J. RaptorRes.

24(4):113-119
¸ 1990 The Raptor ResearchFoundation, Inc.

CLINICAL HEMATOLOGY AND BLOOD CHEMISTRY

VALUES FOR THE COMMON BUZZARD
(Buteo buteo)

MAURO HERNANDEZ, SONSOLESMARTIN AND PALOMA FORES

Departamentode Patologœa
Animal II, Facultadde Veterinaria,
UniversidadComplutense,
28040 Madrid, Spain

ABSTR^CT.--Clinicalhematologyand serumchemistryvaluesfor 23 clinicallynormal CommonBuzzards

(Buteobuteo)haveprovidedreferencevaluesfor usein clinical pathology.Hematologicalvalues,including
red and white blood cell counts,hematocrit,hemoglobinconcentration,leukocytedifferential count and
red cell indiceswere established.Referencevaluesof bloodchemicalparameters,including total plasma
protein,total plasmasolids,fibrinogen,glucose,aspartateaminotransferase (AST, SGOT), alanineami-
notransferase(ALT, SGPT), gammaglutamyltransferase ('y-GT), creatinekinase (CK), lactatedehy-
drogenase(LDH), creatinine,uric acid, calciumand phosphoruswere also establishedand comparedto
results obtained by other authors.

Valoresde hematologlay biogulmicasangulneade ratoneroscomunes(Buteobuteo)

EXTR^CTO.--Losvaloresde hematologlay bioqulmicasangulneade 23 ratoneroscomunes(Buteobuteo)
sanosproporcionaron valoresde referenciapara su uso rutinario en patologlacllnica. Los valoresde
hematologlaque se determinaronfueron:recuentode eritrocitosy leucocitos,hemat6crito,concentraci6n
de hemoõlobina,recuentodiferencialde leucocitose indiceseritrocitarios.Los valoresde bioqulmica
sangulneadeterminadosfueron: protelnasplasmfiticastotales,s61idosplasmfiticostotales,fibrin6geno,
õlucosa,aspartatoaminotransferasa (AST, SGOT), alaninoaminotransferasa (ALT, SGPT), gamma
glutamil transferasa(-y-GT), creatinaquinasa(CK), lactatodeshidrogenasa (LDH), ficidofirico, crea-
tinina, calcioy f6sforo.Los resultadosobtenidosse discutenconlos de otrosautores.

Clinical hematologyand bloodchemistryare use- fromphysiological valuesof selectedhematologic tests

ful diagnostictools (Woerpel and Rosskopf1984, couldbe of greatvalue for both diagnosticand prog-
Campbelland Dein 1984, Campbell 1988). In recent nosticpurposes.Nevertheless,very few data have
years, normal hematologicvaluesfor both pet and been found through the literature on hematologic
wild birds (Hawkey et al. 1983, 1985, Lumeij and values for this species(Veil 1978, Lepoutre 1982,
de Bruijne 1985) and hematologicalchangesin re- Lepoutre et al. 1983) and no information is available
sponseto disease(Hawkey et al. 1984, O'Halloran on the normal plasma concentrations of enzymes
et al. 1988) havebeenreported.Tissue enzymepro- commonlyusedin avian medicine.This paper deals
filesfor someavianspecieshavealsobeenestablished with thenormalclinicalhematologyandbloodchem-
(LumeijandWolfswinkel1988,Lumeijetal. 1988a) istry valuesfor the CommonBuzzard and their ap-
and changesin plasmalevelsof selectedenzymesas plication as diagnosticaids in clinical practice.
a result of diseasehavebeenreviewed(Lumeij et al.
METHODS
1988b, Lumeij and Westerhof1987).
Nevertheless, such testsare of limited clinical use- Blood sampleswere collectedfrom 23 normal adult
fulnessin raptors becauseof the lack of data for Common Buzzards housed in outdoor enclosures at the
referencevaluesin many species(Redig 1978) and the Centrode EspeciesProteõidasde Buitrago,belongingto
Comunidad Autonoma de Madrid.
the limited number of parametersand individuals Thirteenof the birdswereimprintedadultsof unknown
for thosespecies that havebeentested(Cooper1972, age. Time spentin the Center ranged from 6 monthsto
Elliot et al. 1974, Cooper 1975, Redig 1978, Kirk- 2 years.Ten additionalbirdswere illegally taken as nest-
wood et al. 1979, Halliwell 1981, Ivins et al. 1985, lings,confiscatedby the authoritiesand kept in the Center
until theirreleaseintothewild someweeksaftersampling
Hawkey and Hart 1988). Three of thesebirdswere 1 year old and the remaining
The Common Buzzard (Buteo buteo)is one of the sevenbirds were 2 years old.
mostfrequentlyinjuredbirdsof preyin Spain.Data Birds were housed in 15 x 7 x 3 or 10 x 5 x 3 meter

113
114 MAURO HERNANDEZ ET AL. VOL. 24, NO. 4

Table1. Hematological
values
forcaptive
Common
Buzzards.
Thenumber
of samples
(N), meanvalue(,•), standard
deviation(SD) and observedrange are given for eachparameter.

PARAMETER N .• SD RANGE

TRBC (x 106/nl) 22 2.94 0.82 5.44-2.06

TWBC ( x 103/nl) 23 8.04 1.77 10.6-4.6
PCV (%) 22 40.8 4.4 49-36
Hemoglobin(g/dl) 22 12.7 2.4 17.7-9.3
Heterophils (%) 23 63 13.1 75-45
Band (%) 23 0 0 --
Lymphocytes(%) 23 20 9.5 48-10
Eosinophils(%) 23 16 13.8 37-0
Monocytes(%) 23 0 1.0 4-0
Basophils(%) 23 0 0.7 3-0
Heterophils( x 103/t•l) 23 4.58 1.2 5.8-2.3
Band ( x 103/t•1) 23 0 0 0
Lymphocytes ( x 103/t•1) 23 1.4 0.73 2.9-0.2
Eosinophils( x 103//zl) 23 1.2 1.1 3.4-0
Monocytes ( x 103//al) 23 0.05 0.08 0.3-0
Basophils
( x 103/t•1) 23 0.6 0.1 0.2-0
MCV (fl) 22 145.1 25.0 171.4-90.0
MCH (pg) 22 48.3 10.2 65.7-32.5
MCHC (g/dO 22 32.4 6.7 45.3-22.6

pens with sidesand top coveredby wire netting and
equippedwith woodenperches.No birds were known to
be sickor seriouslyinjured during their stayin the Center.
Birds with leg or wing injuries, skin wounds,bumblefoot
and any otherdisease,or birds showingunusualbehavior
were not considered for the study.The buzzardswere fed
oncea day either with chickencarcasses or day-oldchicks
and water was providedad libitum.
Bloodsampleswere takenin May, June andJuly 1989
at the sametime eachday (1100-1230 H) to eliminate
diurnal fluctuations.Birds were alwaysbled beforebeing
fed. Birds were physicallyrestrainedwith the aid of a
falconer's hood and a towel. Blood was taken by veni-
puncturefrom the basilicvein usingdisposable23-gauge
needlesand 2 ml plasticsyringes.After removingthe nee-
dle, 1 ml of whole blood for hematologywas placedin a
commercially availableplastictubecontainingEDTA. The
remaining blood for blood chemistrydeterminationswas
placedin anotherplastictube containing5% lithium hep-
arin. Only onesamplewastaken per bird. The bloodwas
tested within 3 hr of collection.
Total red and white blood cell counts (TRBC and
TWBC) were performedwith the Natt-Herrick solution
(1:200dilution)and Neubauerhemocytometer (Campbell
1988). The hematocritvalue (PCV) was obtainedby the
standard microhematocritmethod. Hemoglobin concen-
tration was estimatedin duplicateby the cyanomethemo-
globin methodand red cell indices(MCV, MCH and
MCHC) were calculatedby usingthe standardformulas
(Campbell 1988). The leukocytedifferentialcountwas
performedby the routinemicroscopic procedure in a smear
stainedwith May-Grfnwald Giemsa(Hawkeyetal. 1983).
Polychromasiaand anisocytosis
were estimatedby ex-
amining blood smearsin order to assesserythropoietic
activity.Biochemicalmethodsusedin bloodchemistryde-
terminationsare summarizedin the Appendix 1.
RESULTS
The values obtained are presentedin Table 1
(hematology)and in Table 2 (bloodchemistry).No
distinctionwas made by sex, age, origin of the bird
or the lengthof time in captivity.A slightanisocytosis
and a certainnumber of polychromaticerythrocytes
(usually a mean of 3% of the erythrocytesin one
100 x oil field) were regardedas normal. The ten-
dencyof thrombocytes to clump precludedthe use
of the Neubauer hemocytometerfor countingthem
and thus their number, estimated in a smear, was
reported as "decreased,""normal" (about a mean
of 2 thrombocytes per 100X oil field of goodcellu-
larity) or "increased."White cell morphologyin
the Common Buzzard was similar to that described
by Hawkey et al. (1983), Campbell (1988) and
Hawkey and Dennet (1989) for other birds.
Normal plasmacolorvariedfrom clearto yellow.
No hemolysisdue to the EDTA was found in the
samplesas has been reportedin other bird species
(Hawkey et al. 1983,Campbell1988).Total plasma
solids(TPS) valuesobtainedby the refractometric
WINTER 1990 COMMONBUZZARDCLINICALHEMATOLOGY 115

Table 2. Bloodchemistryvaluesfor captiveCommonBuzzards.

PARAMETER N .• SD RANGE

TPS (g/dl) 21 4.6 0.8 5.89-2.3

TPP (g/dl) 21 3.1 1.5 5.3-1.1
Fibrinogen (g/dl) 21 1.5 0.8 2.9-0.3
Glucose (mg/dl) 20 301.1 53.1 370-173
AST (SGOT) (IU/liter) 21 227.7 155.5 365-66.9
ALT (SGPT) (IU/liter) 18 13.1 5.9 28.9-5.17
3'-GT (IU/liter) 18 3.5 0.7 5.1- < 2.8
CK (IU/liter) 20 393.2 187.8 766-119
LDH (IU/liter) 14 631.5 153.0 820-300
Uric acid(mg/dl) 20 6.0 1.5 8.5-2.89
Creatinine (mg/dl) 19 0.9 0.3 1.4-<0.5
Calcium(mg/dl) 16 11.2 2.5 16.6-7.9
Phosphorus (mg/dl) 10 4.6 3.3 9.4-1.3

methodwerefoundhigherthantotal plasmaprotein the mature erythrocytes,

appearmore roundedand
(TPP) valuesobtainedby the Biuret method. havemorebasophiliccytoplasm(CampbellandDein
1984).
DISCUSSION
The cyanomethemoglobin methodis the mostac-
Total red blood cell counts(TRBC), hemoglobin curate method for estimatingthe hemoglobincon-
concentration and PCV values were found similar centrationin both mammalian and avian blood(Smith
by otherauthorsfor the Common and Lience 1977, Amand 1985). Since the red cell
to thosedescribed
Buzzard (Leonard 1969, Veil 1978, Lepoutre 1982, indices(MCV, MCH and MCHC) are calculated
Lepoutreet al. 1983), and for otherraptor species fromthe PCV, hemoglobin concentration
andTRBC,
(Cooper1972,Balaschet al. 1973,Elliot et al. 1974, their validity is influencedby the accuracyof the
Cooper1975, Redig 1978, Kirkwoodet al. 1979, TRBC, the hemoglobindeterminationand PCV val-
Gee et al. 1981). ue (Amand 1985). MCV and MCH fall within the
The numberof circulatingerythrocytes,
andthus rangeof variationdescribedfor wild birds (Leonard
valuesof TRBC, are influencedby a number of 1969, Balaschet al. 1973, Hawkey et al. 1983).
factorssuchassex,age,andaltitude(Leonard1969, Nevertheless,the wide range of MCV and MCH
Stoskopfet al. 1983, Campbell and Dein 1984, valuesfound in our study couldbe due to the in-
Amand 1985). Nevertheless,in our study the wide accuracy of thehemocytometer methodfor red blood
rangeof variationof TRBC valuesmay be due to cell counts.The normal ranges for MCHC values
the technical error inherent in the hemocytometer are similar in all mammalsand birds (Hawkey et
method(Steelet al. 1977, Smith and Lience 1977). al. 1983).
The useof an electronicparticlecountercouldmin- Several methods have been proposed for deter-
imize this error. PCV valuesare lesssubjectto tech- miningavianWBC counts(CampbellandDein 1984,
nicalerrorandthereforeare of greaterclinicalvalue. Amand 1985, Russo et al. 1986). Among them, the
Additionally,the PCV in conjunction with total most accurateand widely usedtechniquesare the
plasmaprotein(TPP) wastheeasiest andleasttime- eosinophilUnopette5877 system(Becton-Dickinson
consumingmeansof assessing the hydrationand and Co., Rutherford, New Jersey) and the Natt-
anemicstatusof a bird (Campbell and Dein 1984, Herrick solution. The method employed for the
Jenkins 1987). Unopette systemis semi-indirectand involvesthe
No reticulocyte countswereperformedsincesig- useof the eosinophilUnopettediluent, composedof
nificanceof high reticulocytenumbersin bird cir- phloxine and propylene glycol, and a Neubauer
culatingbloodremainsunknown(Hawkey et al. hemocytometer. The diluentphloxineonlystainsthe
1983). On the other hand, erythropoieticactivity granulocytes. Therefore,the countobtainedmustbe
couldbeassessed estimatingin the smearthenumber corrected since mononuclear cells are not included
of polychromatic erythrocytes. Thesecells,unlike (Campbell and Dein 1984). This is done by deter-
116 MAURO HERNANDEZ ET AL. VOL. 24, NO. 4

miningtheratioof granulocytesto mononuclearcells this study, TPS were higher than TPP valuesob-
in a stainedblood smear (Amand 1985). The Natt- tained by the Biuret method.TPP valuesfell within
Herrick solution stains only mononuclear cells, the rangedescribedfor both pet and wild birds (Gee
granulocytes,and thrombocytes,permitting direct et al. 1981, Woerpel and Rosskopf1984, Ivins et al
countof thesecellswith a hemocytometer(Russoet 1985).
al. 1986). Hawkey and Hart (1988) provedthat fibrinogen
Direct hemocytometercounts are more accurate level is one of the most useful tests for both confirm-
than WBC estimatesdetermined by the Unopette ing infectionand other inflammatory diseases,and
systemmethodbecause ofthevariationin differential followingthe patient'sprogress.Nevertheless,data
counts (Russo et al. 1986). Both are subjectto the for only a limited number of raptor speciesare now
technical error of the hemocytometermethod, and available. Our results on the Common Buzzard are
changesin the WBC count may be causedby the within the range describedby theseauthorsfor rap-
variability inherent in the method of enumeration tors.
(Russo et al. 1986). Part of this error may be de- The glucosevaluesobtainedfrom buzzardsin this
creasedby standardizingthe technique(using the study are within the normal range of variation ob-
samechamber,coverslipand pipetteand havingthe servedin birds (Lepoutreet al. 1983). Bloodglucose
samepersonperformthe counts)(Russoet al. 1986). levelscould be indicative of the general health status
In our studycell countswere performedby the same of the bird. Low glucosevaluesresult from hepa-
personand by the sameprocedure. topathies,septicemiaor endocrinopathies rather than
Total white cell counts were found to be similar from starvation since starved raptors do not show
to thosedescribed previouslyfor the species
(Leonard hypoglycemiaand may evenbe hyperglycemic(Lu-
1969, Veil 1978, Lepoutre et al. 1983) and within meij 1988).
the range of variation describedin pet and other No information is available on the normal range
wild birds (Hawkey et al. 1982, 1983, 1984, Woer- of variation of AST, LDH, CK, ALT and 3,-GT
pel and Rosskopf1984, Calle and Stewart 1987). values in the Common Buzzard (Gee et al. 1981,
No band heterophilshave been found in the cir- Halliwell 1981, Ivins et al. 1985). Aspartate ami-
culating bloodof healthy buzzards.Thus, a certain notransferase(AST, formerly SGOT) is widely dis-
number of thesecells(left shift) shouldbe considered tributed in avian tissues and its relative distribution
as abnormal becausethey are indicativeof a pe- variesfrom onegenusto another(Lumeij and Wes-
ripheral consumption
of heterophils(Schalmet al. terhof 1987). AST valuesin this studycomparewell
1975). with thosedescribedfor pet and other birds (Gee et
High eosinophilcountshave beenfound in buz- al. 1981, Woerpel and Rosskopf1984, Ivins et al.
zard blood (Veil 1978, Lepoutre 1982, Lepoutre et 1985, Calle and Stewart 1987). Lactate dehydro-
al. 1983). High countsare thoughtto be associated genase(LDH) alsooccursin mostaviantissues(Lu-
with intestinal parasitism(Hawkey et al. 1983). meij and Westerhof1987) and the bloodconcentra-
Nevertheless,Lepoutre et al. (1983) demonstrated tion found in the buzzard showsa wider range and
that raptors,and the CommonBuzzardin particular, a higher mean value than thosedescribedfor psit-
are characterizedby high numbersof eosinophilsin accines(Woerpel and Rosskopf1984) but similar to
circulating blood and this finding is not associated thosefor raptors(Gee et al. 1981, Ivins et al. 1985).
with a clinical condition.Blood chemistryvaluesfor LDH values varied more than AST values. Creatine
a variety of species,including raptors, have been kinase (CK) is mainly found in muscle,and small
reported(Gee et al. 1981, Lepoutre 1982, Lepoutre amountsare foundin kidneyandduodenum(Lumeij
et al. 1983, Ivins et al. 1985, Ferrer et al. 1987). and Wolfwinkel 1988, Lumeij et al. 1988). No in-
The refractometricmethod is being used for the formationhas beenreportedabout normal levelsof
determinationof plasmaproteinconcentration(total CK in raptor blood (Gee et al. 1981, Ivins et al.
plasmasolids)by avian practitioners.Nevertheless, 1985). CK valuesin buzzardswere higherthan those
Lumeij and de Bruijne (1985) demonstrated that the observedfor racing pigeons(Lumeij and de Bruijne
refractometric method is unreliable for determina- 1985).
tion of plasma protein concentrationin avian blood Alanine aminotransferase (ALT, formerlySGPT)
sincesubstancesother than protein contributesub- is mainly found in liver and kidney in pigeons(Lu-
stantiallyto the refractiveindex (Lumeij 1987). In meij et al. 1988). Nevertheless,its low activity in
WINTER 1990 COMMON BUZZARD CLINICAL HEMATOLOGY
plasma,high activity in erythrocytesand seasonal and sampleprocessing;to Dr. F. Parra who has provided
variation (Lewandowski et al. 1986, Lumeij and
Westerhof 1987) limits its use for diagnosticpur-
poses.ALT valuesin this studywere found lower
than thoseobservedin raptors(Gee et al. 1981) but
similar to racingpigeons'plasmalevels(Lumeij and
de Bruijne 1985). Gamma glutamyltransferase('•-
GT) is almostentirelynephrospecific in birds (Lu-
LITERATURE CITED
meij and Wolfswinkel 1988). Enzymesoccurringin
the kidney might be of limited clinical value since AMAND,W.B. 1985. Avian clinicalhematologyand blood
theseenzymesare largely eliminatedvia the urine
afterkidneydamage(LumeijandWolfswinkel1988).
'•-GT valueswere found similar to thosepreviously
reported(Gee et al. 1981).
Plasmacalciumand phosphoruslevelswere with-
in the rangeof variationfoundfor thespecies(Ferrer
et al. 1987, Lepoutre 1982). Since there is an al-
bumin-boundcalciumfraction,it is necessary to con-
sider calcium levelsin conjunctionwith TPP levels
(Ivins et al. 1985). Both calcium and phosphorus
levelsmay be indicatorsof renal function and may
help to evaluatenutritional deficiencies.
Uric acidis the major end productof deamination
of amino acidsin avian speciesand is excretedby
the kidney mainly by tubular excretion(Lewan-
dowskiet al. 1986, Lumeij 1987). Sincethe rate of
secretionis largely independentof the state of hy-
dration, the measure of uric acid is the most reliable
method to assessrenal function in birds (Amand
1985, Lumeij and de Bruijne 1985, Lewandowski
et al. 1986, Lumeij 1987). The Common Buzzard
has lower valuesthan other raptors and other birds
(Gee et al. 1981, Lepoutre 1982, Woerpel and Ross-
kopf 1984, Ivins et al. 1985).
Plasmacreatinineconcentrationis of questionable
value in evaluatingrenal function in birds (Lewan-
dowski et al. 1986, Lumeij 1987). The amount of
creatinine formed from creatine is negligible and
creatininevalue measuredby conventionalmethods
includespseudocreatinines, suchas glucose,protein,
ascorbicacid and pyruvic acid and may not reflect
glomerularfunction(Lewandowskiet al. 1986, Lu-
meij 1987). Creatininelevelsin this studywere with-
in the range of variation found in raptors (Gee et
al. 1981, Ivins et al. 1985) and considerablyhigher
thanvaluesobserved in petbirds(Woerpeland Ross-
kopf 1984).
ACKNOWLEDGMENTS
We are grateful to A. Fernandez-Arias, A. Altozano
and F. Villarina for their assistance
during bloodcollection
1 17
us with the licenceto take samplesfrom birds housedin
the Buitrago Center; to Dr. C.M. Hawkey and Dr. M.G.
Hart for their assistancein the fibrinogen measurements,
blood cell identificationand staining procedures;and to
Dr. G.E. Duke, Dr. P.T. Redig and two anonymousre-
viewers who made useful comments and corrections in an
early versionof this paper.
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referencevalues in racing pigeons.Arian Pathol. 14: experiencewith avian laboratorydiagnostics.
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401-408. North Am.: Small Anita. Pract. 14:249-286.
, --, A. SLOB, J. WOLFSWINKELAND J.
ROTHUIZEN. 1988a. Enzyme activitiesin tissuesand
elimination half-lives of homologousmuscleand liver
enzymesin the racing pigeon.Arian Pathol. 17:851-
864. Received8 November 1989; accepted11 October 1990
WINTER 1990 COMMON BUZZARD CLINICAL HEMATOLOGY 119

Appendix 1. Blood chemistrytest methodsusedfor analysisof Common Buzzard blood.

TEST METHOD AND SOURCE

Total plasma solids(TPS) Refractometer.

Total plasmaprotein (TPP) ColorimetricBiuret Method. Weichselbaum,T.E. Amer. J. Clin. Path. 16 (1946):
40. a

Fibrinogen Proteinprecipitated
by the microhematocrit
at 56øC.b
Glucose GOD-POD Method. Trasch, H., P. Koller, W. Tritschler, Clin. Chem. 30
(1984):969. a
Aspartate aminotransferase GOT-POD Method. 25 ø. Deneke, V., W. Rittersdorf, W. Werner, Clin. Chem.
(AST, SCOT) 31 (1985):921. a
Alanine aminotransferase GPT-POD Method. 25ø. Deneke, V., W. Rittersdorf, Clin. Chem. 30 (1984):
(ALT, SGPT) 1009.a
•,-Glutamyl transferase Reductionof 6[Fe(CN)6]4-. 25ø. Deneke, V., K. D. Willamowski, W. Tritschler.
(•,-GT) Clin. Chem. 30 (1984):1010. a
Lactic dehydrogenase (LDH) Reduction of NAD. 30ø. Z. Klin. Chem. u. Klin. Biochem. 10 (1972):182. a
Creatine kinase (CK) Oxidation of 6-Phosphogluconate.30ø. Gruber, W. Clin. Chem. 24 (1978): 177.a
Uric acid Uricase-POD Method. Merdes, H., W. Rittersdorf,W. Werner, J. Clin. Chem.
Clin. Biochem. 28 (1985):608. a
Greatinine PeroxidaseOxidation. Wahbfeld, A., G. Hozt and H. Bergmeyer.Page 1834 in
H. Bergmeyer[Ed.], Methoden der EnzymatischenAnalyse.3rd ed. Vol. II.
Verlag Chemie. Weinheim.a
Calcium Methylthymol Blue Method. Gener, J., Vila, J. and Concustell,E. Lab. Knicher-
bocker S.A.E. (1971). c
Phosphorus Phosphomolybdate Method. Drewes, P.A. Clin. Chim. Acta 39 (1972):81.c
BoehringerMannheim Gmbh Diagnostica,Mannheim, Germany.
Hawkeyet al. 1983.
KnicherbockerReagents,KnicherbockerLab., Barcelona,Spain.