Case Report: Metarubricytosis in Two Atlantic Bottlenose Dolphin (Tursiops truncatus truncatus) Calves
IAAAM 2012
Leigh A. Clayton1; Jill Arnold1; Simon Long2; Joseph L. Mankowski2; Richard J. Montali2; Catherine A. Hadfield1; Diane E. Brown3
1National Aquarium Baltimore, Department of Animal Health, Baltimore, MD, USA; 2Department of Molecular and Comparative Pathobiology, School of Medicine, Johns Hopkins University, Baltimore, MD, USA; 3Department of Pathology and Center for Comparative Medicine, Massachusetts General Hospital, Boston, MA, USA

Abstract

Metarubricytes (nucleated red blood cells, nRBC) are the final nucleated stage of erythrogenesis in mammals. The erythrocyte nucleus is extruded prior to release from the bone marrow into circulation, and the number of nRBCs is generally low in healthy mammals. Causes for increased circulating nRBCs include response to anemia, hypoxia, other causes of bone marrow activation (e.g., severe infection), zinc toxicosis (Heinz-body hemolytic anemia), heat stroke, lead toxicity, non-functional or absent spleen, extramedullary hematopoiesis, and neoplasia. Species vary in their propensity for responsive metarubricytosis.

Two captive-born Atlantic bottlenose dolphin (Tursiops truncatus truncatus) calves, co-housed in an indoor artificial salt-water facility, died acutely within four days of each other. The calves had the same sire. The primiparous dams were paternal half siblings. Calf 1 (55-day-old male) had no ante-mortem clinical signs and was found dead during morning rounds. Calf 2 (73-day-old female) had progressive periodic tachypnea, reduced nursing activity, weakness, regurgitation, and hematuria over 12–18 hours. Medical intervention failed to stabilize the calf and she died approximately 6 hours later. Gross necropsy and histopathology findings supported cause of death as acute bronchopneumonia in calf 1, and renal and abdominal hemorrhage, presumably from trauma, in calf 2.

While the calves had different terminal disease processes, both exhibited increased ante-mortem erythropoiesis including marked circulating metarubricytosis, hepatic and splenic EMH, erythrophagocytosis, and increased bone marrow erythropoiesis on histopathological evaluation. Both calves had inflammatory leukograms. Calf 1 had leukocytosis with a left shift and 93 nRBC/100 WBC on a post-mortem blood sample. Calf 2 had leukopenia with a left shift, marked regenerative anemia (Hct 14%) with 26 nRBC/100 WBC and reticulocytosis. Erythroid morphologic changes in calf 2 were consistent with marked erythroid regeneration (anisocytosis, basophilic stippling, Howell-Jolly bodies, metarubricytes and earlier erythroid forms) with characteristics of hemolysis (spherocytosis, stomatocytosis). Bone marrow cytology in calf 2 showed a myeloid left shift with increased erythropoiesis and concurrent erythrodysplastic change.

Adequate published descriptions of hematology of neonatal bottlenose dolphin are lacking. Published references for juvenile and adult bottlenose dolphins (0–4 nRBC/100 WBC)1-4 may not be representative of neonates. Whether low numbers of nRBCs are common in neonatal dolphins has not been thoroughly reported; however, nRBCs may occur more frequently in bottlenose dolphins compared to other cetaceans,2 and adults in captivity may have slightly higher numbers than free ranging animals1,2. In addition to responsive erythropoiesis, metarubricytosis can occur with inflammatory disease,1,5 a potential contributing factor in these calves. While metarubricytosis can be associated with lead poisoning in mammals, animals at this facility have been historically negative for blood lead, so testing was not performed. Further review of neonatal, juvenile, and adult bottlenose dolphin hematology in health and disease is warranted, specifically to include enumeration of circulating metarubricytes. Blood film review is always recommended for sick animals, not only to enumerate nRBCs but also to determine left shift, polychromasia, and cellular morphological abnormalities. The neonatal bottlenose dolphin appears able to generate a vigorous nRBC response; determining the numerical nRBC range at various ages will facilitate accurate interpretation of hematological responses in these animals.

References

1.  Bossart GD, Reidarson TH, Dierauf LA, Duffield DA. Clinical pathology. In: Dierauf LA, Frances MD, eds. CRC Handbook of Marine Mammal Medicine, 2nd ed. Boca Raton, FL: CRC Press; 2001:383–436.

2.  Reidarson TH. Hematology of marine mammals. In: Weiss DJ, Wardrop KJ, eds. Schalm's Veterinary Hematology. 6th ed. Ames, IA: Wiley-Blackwell; 2010:950–957.

3.  Fair PA, Hulsey TC, Varela RA, Goldstein JD, Adams J, Zolman ES, Bossart GD. Hematology, serum biochemistry, and cytology findings from apparently healthy Atlantic bottlenose dolphins (Tursiops truncatus) inhabiting the estuarine waters of Charleston, South Carolina. Aquat Mamm. 2006;32:182–195.

4.  Goldstein JD, Reese E, Reif JS, Varela RA, McCulloch SD, Defran RH, Fair PA, Bossart GD. Hematologic, biochemical, and cytology findings from apparently healthy Atlantic bottlenose dolphins (Tursiops truncatus) inhabiting the Indian River Lagoon, Florida, USA. J Wildlife Dis. 2006;42:447–454.

5.  Townsend FI Jr, Petro S. Significant panhypoproteinemia and regenerative anemia secondary to duodenitis in rough-toothed dolphins (Steno bredanensis). IAAAM 29th Annual Conference Proceedings, San Diego, CA; 1998:164.

  

Speaker Information
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Leigh A. Clayton
National Aquarium Baltimore
Department of Animal Health
Baltimore, MD, USA


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