancreatic insufficiency in dogs. Journal of Veterinary Internal Medicine 1999; 13: 426–432.
119. Wiberg ME, Saari SAM and Westermarck E. Exocrine pancreatic atrophy in German shepherds and roughcoated Collies: An end-result of lymphocytic pancreatitis. Veterinary Pathology 1999; 36: 530–541.
120. Wiberg ME, Saari SAM, Westermarck E and Meri S. Cellular and humoral immune responses in atrophic lymphocytic pancreatitis in German shepherd dogs and rough-coated Collies. Veterinary Immunology and Immunopathology 2000; 76: 103–115.
121. Wiberg ME, Westermarck E, Spillmann T, Teigelkamp S and Eifler T. Canine faecal pancreatic elastase (cE1) for the diagnosis of subclinical exocrine pancreatic insufficiency in dogs. European Journal of Comparative Gastroenterology 2001; 2: 21–25.
122. Wiberg ME and Westermarck E. Subclinical exocrine pancreatic insufficiency in dogs. Journal of the American Veterinary Medical Association 2002; 220: 1183–1187.
123. Williams DA and Batt RM. Diagnosis of canine exocrine pancreatic insufficiency by the assay of serum trypsin-like immunoreactivity. Journal of Small Animal Practice 1983; 24: 583–588.
124. Williams DA and Batt RM. Exocrine pancreatic insufficiency diagnosed by radioimmunoassay of serum trypsin-like immunoreactivity in a dog with normal BT-PABA test result. Journal of the American Animal Hospital Association 1986; 22: 671–674.
125. Williams DA, Batt RM and Mclean L. Bacterial overgrowth in the duodenum of dogs with exocrine pancreatic insufficiency. Journal of the American Veterinary Medical Association 1987; 191: 201–206.
126. Williams DA and Batt RM. Sensitivity and specificity of radioimmunoassay of serum trypsin-like immunoreactivity for the diagnosis of canine exocrine pancreatic insufficiency. Journal of the American Veterinary Medical Association 1988; 192: 195–200.
127. Williams DA and Reed SD. Comparison of methods for assay of canine fecal proteolytic activity. Veterinary Clinical Pathology 1990; 19: 20–24.
128. Williams DA. Exocrine pancreatic disease. In: Textbook of Veterinary Internal Medicine: Diseases of the dog and cat, 5th edition, 2000. Edited by S.J. Ettinger and E.C. Feldman. W.B. Saunders, Philadelphia. pp. 1345–1367.
129. Williard MD, Simpson RB, Fossum TW, Cohen ND, Delles EK, Kolp DL, Carey DP and Reinhart GA. Characterization of naturally developing small intestinal bacterial overgrowth in 16 German shepherd dogs. Journal of the American Veterinary Medical Association 1994; 204: 1201–1206.
130. Yoshida K, Toki F, Takeuchi T, Watanabe SI, Shiratori K and Hayashi N. Chronic pancreatitis caused by an autoimmune abnormality. Proposal of concept of autoimmune pancreatitis. Digestive Diseases and Sciences 1995; 40: 1561–1568.
131. Zimmer JF and Todd SE. Further evaluation of bentiromide in the diagnosis of canine exocrine pancreatic insufficiency. Cornell Veterinarian 1985; 75: 426–440.