{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T01:20:24Z","timestamp":1790040024795,"version":"4.0.1"},"reference-count":66,"publisher":"American Animal Hospital Association","issue":"3","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2013]]},"abstract":"Juvenile cobalamin deficiency is a rare disease in border collies and its diagnosis requires a high level of clinical suspicion. The goal of this study was to increase awareness of this disease by describing the clinical and laboratory findings in four young border collies with inherited cobalamin deficiency. The median age of the dogs was 11.5 mo (range, 8\u201342 mo), and two of the four dogs were full siblings. Clinical signs included intermittent lethargy (n = 4), poor body condition (n = 4), odynophagia (n = 2), glossitis (n = 1), and bradyarrhythmia (n = 1). Pertinent laboratory abnormalities were mild to moderate normocytic nonregenerative anemia (n = 3), increased aspartate aminotransferase (AST) activity (n = 3), and mild proteinuria (n = 3). All of the dogs had serum cobalamin levels below the detection limit of the assay, marked methylmalonic aciduria, and hyperhomocysteinemia. Full clinical recovery was achieved in all dogs with regular parenteral cobalamin supplementation, and laboratory abnormalities resolved, except the proteinuria and elevated AST activity persisted. This case series demonstrates the diverse clinical picture of primary cobalamin deficiency in border collies. Young border collies presenting with ambiguous clinical signs should be screened for cobalamin deficiency.<\/jats:p>","DOI":"10.5326\/jaaha-ms-5867","type":"journal-article","created":{"date-parts":[[2013,3,27]],"date-time":"2013-03-27T21:56:58Z","timestamp":1364421418000},"page":"197-203","source":"Crossref","is-referenced-by-count":25,"title":["Clinical and Laboratory Findings in Border Collies with Presumed Hereditary Juvenile Cobalamin Deficiency"],"prefix":"10.5326","volume":"49","author":[{"given":"Sabina","family":"Lutz","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adrian C.","family":"Sewell","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claudia E.","family":"Reusch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter H.","family":"Kook","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"3280","reference":[{"issue":"4","key":"bib1","series-title":"Cobalamin. 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Intrinsic factor-mediated intestinal absorption of cobalamin in the dog. Am J Physiol1981;241(4):G294\u20139."},{"issue":"5","key":"bib4","series-title":"Blood","first-page":"1573","article-title":"The functional cobalamin (vitamin B12)-intrinsic factor receptor is a novel complex of cubilin and amnionless","volume":"103","author":"Fyfe","year":"2004","unstructured":"Fyfe\n JC\n , MadsenM, H\u00f8jrupP. The functional cobalamin (vitamin B12)-intrinsic factor receptor is a novel complex of cubilin and amnionless. Blood2004;103(5):1573\u20139."},{"issue":"1","key":"bib5","series-title":"Res Vet Sci","first-page":"17","article-title":"Role of serum folate and vitamin B12 concentrations in the differentiation of small intestinal abnormalities in the dog","volume":"32","author":"Batt","year":"1982","unstructured":"Batt\n RM\n , MorganJO. Role of serum folate and vitamin B12 concentrations in the differentiation of small intestinal abnormalities in the dog. Res Vet Sci1982;32(1):17\u201322."},{"key":"bib6","series-title":"J Am Anim Hosp Assoc","first-page":"533","article-title":"Inherited Selective Malabsorption of Vitamin-B12 in Giant Schnauzers","volume":"25","author":"Fyfe","year":"1989","unstructured":"Fyfe\n JC\n , JezykPF, GigerU. Inherited Selective Malabsorption of Vitamin-B12 in Giant Schnauzers. J Am Anim Hosp Assoc1989;25:533\u20139."},{"issue":"1","key":"bib7","series-title":"Pediatr Res","first-page":"24","article-title":"Inherited selective intestinal cobalamin malabsorption and cobalamin deficiency in dogs","volume":"29","author":"Fyfe","year":"1991","unstructured":"Fyfe\n JC\n , GigerU, HallCA. Inherited selective intestinal cobalamin malabsorption and cobalamin deficiency in dogs. 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J Hered2010;101(2):211\u20137."},{"issue":"5","key":"bib10","series-title":"J Am Anim Hosp Assoc","first-page":"392","article-title":"Cobalamin deficiency associated with erythroblastic anemia and methylmalonic aciduria in a border collie","volume":"35","author":"Morgan","year":"1999","unstructured":"Morgan\n LW\n , McConnellJ. Cobalamin deficiency associated with erythroblastic anemia and methylmalonic aciduria in a border collie. J Am Anim Hosp Assoc1999;35(5):392\u20135."},{"issue":"7","key":"bib11","series-title":"J Small Anim Pract","first-page":"339","article-title":"Hyperammonaemic encephalopathy secondary to selective cobalamin deficiency in a juvenile Border collie","volume":"46","author":"Battersby","year":"2005","unstructured":"Battersby\n IA\n , GigerU, HallEJ. Hyperammonaemic encephalopathy secondary to selective cobalamin deficiency in a juvenile Border collie. J Small Anim Pract2005;46(7):339\u201344."},{"issue":"2","key":"bib12","series-title":"Am J Hematol","first-page":"99","article-title":"Diagnosis of cobalamin deficiency: II. Relative sensitivities of serum cobalamin, methylmalonic acid, and total homocysteine concentrations","volume":"34","author":"Lindenbaum","year":"1990","unstructured":"Lindenbaum\n J\n , SavageDG, StablerSP. Diagnosis of cobalamin deficiency: II. Relative sensitivities of serum cobalamin, methylmalonic acid, and total homocysteine concentrations. Am J Hematol1990;34(2):99\u2013107."},{"issue":"8","key":"bib13","series-title":"Am J Vet Res","first-page":"1194","article-title":"Serum cobalamin, urinary methylmalonic acid and plasma homocysteine concentrations in healthy and cobalamin-deficient Border Collies","volume":"73","author":"Lutz","year":"2012","unstructured":"Lutz\n S\n , SewellAC, BiglerB. 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QJM2009;102(1):17\u201328."},{"issue":"2 pt 1","key":"bib21","series-title":"Ann Dermatol Venereol","first-page":"191","article-title":"is Signes buccaux r\u00e9v\u00e9lateurs d\u2019une carence en vitamine B12 avant l\u2019apparition d\u2019une an\u00e9mie [Clinical manifestations of the mouth revealing Vitamin B12 deficiency before the onset of anemia]","volume":"130","author":"P\u00e9tavy-Catala","year":"2003","unstructured":"P\u00e9tavy-Catala\n C\n , Font\u00e8sV, GironetN. is Signes buccaux r\u00e9v\u00e9lateurs d\u2019une carence en vitamine B12 avant l\u2019apparition d\u2019une an\u00e9mie [Clinical manifestations of the mouth revealing Vitamin B12 deficiency before the onset of anemia]. Ann Dermatol Venereol2003;130(2 pt 1):191\u20134 [in French]."},{"issue":"6","key":"bib22","series-title":"Pacing Clin Electrophysiol","first-page":"975","article-title":"Assessment of autonomic nervous system functions in patients with vitamin B12 deficiency by power spectral analysis of heart rate variability","volume":"23","author":"Aytemir","year":"2000","unstructured":"Aytemir\n K\n , Aks\u00f6yekS, B\u00fcy\u00fckasikY. Assessment of autonomic nervous system functions in patients with vitamin B12 deficiency by power spectral analysis of heart rate variability. Pacing Clin Electrophysiol2000;23(6):975\u20138."},{"issue":"11","key":"bib23","series-title":"J Pediatr Hematol Oncol","first-page":"715","article-title":"Imerslund-Grasbeck syndrome associated with recurrent aphthous stomatitis and defective neutrophil function","volume":"28","author":"Broides","year":"2006","unstructured":"Broides\n A\n , YerushalmiB, LevyR. Imerslund-Grasbeck syndrome associated with recurrent aphthous stomatitis and defective neutrophil function. J Pediatr Hematol Oncol2006;28(11):715\u20139."},{"issue":"4","key":"bib24","series-title":"Acta Hepatogastroenterol (Stuttg)","first-page":"313","article-title":"Functional and morphological abnormalities of the small intestinal mucosa in pernicious anemia\u2014a prospective study","volume":"25","author":"Arvanitakis","year":"1978","unstructured":"Arvanitakis\n C\n \n . Functional and morphological abnormalities of the small intestinal mucosa in pernicious anemia\u2014a prospective study. Acta Hepatogastroenterol (Stuttg)1978;25(4):313\u20138."},{"issue":"4","key":"bib25","series-title":"Clin Lab Med","first-page":"667","article-title":"Aminotransferases in disease","volume":"9","author":"Rej","year":"1989","unstructured":"Rej\n R\n \n . Aminotransferases in disease. Clin Lab Med1989;9(4):667\u201387."},{"issue":"6","key":"bib26","series-title":"Am J Kidney Dis","first-page":"1195","article-title":"Association between serum aspartate transaminase and homocysteine levels in hemodialysis patients","volume":"40","author":"Huang","year":"2002","unstructured":"Huang\n JW\n , YenCJ, PaiMF. Association between serum aspartate transaminase and homocysteine levels in hemodialysis patients. Am J Kidney Dis2002;40(6):1195\u2013201."},{"issue":"3","key":"bib27","series-title":"FASEB J","first-page":"512","article-title":"Homocysteine-betaine interactions in a murine model of 5,10-methylenetetrahydrofolate reductase deficiency","volume":"17","author":"Schwahn","year":"2003","unstructured":"Schwahn\n BC\n , ChenZ, LaryeaMD. Homocysteine-betaine interactions in a murine model of 5,10-methylenetetrahydrofolate reductase deficiency. FASEB J2003;17(3):512\u20134."},{"issue":"2","key":"bib28","series-title":"Hepatology","first-page":"442","article-title":"Role of TNF-alpha in ethanol-induced hyperhomocysteinemia and murine alcoholic liver injury","volume":"40","author":"Ji","year":"2004","unstructured":"Ji\n C\n , DengQ, KaplowitzN. Role of TNF-alpha in ethanol-induced hyperhomocysteinemia and murine alcoholic liver injury. Hepatology2004;40(2):442\u201351."},{"issue":"27","key":"bib29","series-title":"J Biol Chem","first-page":"17012","article-title":"Homocyst(e)ine decreases bioavailable nitric oxide by a mechanism involving glutathione peroxidase","volume":"272","author":"Upchurch","year":"1997","unstructured":"Upchurch\n GR\n Jr\n , WelchGN, FabianAJ. Homocyst(e)ine decreases bioavailable nitric oxide by a mechanism involving glutathione peroxidase. J Biol Chem1997;272(27):17012\u20137."},{"key":"bib30","article-title":"Cobalamin deficiency in a collie cross bedlington terrier","author":"Maguire","unstructured":"Maguire\n D\n , Solano-GallegoL, EnglishK. Cobalamin deficiency in a collie cross bedlington terrier. http:\/\/www.esvcp.org.Accessed July 15, 2011."},{"issue":"2","key":"bib31","series-title":"Clin Sci (Lond)","first-page":"139","article-title":"Distribution of endogenous cobalamin between the transcobalamins in various mammals","volume":"57","author":"Linnell","year":"1979","unstructured":"Linnell\n JC\n , CollingsL, DownMC. Distribution of endogenous cobalamin between the transcobalamins in various mammals. Clin Sci (Lond)1979;57(2):139\u201344."},{"issue":"3","key":"bib32","series-title":"Vet J","first-page":"306","article-title":"Association between serum cobalamin and methylmalonic acid concentrations in dogs","volume":"191","author":"Berghoff","year":"2012","unstructured":"Berghoff\n N\n , SuchodolskiJS, SteinerJM. Association between serum cobalamin and methylmalonic acid concentrations in dogs. Vet J2012;191(3):306\u201311."},{"issue":"11","key":"bib33","series-title":"Clin Chem","first-page":"2151","article-title":"Nonradioactive vitamin B12 absorption test evaluated in controls and in patients with inherited malabsorption of vitamin B12","volume":"51","author":"Bor","year":"2005","unstructured":"Bor\n MV\n , CetinM, Ayta\u00e7S. Nonradioactive vitamin B12 absorption test evaluated in controls and in patients with inherited malabsorption of vitamin B12. Clin Chem2005;51(11):2151\u20135."},{"issue":"4","key":"bib1","series-title":"Cobalamin. Crit Rev Clin Lab Sci","first-page":"247","volume":"33","author":"Markle","year":"1996","unstructured":"Markle\n HV\n \n . Cobalamin. Crit Rev Clin Lab Sci1996;33(4):247\u2013356."},{"key":"bib2","series-title":"Trans Assoc Am Physicians","first-page":"336","article-title":"Mechanism of enterohepatic circulation of vitamin B12: movement of vitamin B12 from bile R-binder to intrinsic factor due to the action of pancreatic trypsin","volume":"96","author":"Kanazawa","year":"1983","unstructured":"Kanazawa\n S\n , HerbertV. Mechanism of enterohepatic circulation of vitamin B12: movement of vitamin B12 from bile R-binder to intrinsic factor due to the action of pancreatic trypsin. Trans Assoc Am Physicians1983;96:336\u201344."},{"issue":"4","key":"bib3","series-title":"Am J Physiol","first-page":"G294","article-title":"Intrinsic factor-mediated intestinal absorption of cobalamin in the dog","volume":"241","author":"Marcoullis","year":"1981","unstructured":"Marcoullis\n G\n , RothenbergSP. Intrinsic factor-mediated intestinal absorption of cobalamin in the dog. 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Ann Dermatol Venereol2003;130(2 pt 1):191\u20134 [in French]."},{"issue":"6","key":"bib22","series-title":"Pacing Clin Electrophysiol","first-page":"975","article-title":"Assessment of autonomic nervous system functions in patients with vitamin B12 deficiency by power spectral analysis of heart rate variability","volume":"23","author":"Aytemir","year":"2000","unstructured":"Aytemir\n K\n , Aks\u00f6yekS, B\u00fcy\u00fckasikY. Assessment of autonomic nervous system functions in patients with vitamin B12 deficiency by power spectral analysis of heart rate variability. Pacing Clin Electrophysiol2000;23(6):975\u20138."},{"issue":"11","key":"bib23","series-title":"J Pediatr Hematol Oncol","first-page":"715","article-title":"Imerslund-Grasbeck syndrome associated with recurrent aphthous stomatitis and defective neutrophil function","volume":"28","author":"Broides","year":"2006","unstructured":"Broides\n A\n , YerushalmiB, LevyR. Imerslund-Grasbeck syndrome associated with recurrent aphthous stomatitis and defective neutrophil function. J Pediatr Hematol Oncol2006;28(11):715\u20139."},{"issue":"4","key":"bib24","series-title":"Acta Hepatogastroenterol (Stuttg)","first-page":"313","article-title":"Functional and morphological abnormalities of the small intestinal mucosa in pernicious anemia\u2014a prospective study","volume":"25","author":"Arvanitakis","year":"1978","unstructured":"Arvanitakis\n C\n \n . Functional and morphological abnormalities of the small intestinal mucosa in pernicious anemia\u2014a prospective study. Acta Hepatogastroenterol (Stuttg)1978;25(4):313\u20138."},{"issue":"4","key":"bib25","series-title":"Clin Lab Med","first-page":"667","article-title":"Aminotransferases in disease","volume":"9","author":"Rej","year":"1989","unstructured":"Rej\n R\n \n . Aminotransferases in disease. 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