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Hematologic and Plasma Biochemistry Reference Intervals of Healthy Adult Barn

Owls (Tyto alba)


Source: Avian Diseases, 58(2):228-231.
Published By: American Association of Avian Pathologists
DOI: http://dx.doi.org/10.1637/10715-111013-Reg.1
URL: http://www.bioone.org/doi/full/10.1637/10715-111013-Reg.1

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AVIAN DISEASES 58:228231, 2014

Hematologic and Plasma Biochemistry Reference Intervals of Healthy Adult


Barn Owls (Tyto alba)
Zoltan Szabo,AD Akos Klein,B and Csaba JakabC
A

Tai Wai Small Animal and Exotic Hospital, 75 Chik Shun Street, Tai Wai, Shatin, New Territories, Hong Kong
Department of Animal Ecology and Taxonomy, Faculty of Science, Eotvos Lorand University, H-1117, Pazmany P. setany 1/c.,
Budapest, Hungary
C
Faculty of Veterinary Science, Szent Istvan University, H-1078, Istvan u. 2., Budapest, Hungary
Received 15 November 2013; Accepted 7 January 2014; Published ahead of print 8 January 2014
SUMMARY. Hematologic and plasma biochemistry parameters of barn owls (Tyto alba) were studied in collaboration by the
Exotic Division of the Faculty of Veterinary Science of the Szent Istvan University and the Eotvos Lorand University, both in
Budapest, Hungary. Blood samples were taken from a total of 42 adult barn owls kept in zoos and bird repatriation stations. The
following quantitative and qualitative hematologic values were determined: packed cell volume, 46.2 6 4%; hemoglobin
concentration, 107 6 15 g/L; red blood cell count, 3.2 6 0.4 3 1012/L; white blood cell count, 13.7 6 2.7 3 109/L; heterophils,
56.5 6 11.5% (7.8 6 2 3109/L); lymphocytes, 40.3 6 10.9% (5.5 6 1.9 3 109/L); monocytes, 1.8 6 2.1% (0.3 6 0.3 3 109/
L); eosinophils, 1 6 1% (0.1 6 0.1 3 109/L); and basophils, 0.6 6 0.5% (0.1 6 0.1 3 109/L). The following plasma
biochemistry values also were determined: aspartate aminotransferase, 272 6 43 U/L; L-c-glutamyltransferase, 9.5 6 4.7 U/L;
lipase, 31.7 6 11.1 U/L; creatine kinase, 2228 6 578 U/L; lactate dehydrogenase, 1702 6 475 U/L; alkaline phosphatase, 358 6
197 U/L; amylase, 563 6 114 U/L; glutamate dehydrogenase, 7.5 6 2.5 U/L; total protein, 30.6 6 5.3 g/L; uric acid, 428 6
102 mmol/L; and bile acids, 43 6 18 mmol/L. These results provide reliable reference values for the clinical interpretation of
hematologic and plasma biochemistry results for the species.
RESUMEN. Intervalos de referencia hematologicas y de bioqumica plasmatica de lechuzas comunes adultas sanas (Tyto alba).
Se estudiaron los parametros hematologicos y de bioqumica plasmatica de lechuzas comunes o tambien llamadas de campanarios
(Tyto alba) con la colaboracion de la Division de Animales Exoticos de la Facultad de Ciencias Veterinarias de la Universidad Szent
Istvan y de la Universidad Eotvos Lorand, ambas localizadas en Budapest, Hungra. Las muestras de sangre fueron tomadas de un
total de 42 lechuzas adultas que se encontraban en zoologicos y en estaciones de refugio de aves. Se determinaron los siguientes
valores hematologicos cuantitativos y cualitativos: volumen de hematocrito, 46.2 6 4%; concentracion de hemoglobina, 107 6
15g/L; recuento de globulos rojos, 3.2 6 0.4 3 1012/L; recuento de globulos blancos, 13.7 6 2.7 3 109/L; heterofilos, 56.5 6
11.5% (7.8 6 2 3 109/L); linfocitos, 40.3 6 10.9% (5.5 6 1.9 3 109/L); monocitos, 1.8 6 2.1% (0.3 6 0.3 3 109/L);
eosinofilos, 1 6 1% (0.1 6 0.1 3 109/L) y basofilos, 0.6 6 0.5% (0.1 6 0.1 3 109/L). Tambien se determinaron los siguientes
valores bioqumicos plasmaticos: aspartato aminotransferasa, 272 6 43 U/L; L-c-glutamil transferasa, 9.5 6 4.7 U/L; lipasa, 31.7
6 11.1 U/L; quinasa de creatina, 2228 6 578 U/L; lactato deshidrogenasa, 1702 6 475 U/L; fosfatasa alcalina, 358 6 197 U/L;
amilasa, 563 6 114 U/L ; glutamato deshidrogenasa, 7.5 6 2.5 U/L; protena total, 30.6 6 5.3 g/L; acido urico, 428 6 102 mmol/
L y acidos biliares, 43 6 18 mmol/L. Estos resultados proporcionan valores de referencia confiables para la interpretacion clnica de
resultados hematologicos y de bioqumica plasmatica para dicha especie.
Key words: bird, barn owl, Tyto alba, hematology, biochemistry, blood, reference interval
Abbreviations: ALP 5 alkaline phosphatase; AST 5 aspartate aminotransferase; CK 5 creatine kinase; GGT 5 c-glutamyl
transpeptidase; GLDH 5 glutamate dehydrogenase; Hb 5 hemoglobin; LDH 5 lactate dehydrogenase; PCV 5 packed cell volume;
RBC 5 red blood cell; WBC 5 white blood cell

The barn owl (Tyto alba) is the most widely distributed species of
owl; it is found worldwide outside polar and desert regions, and in
Asia north of the Alpide belt, most of Indonesia, and the Pacific
islands. Because of its wide distribution, the barn owl has formed 36
subspecies. In Hungary, Tyto alba alba and Tyto alba guttata are
common (15).
The barn owl is a cosmopolitan nocturnal hunter. It is closely
associated with people, foraging, nesting, and roosting around
human settlements and in agricultural areas. Barn owl populations
have been decreasing in number in developed countries in the
previous decades, and only 8001000 pairs live in Hungary (14,15).
The main causes of this decline are the loss of traditional nesting sites
(e.g., old farm buildings and open spires), the intensification of
agriculture, road traffic accidents, and loss of suitable foraging
D

Corresponding author. E-mail:zszabo0906@gmail.com

habitats. Without intensive protection and without work to change


public attitudes toward the barn owl, the long-term survival of these
marvelous birds is in doubt (14,15).
The veterinary care of injured, starving, or poisoned barn owls is a
common task of wildlife veterinarians. After proper treatment, some
of the injured, sick, poisoned, and debilitated birds can be released
back into the wild. During the veterinary treatment of owls,
hematologic and plasma biochemistry tests are often required to
establish the right diagnosis (3). Knowledge of the reference intervals
is necessary for a correct interpretation of the test results. In this
study, the reference intervals of hematologic and plasma biochemistry parameters, parameters considered to be very important for the
veterinary clinician, were determined. The study was motivated by,
to the our knowledge, few such studies in barn owls; we only found
two articles about hematology of barn owls. In 1975, Cooper (6)
described packed cell volume (PCV), hemoglobin (Hb), and red
blood cell (RBC) values of 11 East African barn owls; and in 1998,

228

229

Blood reference intervals of barn owls

Table 1.

Mean, SD, and range of hematologic values for healthy adult barn owls.
This study (n 5 31)

Hematology
9

WBC (3 10 /L)
RBC (3 1012/L)
Hb (g/L)
Hemacrit (%)
Absolute values
Heterophils (3 109/L)
Lymphocytes (3 109/L)
Monocytes (3 109/L)
Eosinophils (3 109/L)
Basophils (3 109/L)
Differential
Heterophils (%)
Lymphocytes (%)
Monocytes (%)
Eosinophils (%)
Basophils (%)

Mean 6 SD

Range

13.7
3.2
107
46.2

6
6
6
6

2.7
0.4
15
4

8.419.0
2.34.1
75126
4053

7.8
5.5
0.3
0.1
0.1

6
6
6
6
6

2.0
1.9
0.3
0.1
0.1

2.511.1
2.59.9
0.01.4
0.00.5
0.00.3

56.5
40.3
1.8
1
0.6

6
6
6
6
6

11.5
10.9
2.1
1
0.5

20.076.0
23.079.0
0.09.0
0.03.0
0.02.0

Hawkey and Samour (9) described several hematology parameters of


10 barn owls. We did not find any normal values for plasma
biochemistry parameters of barn owls. As regard other owl species
Spagnolo et al. (23) described the hematologic, biochemical, and
protein electrophoretic values of 10 captive tawny owls (Strix aluco)
in 2008, and Chan et al. (5) described hematology and plasma
biochemistry parameters of 38 adult captive collared scops owls
(Otus lettia) in 2012.
MATERIALS AND METHODS
This study was conducted between 2002 and 2006, during which
time blood samples were taken from 42 adult (.1-yr-old) healthy barn
owls held in captivity. The owls belonged to the bird population of some
Hungarian zoos (Budapest Zoo and Botanical Garden; Kalman
Kittenberger Zoo and Botanical Garden, Veszprem; Game Preserve of
Kecskemet; Zoo and Botanical Garden of Jaszbereny) and bird
repatriation stations (Barn Owl Foundation, Gyomro; Bird Hospital in
Hortobagy; Istvan Chernel Bird Protection Centre and Memorial
Museum, Koszeg; Misina Nature and Animal Protecting Association,
Pecs). Because all the adult owls included in this study had been captured
in the wild previously, their precise age could not be determined. Neither
could their sex be ascertained using physical examination because barn
owls do not have sexual dimorphism. Coelioscopy and DNA analysis were
not performed for sex identification.
The birds were manually restrained with a help of a thick towel.
Before sampling, all of the birds were physically examined by an expert
veterinarian who was experienced in examining wild and zoo animals.
Most of the birds had suffered previously road traffic accidents or other
traumas, and some of them had wing and leg fractures. However, these
injuries were already healed at the time of the blood sampling, and the
examining veterinarian declared each owl clinically normal. The health
status of the owls was determined by their clinical history and by
physical examination. No additional diagnostic procedures were
performed. Any animal with signs of disease, unhealed injuries,
anorexia, or weight loss was excluded from the study.
Withdrawal and storage of blood samples. Blood samples were
taken from the wing vein (v. cutanea ulnaris) of conscious barn owls
before the morning feeding, using a 22 gauge needle. For hematologic
examinations, a 0.3-ml blood sample was taken into tubes containing
K3EDTA, whereas for the determination of biochemistry parameters,
1 ml of blood was withdrawn into tubes containing lithium-heparin.
After sampling, blood smears were made from blood that had not yet

Hawkey and Samour (9) (n 5 10)


Mean 6 SD

16.6
2.7
142
46

6
6
6
6

4.2
0.3
15
3

Cooper (6) (n 5 11)

Range

Mean

11.522.3
2.23.0
127164
4251

8.9 6 3
5 6 1.7

2.16
187
43.7

Range

1.72.75
115231
3652

5.212.5
2.57.5
01
02.5
00.9

been exposed to anticoagulant. Once dried, the smears were fixed in


methanol.
Blood samples treated with anticoagulant were transported at a
temperature between 1 C and 4 C to the Clinical Laboratory of the
Department of Internal Medicine of the Faculty of Veterinary Science,
Szent Istvan University, Budapest, Hungary. In the laboratory, the
heparinized blood samples were centrifuged, and a hematologic analysis
was carried out within 12 hr of withdrawal. The samples were stored at
24 C pending plasma biochemistry analyses that were carried out
within 24 hr after blood sampling.
Hematologic analyses. PCV was determined by the microhematocrit
method (Z-233M-2 centrifuge, Hermle Labortechnik GmbH, Wehingen, Germany), whereas Hb concentration was measured using a
Minidil-2 automatic hematologic analyzer (Diatron Ltd., Budapest,
Hungary). RBC and white blood cell (WBC) counts were determined
using a Buerker chamber by the method of Natt and Herrick (20).
Blood smears were stained with May-Grunwald Giemsa stains (ReanalKer Ltd., Budapest, Hungary), and the differential blood count was
taken by counting 200 cells in each smear (3). Only smears with ,25%
smudge cells were used for hematologic analysis.
Plasma biochemistry analyses. Plasma was obtained by centrifugation. Plasma biochemistry parameters were determined with an RX
Daytona automatic analyzer (Randox Laboratories Ltd., Crumlin,
Antrim, U.K.). Total plasma protein (7), aspartate aminotransferase
(AST, glutamic-oxaloacetic transaminase) (1), alkaline phosphatase (13),
L-c-glutamyltransferase (24), lactate dehydrogenase (LDH) (11),
creatine kinase (CK with N-acetylcysteine) (2), amylase (19), lipase
(16), and uric acid (25) were assayed with commercial reagent kits
(Diagnosticum Co., Budapest, Hungary). Bile acids (17,18,21) and
glutamate dehydrogenase (GLDH) (22) were determined with Randox
procedures (Randox Laboratories Ltd.)

RESULTS

No hemoparasites or hemopathologic changes were detected in


any of the individual blood smears. The hematologic and plasma
biochemistry values (mean, SD, ranges) of healthy, captive, adult
barn owls (n 5 42) are presented in Tables 1 and 2.
DISCUSSION

Hematologic and plasma biochemistry parameters may be


influenced markedly by the habitat (4), health status (8), age (12),

230

Z. Szabo et al.

Table 2. Mean, SD, and range of plasma biochemistry values for captive, healthy adult barn owls.
This study, barn owls (n 5 42)
Mean 6 SD

AST (U/L)
GGT (U/L)
Lipase (U/L)
CK (U/L)
LDH (U/L)
ALP (U/L)
Amylase (U/L)
GLDH (U/L)
Total protein (g/L)
Uric acid (mmol/L)
Bile acids (mmol/L)

272
9.5
31.7
2228
1702
358
563
7.5
30.6
428
43

6
6
6
6
6
6
6
6
6
6
6

43
4.7
11.1
578
475
197
114
2.5
5.3
102
18

Spagnolo et al. (23), tawny owls


(n 5 48)

Range

175335
1.219
1059
11903585
10282374
115658
302823
4.312.4
2442
280646
2089

and husbandry and nutrition (10) of the birds. The hematology


values measured in adult barn owls in this study were compared with
those obtained by Cooper (6) and Hawkey and Samour (9) (Table 1).
The hematocrit values were similar in all three studies (present study,
46.2%; Hawkey and Samour, 46%; and Cooper, 43.7%). The total
WBC, heterophil, lymphocyte, monocyte, eosinophil, and basophil
counts of our study and those of Hawkey and Samour (9) were also
similar. Heterophils were found to be the most common cell type
(56.5%), followed by lymphocytes (40.3%), whereas the proportions
of the other WBC types were relatively small. The RBC count of our
study was close to Hawkey and Samour (9) result but higher than the
result Cooper described (6) (this study, 3.2 3 1012/L; Hawkey and
Samour, 2.7 3 1012/L; and Cooper, 2.16 3 1012/L). In the present
study, much lower Hb value was measured than the high value
reported by Cooper (6). Our Hb value was closer to, but lower than
the value determined by Hawkey and Samour (9) (this study, 107 g/L;
Hawkey and Samour, 142 g/L; and Cooper, 187 g/L).
Because we did found any publications about the normal plasma
biochemistry parameters of barn owls, the values of our study were
compared with the Spagnolo et al. (23) results of tawny owls and the
Chan et al. (5) results of collared scops owls (5) (Table 2). The uric
acid values were similar in all three studies (this study, 428 mmol/L;
Spagnolo et al., 457 mmol/L; Chan et al., 523 mmol/L). The AST
results of Spagnolo et al. (23) and our study were similar but
approximately five times higher than the values Chan et al. (5) reported
(this study, 272 U/L; Spagnolo et al., 281 U/L; and Chan et al., 59 U/
L). Our studys c-glutamyl transpeptidase (GGT) (9.5 U/L) and total
protein (30.6 U/L) values were lower than those that Spagnolo et al.
(23) described. The CK (2228 U/L) and LDH (1702 U/L) enzymes in
our study were much higher than the values Chan et al. (5) reported.
The alkaline phosphatase (ALP) value of our study was between the
values that Spagnolo et al. (23) and Chan et al. (5) reported (this study,
358 U/L; Spagnolo et al., 629 U/L; and Chan et al., 179 U/L).
The difference between the biochemistry parameters can be
caused by the different methods used in the mentioned studies. In
Chan et al. (5), the biochemical plasma analyses were undertaken
using an automated clinical dry chemistry analyzer (Dri-Chem 3000,
Fujifilm, Tokyo, Japan). However, in Spagnolo et al. (23), the
plasma was immediately frozen at 230 C, and samples were
analyzed within 2 mo by using an automated analyzer and liquid
reagents (Eos Bravo, Hospitex Diagnostics, Firenze, Italy). For
lipase, GLDH, and bile acids, no reference values were found in the
literature to which the present results could be compared.
A limitation of our study is that only captive barn owls were
examined. Husbandry and nutrition that differed from the natural

Mean

Chan et al. (5), collared scops owls


(n 5 3337)

Range

Mean

Range

281
31

214368
477

59

3782

86

2344

629

1841459

346
678
179
601

50849
2851170
89375
2001024

38.6
457

33.554
282632

47
523

3458
273945

circumstances may have an impact on the hematologic and plasma


biochemistry parameters. This relationship must be taken into
account when using the results reported here as reference values.
The main objective of this study was to determine baseline data of
hematocrit and plasma biochemistry values for captive, healthy adult
barn owls. Our results may help clinicians working in zoos and bird
rescue centers to evaluate the health status of the birds and to make
decisions as to when to release healthy animals.
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