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Comparative study of hematologic and plasma biochemical
variables in Eastern Atlantic juvenile and adult nesting
loggerhead sea turtles (
Caretta caretta
)
Ana B. Casal
1
, Mar´
ıa Camacho
1
, Luis F. L ´
opez-Jurado
2
, Candelaria Juste
3
, Jorge Or ´
os
1
Departments of
1
Morphology and
2
Biology in the Veterinary Faculty and
3
Department of Animal Pathology, University of Las Palmas de Gran Canaria,
Arucas (Las Palmas), Spain [Correction added after publication 2 Feb 2009: The original title, ‘‘Comparative study of hematologic plasma biochemical
variables...’’ has been corrected to read ‘‘Comparative study of hematologic plasma and biochemical variables...’’.]
Key Words
Caretta caretta, clinical chemistry, hematology,
reference values, reptile, sea turtle
Correspondence
Jorge Or ´
os, Veterinary Faculty ULPGC,
Trasmontana s/n, 35413 Arucas (Las Palmas),
Spain
E-mail: joros@dmor.ulpgc.es
DOI:10.1111/j.1939-165X.2008.00106.x
Background: Plasma biochemical and hematologic variables are important in
the management of endangered sea turtles, such as loggerheads. However,
studies on blood biochemistry and hematology of loggerheads are limited, and
different concentrations according to variable criteria have been reported.
Objective: The purpose of this study was to establish and compare baseline
plasma chemistry and hematology values in Eastern Atlantic juvenile and
adult nesting loggerhead sea turtles (Caretta caretta).
Methods: Blood samples were collected from 69 healthy juvenile logger-
head sea turtles after their rehabilitation in captivity, and from 34 adult
nesting loggerheads after oviposition. Fresh blood was used for leukocyte
differential count and PCV determination. Heparinized blood was used for
RBC and WBC counts. Plasma biochemical concentrations were measured
using an automated biochemical analyzer. For the comparative study, non-
parametric statistical analysis was done using the Mann–Whitney U-test.
Results: Minimum, maximum, and median concentrations were obtained
for 14 hematologic and 15 plasma chemistry variables. Statistically signif-
icant differences between juvenile and adult turtles were found for PCV;
RBC, WBC, and leukocyte differential counts; total protein, albumin, glob-
ulins, calcium, triglycerides, glucose, total cholesterol and urea concentra-
tions; and lactate dehydrogenase activity.
Conclusions: Age, size, and reproductive status cause important variations
in the hematologic and plasma biochemical results of loggerheads. The ref-
erence values obtained in this study may be used as a standard profile, use-
ful for veterinary surgeons involved in sea turtle conservation.
Introduction
Currently, many veterinary surgeons are involved in
sea turtle conservation in wildlife rehabilitation hospi-
tals around the world. Sea turtle conservation includes
medical management and clinical and pathologic stud-
ies on stranded animals. Two families and 7 species of
sea turtles are recognized. The family Cheloniidae in-
cludes the green (Chelonia mydas), loggerhead (Caretta
caretta), hawksbill (Eretmochelys imbricata), Kemp’s rid-
ley (Lepidochelys kempii), olive ridley (Lepidochelys oliv-
acea), and flatback (Natator depressa) turtles. The family
Dermochelyidae includes only the leatherback turtle
(Dermochelys coriacea). All of these species are included
in the Red List of the World Conservation Union of en-
dangered species.
1
Studies on blood biochemistry and hematology of
sea turtles are limited.
2–7
However, recently, a mor-
phologic classification based on the cytochemical char-
acteristics of blood cells of juvenile loggerhead sea
turtles has been reported.
8
Sea turtles are affected by
several diseases. Some of these health problems are
naturally occurring processes and are observed in both
wild and captive turtles. Therefore, establishing
biochemical and hematologic reference values is
important for evaluating the health status of these
Vet Clin Pathol 38/2 (2009) 213–218 c2009 American Society for Veterinary Clinical Pathology 213
Veterinary Clinical Pathology ISSN 0275-6382
endangered reptiles. The aim of the present study
was to measure plasma biochemical and hematologic
variables in juvenile loggerheads from the Canary
Islands and nesting adults from Cape Verde.
Materials and Methods
Sixty-nine juvenile loggerhead sea turtles stranded in
the Canary Islands and rehabilitated in outdoor facili-
ties with seawater belonging to Tafira Wildlife Rehabil-
itation Center (TWRC, Las Palmas de Gran Canaria,
Canary Islands, Spain) throughout 2003 and 2004
were used in this study. The mean SD of the straight
carapace length and weight of juvenile turtles were
33.3 5.1 cm (range, 16.5–49.3 cm) and 10.3 2.8 kg
(range, 1.4–26 kg), respectively. Visualization of the
gonads via surgery or endoscopy was not performed.
Sea turtles were placed individually in outdoor pools
with continuous flow of seawater, and a capacity of
10,000 L and 1 m in depth, providing plenty of room
for swimming. Sea turtles were fed fresh and/or frozen
fish (sardine, Atlantic mackerel, and Atlantic horse
mackerel) once a day. Light periodicity ranged from 8
hours in the winter to 14 hours in the summer. Water
temperature in the pools ranged from 181C in the win-
ter to 221C in the summer. The causes of stranding had
been entanglement in fishing nets (n= 42, 60.9%), in-
gestion of hooks and monofilament lines (n=11,
15.9%), trauma caused by boat strikes (n= 4, 5.8%),
crude oil ingestion (n=2,2.9%),malnutrition(n=3,
4.3%), and unidentified causes (n= 7, 10.1%). The min-
imum and maximum times in rehabilitation were
10–195 days. Clinical evaluation, including physical ex-
amination, evaluation of swimming activity, core body
temperature (measured from the cloaca), food ingestion,
weight–straight carapace length ratio, and hydration, was
performed daily by the Veterinary Services staff of the
TWRC following a complete clinical assessment protocol.
Each turtle was released when it was determined to be
clinically normal and in good physical condition. Blood
samples were obtained 2–3 h before each turtle was set
free between 10 a.m. and 1 p.m. Turtles were placed on
foam padding and restrained manually, without seda-
tion. Water temperature ranged from 18.6 1Cto21.81C
depending on the month in which release took place.
Thirty-four female adult loggerhead sea turtles
nesting in Ervatao and Punta Cosme beaches
(Boa Vista Island, Cape Verde) between August and
September of 2004 were also used in this study. The
straight carapace length of the adult turtles was
74.4 3.8 cm (range, 70–87.1 cm). Clinical evaluation
included physical examination, core body temperature
(measured from the cloaca), and observation of ovipo-
sition behavior. None of the adult turtles used in this
study had external lesions, and all showed normal ovi-
position behavior. Environmental temperature ranged
from 22 1Cto261C. Blood samples were obtained be-
tween 2 a.m. and 5 a.m., before the turtles returned to
sea. Turtles were restrained manually, without sedation.
Blood (2 mL) was collected from the cervical sinus
using a disposable 2-mL syringe and a 23-G disposable
needle.
9
Two blood smears were prepared immedi-
ately, air-dried, and stained with Diff-Quik (Everest,
Barcelona, Spain), according to the manufacturer’s
instructions for differential leukocyte count. PCV
was determined immediately using microhematocrit
capillary tubes (Hematokrit, Kapillaren, Hirschmann
Laborgerate, Eberstadt, Germany) centrifuged at 6000g
for 5 minutes (M-24 Boeco, Hamburg, Germany). The
remaining blood was placed in heparinized microtubes
(2-mL capacity; Terumo Europe N.V., Leuven, Bel-
gium) that contained 30 U of lithium heparin, and
stored at 4 1C. One aliquot was used for RBC and
WBC counts, which were carried out within 2 hours
after collection. The remainder was placed in plastic
tubes (1.5-mL capacity; Eppendorf Ib ´
erica, Madrid,
Spain) and about 30 minutes after blood collection,
centrifuged for 15 minutes at 10,000g. Plasma was im-
mediately separated using a Pasteur pipette (Normax,
Marinha Grande, Portugal) and stored up to 10 days at
–201C until analysis. For differential leukocyte counts,
200 leukocytes were counted. RBCs and WBCs were
counted with a Neubauer hemacytometer (Canemco
Inc., Quebec, Canada), using the Natt and Herrick
method. Thrombocytes per liter of blood were esti-
mated according to a method described previously.
10
Plasma biochemical constituents were measured
using an automated dry chemistry analyzer (Spotchem
SP-4430, Arkray Inc., Kyoto, Japan) and reagent strips
(Spotchem II Panel-1, Panel-2, and Panel-V) according
to the manufacturer’s instructions. The biochemical
analytes and methods were as follows: total protein
(colorimetric method using copper sulfate), albumin
(bromcresol green), globulins (calculated), calcium (o-
cresolphthalein complexone), triglycerides (glycerol-
phosphate oxidase), uric acid (uricase), glucose (glucose
oxidase), total cholesterol (cholesterol oxidase), urea
(colorimetric reaction using o-phthaldehyde and N-1-
naphthyl-N0-diethylethylenediamine), total bilirubin
(colorimetric reaction using sulfanilic acid, sodium ni-
trite, and dyphylline), creatinine (3,5-dinitrobenzoic
acid), lactate dehydrogenase (LDH; lithium L-lactate
as a substrate), aspartate aminotransferase (sodium L-
aspartate and a-ketoglutaric acid as substrates), alanine
aminotransferase (L-alanine and a-ketoglutaric acid as
214 Vet Clin Pathol 38/2 (2009) 213–218 c2009 American Society for Veterinary Clinical Pathology
Casal et alHematology and biochemistry of sea turtles
substrates), and alkaline phosphatase (p-nitrophenyl
phosphate as a substrate). Temperature of reaction for
the enzymatic analyses was 371C. All samples were
measured in duplicate and a normal serum control
(Spotchem Calibration Check) was assayed between
each replicate. The analyzer was calibrated for each test
according to the manufacturer’s instructions.
Normality (Kolmogorov–Smirnov test) and Le-
vene tests were used (SPSS 14.0 for Windows, SPSS
Inc., Chicago, IL, USA) to assess data distribution. Be-
cause all distributions were not normal, the
Mann–Whitney U-test was used to compare results be-
tween juvenile and adult turtles, considering Po.05 as
significant. For all samples with concentrations below
the limit of quantification, the limit of quantification
was used in the calculation. Results were expressed as
median, minimum, and maximum values.
Results and Discussion
Results were tabulated for juvenile and adult turtles
(Table 1). Several hematologic and biochemical vari-
ables were significantly different based on age group.
Variation in the hematologic and blood biochemi-
cal variables due to age, size, and species have been
described previously in sea turtles.
2–5
Although serum
is usually used for biochemical analysis in mammals,
serum is not recommended for reptile studies because
clot formation is unpredictable and the time required
for clotting may allow substantial changes in the
chemical composition of the sample.
11
Sea turtles are
ectothermic vertebrates and their blood biochemical
pattern is highly influenced by external factors, such as
nutritional and environmental conditions.
12
In addi-
tion, differences in the methodology and instrumenta-
tion can explain the variations of the blood biochemical
pattern reported by several authors. No methods have
been validated in sea turtles and this may result in low
transference of results.
PCV values of the adult nesting turtles were signif-
icantly higher than those observed in the juvenile tur-
tles. A significant correlation between PCV and the
straight carapace length of sea turtles has been previ-
ously reported.
2,4,5
Several authors reported that age
can affect the PCV values of sea turtles.
2,4
Bradley et al
6
cited a PCV value of 19.2% for the hatchlings of
loggerhead sea turtles. PCV median value of our
Table1. Hematologic and plasma biochemical results for juvenile and adult nesting loggerhead sea turtles (Caretta caretta).
Analyte (Unit)
Juveniles (n= 69) Adults (n=34)
P-Value
Minimum–Maximum Median Minimum–Maximum Median
PCV (%) 17–45 28 28–54 40 o.001
RBCs ( 10
10
cells/L) 3–60 18.7 2–40 9.4 o.001
Thrombocyte estimate ( 10
9
cells/L) 10–90 44.3 30–90 42.6 .508
WBCs ( 10
9
cells/L) 2.0–18.9 5.9 0.3–4.4 1.6 o.001
Heterophils ( 10
9
cells/L) 1.8–7.3 4.6 0.3–3.1 1.1 .048
Eosinophils ( 10
9
cells/L) 0–1.2 0.2 0.1–1.3 0.3 o.001
Basophils ( 10
9
cells/L) 0–0.00001 0.000001 0–0.00001 0.000001 —w
Lymphocytes ( 10
9
cells/L) 0.1–1.8 1.0 0.1–0.6 0.3 .01
Monocytes ( 10
9
cells/L) 0–0.3 0.07 0–0.2 0.01 .045
Total protein (g/L) 20–110 24 26–60 41 o.001
Albumin (g/L) 10–14 11 11–26 17 o.001
Globulins (g/L) 0–26 13 15–36 24 o.001
Creatinine (mmol/L) o26.5–70.7 31.8 o26.5–88.4 39.7 .66
Uric acid (mmol/L) o0.05–0.10 0.06 o0.05–0.20 0.10 .156
Urea (mmol/L) 1.8–67.3 36.3 5.0–9.7 7.2 o.001
Bilirubin (mmol/L) o3.4–8.5 3.4 3.4–51.3 17.2 .051
Total cholesterol (mmol/L) 1.3–10.3 3.6 5.5–9.1 8.7 .001
Triglyceride (mmol/L) 0.3–21.0 7.4 1.1–5.6 1.3 o.001
Glucose (mmol/L) 1.1–16.2 7.2 1.9–5.5 3.3 .001
Calcium (mmol/L) 0.7–3.1 2.0 2.1–4.3 3.1 .002
AST (U/L) o10–844 194 51–214 123 .294
ALT (U/L) o10–258 24 o10–23 11 .948
ALP (U/L) 51–562 67 50–226 103 .056
LDH (U/L) o100 o100 o100–827 310 .001
Based on a Mann–Whitney U-test between juveniles and adults.
wTest could not be done.
AST, aspartate aminotransferase; ALT, alanine aminotransferase; ALP, alkaline phosphatase; LDH, lactate dehydrogenase.
Vet Clin Pathol 38/2 (2009) 213–218 c2009 American Society for Veterinary Clinical Pathology 215
Casal et al Hematology and biochemistry of sea turtles
juvenile turtles (28%) was higher than that reported
for hatchlings.
RBC count in our juvenile loggerheads was lower
than those reported by Kakizoe et al
7
(36.2 10
10
cells/L)
for the same species, but similar to those reported for
other chelonians.
13
It is uncertain why such differ-
ences were noted. RBC counts of the adult nesting tur-
tles were significantly lower than those observed in the
juvenile turtles. WBC counts in our juvenile logger-
heads were lower than those reported by Raphael
13
for
the same species (14.67 10
9
cells/L). Captivity has
been reported as a possible cause of higher WBC
counts in bog turtles (Clemmys muhlenbergii).
14
The thrombocyte concentration may be difficult to
determine in sea turtles and we are unaware of previ-
ously published values. Thrombocytes from reptilian
species can be difficult to distinguish from lympho-
cytes.
15,16
According to Work et al,
17
thrombocytes
usually retain their morphologic characteristics on
freshly prepared smears. However, if blood smears are
prepared from blood that has been chilled, cellular
shrinkage makes differentiation more difficult, and
their characteristic tendency to aggregate in blood
smears may affect the quality of estimates. We found
similar concentrations of thrombocytes in both juve-
nile and adult nesting loggerhead sea turtles.
In our study, heterophils were the most numerous
leukocytes in juvenile loggerhead turtles, followed by
lymphocytes, similar to that described for loggerhead
turtles.
6
However, lymphocytes were the most numer-
ous circulating leukocytes, followed by heterophils,
eosinophils, azurophils, and basophils in loggerheads
from the East coast of the USA.
18
Lymphocytes were
also the most numerous circulating leukocytes from
green turtles, followed by eosinophils, heterophils, and
monocytes.
17
Differences in the site of blood collection
(with potential for dilution by lymph), criteria used to
identify blood cells, differences in wild-caught vs reha-
bilitated turtles, sex, age, or geographical differences
could explain these different results.
8
In our study,
basophils were scarce in healthy loggerhead turtles,
similar to what was described by Work et al
17
in green
turtles. Cannon
19
did not identify basophils in Kemp’s
Ridley turtles. References on azurophils in the blood of
sea turtles are rare; most authors have not identified
azurophils in sea turtles.
4,6,8,17,19,20
Adult nesting turtles had significantly higher eo-
sinophil counts, and lower heterophil, monocyte, and
lymphocyte counts than the juvenile turtles. Similar
differences have also been described for other reptilian
species.
21
In a previous study on diseases and causes
of mortality among sea turtles stranded in the Canary
Islands, the prevalence of parasitic diseases among
juvenile loggerheads was lower than that observed in
adults.
22
In our study, nesting adult loggerheads had
significantly higher concentrations of total protein,
globulins, albumin, total cholesterol, triglycerides,
and calcium than did juvenile turtles. This finding
has been observed previously in many reptiles, includ-
ing turtles, as a consequence of vitellogenesis and
folliculogenesis.
13,23,24
Increased estrogen is associated
with hyperproteinemia, primarily due to an increase in
globulins necessary for yolk production.
13
A 2–4-fold
increase in the total serum calcium concentration is
associated with an increase in protein-bound calcium
during follicular development before ovulation.
13
Glucose concentrations in adult nesting turtles
were significantly lower than those in juvenile turtles.
This has also been reported in iguanas.
23
Energy re-
quired to complete the nesting process can be high.
25
In addition, the wide range of glucose, triglycerides,
and cholesterol concentrations in juveniles could have
resulted from the time since the last meal in captivity.
In our study, uric acid concentrations in juvenile
loggerheads were similar to those reported previously
for this species.
26
Among the class Reptilia only
chelonids and rhynchocephalids excrete urea as a sig-
nificant fraction of urinary nitrogen.
27
Urea concen-
trations in the adult nesting turtles were significantly
lower than those observed in the juvenile turtles. In a
study on blood biochemistry of the loggerhead sea tur-
tle, Lutz and Dunbar-Cooper
12
reported higher urea
concentrations in the males that were not influenced
by diet.
Bilirubin concentrations were slightly higher in
this study than those in a previous anecdotal report on
this species.
28
Because most turtles produce very little
bilirubin, the bilirubin assay is generally considered to
be of no use in reptile medicine. Creatinine concentra-
tions in both juvenile and adult nesting loggerheads
were also higher than those cited for this species.
28
Regarding plasma enzymes, only LDH activity was
significantly higher in adult turtles. Increases in serum
LDH may be associated in reptiles with damage to the
liver, skeletal muscle, or cardiac muscle.
21
Hemolysis
may also result in increased serum LDH activity
21
;
however, our samples were not hemolyzed.
Acknowledgments
The authors would like to thank Dr. Pascual Calabuig
(TWRC) for the help he offered. They are grateful to mem-
bers of Consejer´ıa de Medio Ambiente, Cabildo Insular de
Gran Canaria, Canary Islands Government, and Cape Verde
Government, for providing us the turtles. This study was
216 Vet Clin Pathol 38/2 (2009) 213–218 c2009 American Society for Veterinary Clinical Pathology
Casal et alHematology and biochemistry of sea turtles
partially supported by the Spanish national project I1D
CGL2004-01111.
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