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Thromboelastography values in Hispaniolan Amazon parrots (Amazona ventvalis): a pilot study.

Abstract: Thromboelastography (TEG) provides a global assessment of coagulation, including the rate of clot initiation, clot kinetics, achievement of maximum clot strength, and fibrinolysis. Thromboelastography (TEG) is used with increasing frequency in the field of veterinary medicine, although its usefulness in avian species has not been adequately explored. The purpose of this preliminary study was to assess the applicability of TEG in psittacine birds. Kaolin-activated TEG was used to analyze citrated whole blood collected routinely from 8 healthy adult Hispaniolan Amazon parrots (Amazona ventralis). The minimum and maximum TEG values obtained included time to clot initiation (2.6-15 minutes), clot formation time (4.3-20.8 minutes), [alpha] angle (12.7[degrees]- 47.9[degrees]), maximum amplitude of clot strength (26.3-46.2 mm), and percentage of lysis 30 minutes after achievement of maximum amplitude (0%--5.3%). The TEG values demonstrated comparative hypocoagulability relative to published values in canine and feline species. Differences may be explained by either the in vitro temperature at which TEG is standardly performed or the method of activation used in this study. Although TEG may have significant advantages over traditional coagulation tests, including lack of need for species-specific reagents, further evaluation is required in a variety of avian species and while exploring various TEG methodologies before this technology can be recommended for use in clinical cases.

Key words: coagulation, thromboelastography, avian, Hispaniolan Amazon parrot, Amazona ventralis


Several coagulopathies have been described in avian species, the most common being rodenticide toxicosis, (1-6) fatty liver disease of chickens, (7) hemorrhagic disease in canaries (Serinus canarius), (8) and conure bleeding syndrome. (6,9) In addition, infectious diseases, metabolic derangements (such as hepatopathy), neoplasia, and vasculitis can induce coagulopathies similar to those identified in domestic animals. (6,10-12)

Most research on avian coagulation has focused on chickens because of the economic importance of this species. (6,13) Classically, coagulation has been described as including the extrinsic, intrinsic, and common pathways, although the intrinsic branch of coagulation appears to be lacking or reduced in avian species. (6,13-15) The current cell-based theory of hemostasis has offered a more integrated and functional in vivo view of the complex biochemical events that occur during coagulation in mammals, taking into account the effect of coagulation enzymes as well as platelets and leukocytes. (16) To date, there are no published studies addressing the applicability of the cell-based theory of hemostasis in avian species.


Current laboratory tests used to assess coagulation that are available to the avian practitioner include thrombocyte number estimation and measures of bleeding time and whole-blood clotting time. (6) The latter two methodologies are crude indicators of blood coagulation, and estimation of thrombocyte counts must be performed manually. (6) Other diagnostic tests used in dogs and cats have also been investigated in avian species but are not currently available commercially. For example, a test for prothrombin time, the major measure of the extrinsic arm of coagulation, has been developed for a variety of avian species. (13,17-23) Partial thromboplastin time, clotting factor concentrations, and Russell's viper venom test have also been investigated. (6,13,17-24) Although these tests may have diagnostic value, they typically require avian-specific reagents, which are commercially unavailable. The lack of standardized reagents and unfamiliarity with methodologies used in research create challenges for application of the data to clinical situations.

Thromboelastography (TEG) is available at many university and specialized diagnostic laboratories and provides a thorough assessment of hemostatic function. (25,26) The design of TEG is simple: an aliquot of blood is allowed to coagulate with or without addition of an activator, and a pin attached to a torsion wire is used to measure the forces associated with clotting as the sample container is finely tilted by 4[degrees]45'. Thromboelastography reports numerical values and generates a tracing of clotting forces (Fig 1). The reaction time is measured from the initiation of the test to the beginning of clot formation (represented graphically by a 2-mm divergence of the traced lines). The coagulation time is the interval from initial clot formation to achievement of predetermined clot strength (represented graphically by a typically 20-mm divergence of traced lines). The [alpha] angle is closely related to coagulation time and indicates the rapidity of fibrin cross-linking in the clot. The maximum amplitude is the peak rigidity manifested by the clot, or maximum clot strength, and amplitude 30 represents the clot strength 30 minutes after maximum amplitude is reached. The maximum amplitude and amplitude 30 are used to calculate 30% lysis, or a 30% reduction in clot strength, which represents fibrinolysis. Thus, TEG allows a global assessment of coagulation by measuring the forces associated with initial clot formation, speed of clot kinetics, clot strength, and fibrinolysis. (25,26)

Thromboelastography has been used for evaluation of coagulopathies in people, (25,26) dogs, (27-33) cats, (34) horses, (35-37) pigs, (38) and rhesus macaques. (39) To our knowledge, only one study has evaluated TEG in an avian species (chicken); however, that study did not outline the specific methodologies used. (17) For the veterinarian treating avian species, TEG may have several advantages over traditional tests of coagulation, including the ability to characterize both hypocoagulable and hypercoagulable states and the lack of need for avian-specific reagents.

The purpose of this study was to assess the applicability of TEG in a psittacine species and to report on values of kaolin-activated citrated whole blood TEG in healthy Hispaniolan Amazon parrots (Amazona ventralis). We hypothesized that TEG values in Elispaniolan Amazon parrots would be similar to other species in which this methodology has been studied.

Materials and Methods


Eight Hispaniolan Amazon parrots belonging to a research flock at the University of California, Davis, School of Veterinary Medicine were used in this study. The birds were housed in a single room in individual stainless-steel cages or in 61 X 58 X 66-cm hanging wire cages for 3 days before venipuncture. Before the study period, birds were housed in a group flight cage measuring 30 X 23 X 18 cm. All birds were fed a commercial pelleted diet (Zupreem Fruit Blend Flavor Diet, Zupreem Nutritional Products, Shawnee, KS, USA) and water was provided ad libitum. The birds were healthy based on history and physical examination findings. None of the birds had received medications or an anesthetic agent for at least 2 weeks before sample collection. The study followed the guidelines for care and use of research animals of the National Institutes of Health and was approved by the Institutional Animal Care and Use Committees of the University of California, Davis.

Sample collection

Three milliliters of blood were collected from the right jugular vein of each bird by using a 3-mL syringe and 25-gauge needle. The blood volume was equally divided among 3.2% trisodium citrate collection tubes (BD Vacutainer Plus Plastic Citrate tubes, Becton Dickinson, Franklin Lakes, NJ, USA), dipotassium EDTA pediatric collection tubes (Microtainer, Becton Dickinson), and lithium-heparin pediatric collection tubes (Microtainer, Becton Dickinson). Blood placed in 3.2% trisodium citrate anticoagulant was mixed at a 9: 1 ratio of whole blood: 3.2% trisodium citrate.

Sample analysis

Blood samples stored in dipotassium EDTA were used to evaluate the complete blood count (CBC) within 2 hours of collection. A spun packed cell volume (PCV) was obtained by using a microhematocrit tube and centrifugation. A blood smear was made on arrival of the blood sample at the laboratory and was processed with a Romanowsky stain by using an automatic slide stainer (Aerospray Stat, Wescor, Logan, UT, USA) then counterstained in Giemsa stain solution (EMD Chemicals, Gibbstown, NJ, USA). A 200-cell manual differential count and a hemacytometer white blood cell count using the Natt and Herricks procedure were performed by the same technologist for all samples. Thrombocyte counts in the smear were subjectively evaluated as decreased, adequate, or increased. Total red blood cell counts and mean corpuscular volumes were reported from an automated analyzer (Advia 120 Hematology System, Global Siemens Healthcare, Erlangen, Germany).

Blood samples stored in lithium heparin were centrifuged within 2 hours of collection at 12 000g for 150 seconds (StatSpin VT Centrifuge, Iris International, Chatsworth, CA, USA); the plasma was decanted and plasma samples were analyzed (Roche Cobas C311 Chemistry Analyzer, Diamond Diagnostics, Holliston, MA, USA). Parameters included in the plasma biochemical profile were albumin, alkaline phosphatase, anion gap, aspartate aminotransferase (AST), bicarbonate, calcium, chloride, cholesterol, creatine kinase (CK), globulin, glucose, glutamate dehydrogenase, phosphorus, potassium, sodium, total protein, and uric acid.

Blood samples stored in 3.2% trisodium citrate were evaluated by TEG within 30 to 120 minutes of collection (TEG 500 Thromboelastograph, Haemoscope, Niles, 1L, USA) by using the kaolincitrate technique according to the manufacturer's recommendations. For each sample, 1 mL of citrated whole blood was added to a kaolin reagent and mixed by gentle inversion. Then, 340 [micro]L of the kaolin-citrated blood mixture was added to 20 [micro]L of prewarmed calcium chloride, and the sample was processed while maintained at the manufacturer's recommended temperature of 37[degrees]C. Preinstalled software (TEG Analytical Software Version 4.2.3., Haemonetics, Braintree, MA, USA) was used to report and calculate TEG variables and generate a tracing.

Statistical analysis

Because of the low sample volume, and according to the American Society of Veterinary Clinical Pathology guidelines on reference intervals, data evaluated for each parameter were the mean, median, standard deviation, and minimum and maximum values (Excel 2010 software, Microsoft, Redmond, WA, USA). Reference intervals were not computed, but all individual values were reported.


None of the birds exhibited clinical signs of abnormal bleeding during the study, nor were such abnormalities evident in their histories, and none of the birds exhibited excessive hematoma formation at the venipuncture site. The CBC values outside normal limits included a low PCV in 2 birds (46.5%; reference interval, 47%-60%), (40) mild leukopenia in 3 birds (range, 3.5-5.6 x [10.sup.3]/[micro]L; reference interval, 5.8-15.9 x [10.sup.3]/[micro]L), (40) mild heteropenia in 1 bird (1.68 x [10.sup.3]/[micro]L; reference interval, 2.3-7.4 x [10.sup.3]/[micro]L) 40 mild lymphopenia in 5 birds (range, 1.1-1.3 x [10.sup.3]/[micro]L; reference interval, 1.4-8.1 x [10.sup.3]/[micro]L), (40) and mild monocytopenia in 2 birds (range, 0.07-0.12 x [10.sup.3]/[micro]L; reference interval, 0.3-2.3 X [10.sup.3]/[micro]L). (40) Thrombocyte counts were adequate in all birds. Plasma biochemical values outside normal limits included mild hypophosphatemia in 3 birds (range, 2-2.7 mg/dL; reference interval, 3.1-5.5 mg/dL), (41) mild hypokalemia in 6 birds (range, 2.1-2.8 mEq/L; reference interval, 3.0-4.5 mEq/L), (41) mild hypernatremia in 6 birds (range, 153-157 mEq/L, reference interval, 136-152 mEq/L), (41) and mild AST elevation in 1 bird (434 U/L; reference interval, 130-350 U/L). (41) The TEG values from individual birds are presented in Table 1.


This study provides the first report of TEG values obtained in a psittacine species. Although TEG values were previously reported in chickens, (17) in that study TEG was performed on whole blood samples without use of an anticoagulant or a method of activation. Previous studies in cats and horses have demonstrated that different techniques used in TEG (eg, activation) result in different values. (34,36) Because the results of this study were obtained by kaolin activation of citrate anti-coagulated blood, they could not be directly compared with those from the previously reported study in chickens.

When compared with kaolin-activated TEG values obtained from citrated canine (33) and feline (34) whole blood samples, data obtained from birds in this study demonstrate several notable differences. In the small sample of birds presented here, the reaction time interval (2.6-15 minutes) was prolonged compared with canine (1.3-5.7 minutes) and feline (2.4-9.5 minutes) reference intervals. (33,34) This difference indicates a comparatively reduced speed of initial clot formation in birds relative to dogs and cats. The coagulation time interval (4.3 20.8 minutes) was prolonged compared with canine (1.3-5.7 minutes) and feline (1.2-3.9 minutes) reference intervals, (33,34) and the oc angle (12.7[degrees]-47.9[degrees]) was reduced relative to canine (36.9[degrees]-74.6[degrees]) and feline (45[degrees]-73.5[degrees]) reference intervals. (33,34) Taken together, these differences indicate a reduced speed of clot formation, or clot kinetics, in psittacine samples relative to their feline and canine counterparts. The reduced maximum amplitude (26.3-46.2 mm) relative to canine (42.9-67.9 mm) and feline (46.8-66.1 mm) reference intervals (33,34) indicate a comparatively reduced overall clot strength. The 30% lysis value (0%5.3%) was similar to feline (0%-9%) reference intervals (canine 30% lysis reference intervals were not available for comparison). (34) Overall, the findings of prolonged reaction and coagulation times coupled with a reduced [alpha] angle and maximum amplitude indicate that the blood of the birds used in this study was hypocoagulable relative to that of their canine and feline counterparts.

These observations need to be interpreted within the limitations of TEG. During TEG, samples are processed at a temperature of 37[degrees]C (99[degrees]F), which way not adequately replicate in vivo conditions of psittacine blood coagulation. Although appropriate for most mammals, 37[degrees]C is considerably lower than the core body temperature of psittacine species (38[degrees]C-42.5[degrees]C [100.4[degrees]F-108.5[degrees]F]). (42) Thus, values reported here could represent delayed or incomplete coagulation activation because of inconsistent enzymatic activation associated with a low processing temperature. Previous TEG-based studies have proven hypothermia-induced hypocoagulable states in humans, dogs, and pigs. (43-45) Investigating the effect of increased in vitro temperatures on the TEG results obtained from avian samples was outside the scope of this study but may be of interest in future studies.

In addition, the activation method used in this study may not have been ideal for evaluation of avian coagulation. Kaolin, a negatively-charged compound, activates coagulation through the intrinsic pathway. (46) Because avian species do not have a well-developed intrinsic pathway, (6,13-15) this activation method may have resulted in incomplete initiation of the coagulation cascade. Using other methods of activation, particularly by means of tissue factor, that initiate coagulation through the extrinsic pathway may be more appropriate for future research. (6) It is unknown at this time what effects the method of activation may have on avian TEG values; however, previous studies in domestic species have shown marked differences in TEG values obtained by using different methods of activation. (34-36)

The birds used in this study were considered clinically normal based on clinical history and physical examination findings. The CBC and electrolyte abnormalities were deemed mild and incidental when compared with laboratory- and institution-specific reference intervals. In addition, the CBC reference intervals (40) used were based on a low sample number; thus, differences should not be overinterpreted. A single bird (bird 2) exhibited a mildly elevated plasma AST activity without concomitant elevation in CK activity. Elevations in blood AST levels are caused by release of muscle or liver isoenzymes. (47) All plasma biochemical values associated with liver function in this bird (glucose, cholesterol, uric acid, albumin) were within reference intervals. Measurement of plasma bile acid concentration was not performed, although results may have provided additional information regarding a possible underlying hepatopathy. The plasma concentration of glutamate dehydrogenase (8 IU/L), another liver-specific enzyme, (47) was considered clinically normal in this bird, although reference intervals in Amazon parrots are not reported. None of the birds exhibited hypocalcemia, indicating that adequate calcium was available for coagulation. (6) Fibrinogen is a proinflammatory protein that is also a component in the common pathway of coagulation. (6) Although normal fibrinogen values have not been reported for Amazona species, fibrinogen concentrations reported for the study birds were similar to those previously reported for other avian species. (17,48,49)

Other variables associated with sample handling have been evaluated in conjunction with performance of TEG. Elemolysis has been shown to cause many TEG abnormalities. (35,50) In the current study, the risk of hemolysis was diminished by obtaining the blood sample by a single venipuncture from the right jugular vein, which was the largest accessible vessel. The hemolysis index is an indicator of free plasma hemoglobin reported by the biochemistry analyzer. (51) Six of the 8 birds had hemolysis index values sufficiently increased to create changes in biochemical values, such as AST and potassium, without inducing gross visual evidence of hemolysis. Study results have also shown that recent exercise can cause changes in TEG variables, including postexercise normalization of certain TEG parameters in dogs with hemophilia A and decreased coagulability in race horses. (31,35) However, the birds in this study did not experience overt exercise before venipuncture, and the periods of capture and restraint were short and uneventful.

The goals of this preliminary study were to evaluate the potential use of TEG in Hispaniolan Amazon parrots; therefore, values reported here should not be interpreted as reference intervals. Reference intervals should be determined from a minimum of 40 individuals, with a preference for at least 120 individuals, depending on the underlying distribution of data and the type of statistical analysis used. (52) Indeed, it is questionable whether the values reported here could be useful when compared to clinical cases in other avian species. Recent studies have shown that significant differences in TEG values are associated with various breeds of dogs. (30,53) If such marked differences are noted within a single species, extrapolation of TEG values from one avian species to another may be clinically unacceptable. In addition, marked differences in TEG values can occur with different operators, indicating the need to develop institution-specific reference ranges. (36)

Further research on the use of TEG in other avian species is required to determine if this diagnostic tool is clinically applicable. Future investigations should focus on modification of TEG methodology to more closely replicate in vivo temperatures, evaluation of various activation methods, and investigation in avian species at particular risk for specific coagulopathies, such as birds of prey with clinical or subclinical rodenticide toxicosis, conures with conure bleeding syndrome, and chickens with fatty liver syndrome.

Krista A. Keller, DVM, Dipl ACZM, David Sanchez-Migallon Guzman, LV, MS, Dipl ECZM (Avian, Small Mammal), Dipl ACZM, Mark J. Acierno, DVM, Dipl ACVIM, Hugues Beaufrere, DrMedVet, PhD, Dipl ABVP (Avian Practice), Dipl ACZM, Dipl ECZM (Avian), Kristin M. Sinclair, DVM, Dipl ABVP (Avian Practice), Sean D. Owens, DVM, Dipl ACVP, Joanne Paul-Murphy, DVM, Dipl ACZM, Dipl ACAW, and Thomas N. Tully, Jr., DVM, MS, Dipl ABVP (Avian Practice), Dipl ECZM (Avian)

From the William R. Pritchard Veterinary Medical Teaching Hospital (Keller, Guzman, Sinclair), Department of Veterinary Medicine and Epidemiology (Paul-Murphy), and Department of Pathology, Microbiology, and Immunology (Owens), University of California, Davis, One Shields Ave, Davis, CA 95616, USA; and the Department of Veterinary Clinical Sciences, Louisiana State University, School of Veterinary Medicine, Skip Bertman Dr, Baton Rouge, LA 70803, USA (Acierno, Beaufrere, Tully). Present address: Kensington Bird and Animal Hospital, 977 Farmington Ave, Kensington, CT 06037, USA (Sinclair); and Health Sciences Centre, Ontario Veterinary College, University of Guelph, 50 Stone Rd, Guelph, Ontario NIG 2W1, Canada (Beaufrere).


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Table 1. Thromboelastography values in healthy Hispaniolan Amazon
parrots (n = 8).

                                  Individual birds
values           1      2      3      4      5      6      7      8

R (min)          3      5.7   10.5    2.8    2.6   12      9     15
K (min)          6     10.9   12.9    4.3    5.8   20.8   14.3   11.2
[alpha] angle   41.8   24.4   19.3   47.9   44.5   12.7   18.1   19
MA (mm)         43.4   34.5   34.4   46.2   44.2   26.3   29.4   38.3
LY30 (%)         0      0      0      0      0      0.1    5.3    0

values          Mean (median)    SD      Min-max

R (min)          7.58 (7.35)     4.74    2.6-15
K (min)         10.78 (11.05)    5.44    4.3-20.8
[alpha] angle   28.46 (21.85)   13.93   12.7-47.9
MA (mm)         37.09 (36.4)     7.21   26.3-46.2
LY30 (%)         0.67 (0)        1.87      0-5.3

Abbreviations: R indicates reaction time; K, coagulation time; MA,
maximum amplitude; LY30, percentage of clot reduction 30 minutes
after MA is achieved; min, minimum; max, maximum; SD, standard
deviation; TEG, thromboelastography.
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Author:Keller, Krista A.; Guzman, David Sanchez-Migallon; Acierno, Mark J.; Beaufrere, Hugues; Sinclair, Kr
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Sep 1, 2015
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