hematologic and blood chemistry values of healthy cebus flavius kept in...

ORIGINAL ARTICLE

Hematologic and blood chemistry values of healthy Cebusflavius kept in northeast of BrazilMagda Guedes Teixeira1, Adriano Fernandes Ferreira2, Aura Antunes Colac�o3, Sibele FernandesFerreira4, M�arcio Eduardo de Melo Benvenutti5 & Felisbina Luisa Pereira Guedes Queiroga3

1 Department of Veterinary Sciences, University of Tr�as-os-Montes and Alto Douro, Vila Real, Portugal

2 Unidade Acad�emica de Medicina Veterin�aria, Universidade Federal de Campina Grande, Campina Grande, Brasil

3 CECAV, Department of Veterinary Sciences, University of Tr�as-os-Montes and Alto Douro, Vila Real, Portugal

4 Acad�emica de Medicina Veterin�aria da Universidade Federal da Para�ıba Centro de Ciencias Agr�arias, Campus de Areia, Brasil

5 Acad�emico de Medicina Veterin�aria da Universidade Federal de Campina Grande, Centro de Sa�ude e Tecnologia Rural, Campina Grande,

Brasil

Keywords

Cebus flavius – hematology – biochemistry

– hematologic range – blood parameters

Correspondence

Felisbina Luisa Queiroga, CECAV,

Department of Veterinary Sciences,

University of Tr�as-os-Montes and Alto

Douro, 5001-801 Vila Real, Portugal.

Tel: + 351 917826982;

Fax: +351 259350480;

e-mail: [email protected]

Accepted December 17, 2012.

Abstract

Background Cebus flavius is a New World Monkey found in the northeast of

Brazil, listed as critically endangered. So far, no hematologic or blood chem-

istry reference intervals have been determined for this species.

Methods Hematologic and biochemistry reference values were determined

for 20 clinically healthy C. flavius, kept in captivity in the Wild Animals

Screening Center, Jo~ao Pessoa, Para�ıba, Brazil. The influence of gender and

age on these variables was evaluated.

Results Considering sex, significant differences are found for the total count

of erythrocytes, hematocrit, hemoglobin, mean corpuscular hemoglobin, and

creatine kinase. Regarding the age, levels of creatinine and alanine amino-

transferase are significantly higher in adults and levels of creatine kinase and

calcium are significantly higher in juveniles. Considering age, no hematologic

differences were found.

Conclusions The factors age and gender had influence on some hematologic

and blood chemistry variables and should not be neglected for a correct

blood interpretation.

Introduction

Marcgrave’s capuchin monkey (Cebus flavius) is a spe-

cies of the New World Monkeys, exclusively found in

the northeast of Brazil, in the Caatinga and Atlantic

Forest biomes [6].

The first author describing this monkey was George

Marcgrave, a Dutch naturalist, in the book ‘Historiae

Rerum Naturalium Brasiliae’, in the year of 1648 [14]. In

his book, he described the fauna and flora of the Brazil-

ian northeastern Atlantic Forest and described this mon-

key, calling it ‘caitaia’. This species was later referred, in

1774, by Schreber, who called it Simia flavia [14].

In 2006, a group of 18 capuchin monkeys was redis-

covered in the Atlantic coast of the Pernambuco state,

enabling its correct identification and description, and

thus, the classification C. flavius is finally established

[14, 16]. Until now, there were sightings of C. flavius

between the states of Rio Grande do Norte and Ala-

goas, in the Caatinga and Atlantic Forest biomes [6].

Marcgrave’s capuchin monkeys or blond capuchins

(C. flavius) are included in the genus Cebus, subfamily

Cebinae, family Cebidae and Infraorder Platyrrhini,

which comprises the New World Monkeys [13, 15]. All

the platyrrhines belong to the list of the Convention on

International Trade in Endangered Species of Wild

J Med Primatol 42 (2013) 51–56

© 2013 John Wiley & Sons A/S. Published by Blackwell Publishing Ltd 51

J Med Primatol doi:10.1111/jmp.12036

Fauna and Flora (CITES), although not all species are

directly endangered [21].

Cebus flavius is included in the International Union

for Conservation of Nature (IUCN) Red List of

Threatened Species, listed as critically endangered [10].

Currently, it is estimated that there are about 180 indi-

viduals, divided by approximately 24 populations [10]

(M.M. Oliveira, J.P. Boubli, M.C.M. Kierulff 2008, non

published data).

Until now, to the best authors’ knowledge, there

are no hematologic or blood chemistries reference

interval determinations for C. flavius. It is of great

importance to be able to interpret the healthy status

of the captive specimens to reintroduce them or its

offspring into nature. For that, we need to have

available the normal hematologic and blood chemis-

tries range parameters. Therefore, the main objectives

of this study were to provide reference intervals for

hematologic and blood chemistries variables for cap-

tive C. flavius, in the State of Para�ıba, and to find

whether there are significant variations in these values

depending on factors such as sex and age.

Materials and methods

Study subjects

Blood samples collected from C. flavius monkeys, kept

in captivity, in the Wild Animals Screening Center

(CETAS), Jo~ao Pessoa, Para�ıba, Brazil, were studied.

These monkeys came to CETAS either through volun-

tary delivery or after having been confiscated from ille-

gal ownership or illegal trade.

This study is based on data from blood samples col-

lected from November 2010 to May 2011 from 20

healthy Cebus flavius (twelve males and eight females).

The animals were grouped according to the gender

(male and female) and age (adults and juveniles). This

last parameter was estimated according to the assess-

ment of teeth (size, color, wear), body size, and develop-

ment of secondary sexual characteristics [7]. The

animals were identified using a three-letter code tattooed

on the internal face of the right thigh.

This research was conducted in compliance with the

Animal Welfare Act and other federal statutes and regu-

lations concerning animals and experiments involving

animals and adheres to principles stated in the Guide

for the Care and Use of Laboratory Animals (National

Research Council, 2011).

All procedures adopted in this study were approved

by the Bioethics Council from the Federal University of

Campina Grande, Brazil, adhering to the legal require-

ments of this country, and to the American Society of

Primatologists (ASP) Principles for the Ethical Treat-

ment of Non-Human Primates.

Housing and handling conditions

The monkeys were housed in two social groups. In

all groups, there were males, females, adults, and

juveniles. The monkeys from both groups were

housed in an indoor–outdoor cage, furnished with

perches, ropes, slides, and wooden blocks. As the

monkeys were inside of an Atlantic Forest, the tem-

perature is the same as in the natural environment

(19–31°C). The animals were fed ad libitum with sea-

sonal fruit and vegetables, acquired in the same geo-

graphic region, and monkey chow. Water was

provided ad libitum as well.

Veterinary checkup

The monkeys were observed during 3 weeks before

the sampling and physical examination were per-

formed on each animal. All animals were dewormed

with ivermectin one% 21 days before the collection of

blood samples, and the stool samples were subjected

to parasitological examination to ensure that they

were not infected when we performed the blood sam-

pling. According to a basic veterinary examination

(physical examination, body temperature, and fur

condition), all monkeys were considered healthy at

the time of the blood collection. Their good health

status was confirmed by their behavior during the

3 weeks they were observed. The food was withheld

from the animals during the night before the blood

collection.

Blood collection and analysis

All of the animals were captured using nets and anesthe-

tized with ketamine (10 mg/kg), administered IM [21].

Using disposable 12 9 8 syringes and 22-gauge needles,

three mL of blood was obtained from each animal by

venepuncture of the inguinal venous plexus.

The hematologic evaluation was performed soon after

the blood sampling (erythrocyte count, white blood

cells, determination of hemoglobin, hematocrit, mean

hemoglobin concentration (MHC), mean corpuscular

volume (MCV), mean corpuscular hemoglobin concen-

tration (MCHC), and differential leukocyte count).

Erythrocytes and leukocytes were counted in a Neu-

bauer type modified chamber using, respectively, Gower

and Turk [20]. Each one was counted twice, and then,

the middle value was calculated. The microhematocrit

was determined by microcentrifugation at 12,000 rpm.


© 2013 John Wiley & Sons A/S. Published by Blackwell Publishing Ltd52

Hematologic and blood chemistry of Cebus flavius Teixeira et al.

Hemoglobin was performed using the method of

cyanmethemoglobin [20]. The blood smears, to perform

differential leukocyte counts, were made with Diff

Quick staining protocol. Two blood smears were ana-

lyzed, 100 cells were counted in each one of them, and

the middle value was calculated.

For the blood chemistry determinations (blood urea

nitrogen, creatinine, alanine aminotransferase (ALT),

alkaline phosphatase (ALP), total protein, albumin,

globulins, total bilirubin, direct bilirubin, indirect bili-

rubin, gamma–glutamyl transpeptidase (GGT), aspar-

tate aminotransferase (AST), lactate dehydrogenase

(LDH), creatine kinase (CK), calcium, inorganic

phosphorus, glucose), samples were centrifuged at

3000 rpm and the plasma was removed to Eppendorf

tubes and frozen.

The blood chemistries were determined using an auto-

mated analyzer (SBA-200, CELM, Brazil). This ana-

lyzer was subjected to a standard calibration according

to the manufacturer’s instructions. All samples with

hemolysis were excluded.

Statistical analysis

To analyze the impact of sex and age, the following

comparisons were made: males vs. females; adults vs.

juveniles; adult males vs. adult females; adult males vs.

juvenile males.

Medians, minimum, and maximum values were calcu-

lated for each variable, using the software Reference

Value Advisor [22].

Statistical analysis was performed using the Statistical

Package for Social Sciences (SPSS), version 19.0. Mean

values were compared using Student’s t-test. P values

<0.05 were considered to be statistically significant.

Results

A total of 30 hematologic and blood chemistry variables

were studied for each animal, and 20 animals (eight

adult males, seven adult females, four young males, and

one adult female) were analyzed.

The references ranges for the hematologic and blood

chemistry variables were reported as median, minimum,

and maximum and are presented in Table 1.

Table 2 comprises analytes with statistically signifi-

cant differences between classes.

Considering sex as the only variable (males vs.

females), Table 2 shows significant differences in the

hematological variables: erythrocytes, hematocrit,

hemoglobin, and mean corpuscular hemoglobin (higher

in males) and in the blood chemistry parameter creatine

kinase (higher in males).

Considering age as the only variable (adults vs. juve-

niles), Table 2 shows significant differences in the bio-

chemical variables: creatinine and alanine transaminase

(higher in adults), and creatine kinase and calcium

(higher in juveniles). No significant differences in hema-

tological parameters were found.

Considering the association of the two parameters,

sex and age (Table 2), in the subgroup adult males vs.

adult females, significant differences were observed in

hematologic variables concerning erythrocytes, hemato-

crit, hemoglobin, and mean corpuscular hemoglobin

(higher in males). No significant differences in blood

chemistry variables were found.

The subgroup adult males vs. juvenile males (Table 2)

demonstrated no significant differences in hematology;

however, significant differences were observed in blood

chemistry variables for creatinine and alanine transami-

nase (higher in adult males) and creatine kinase and

calcium (higher in juvenile males).

Table 1 Hematological and biochemical range values from 20 blond

capuchin monkeys (Cebus flavius)

Analyte (Conventional Units) Median (Min–Max)

Erythrocytes (9106 cel/mm3) 5.6 (3.9–7.1)

Hematocrit (%) 40.30 (31–47)

Hemoglobin (g/dl) 12.7 (6.8–14.1)

Mean corpuscular volume (fl) 67.9 (62.3–88.9)

Mean corpuscular hemoglobin

concentration (%)

30.1 (23.1–36.4)

Mean corpuscular

hemoglobin (%)

21.8 (14.7–27.9)

Leukocytes (cel/mm3) 11317.9 (4912–20094)

Band cells (cel/mm3) 108.0 (0–339)

Segmented neutrophils

(cel/mm3)

6499.5 (1768.3–11361.2)

Eosinophils (cel/mm3) 259.5 (0–710.0)

Basophils (cel/mm3) 2.8 (0–148.0)

Lymphocytes (cel/mm3) 4155.1 (1535–7563)

Monocytes (cel/mm3) 197.3 (0–630)

Urea (mg/dl) 32.9 (14.4–48.9)

Creatinine (mg/dl) 1.1 (0.5–1.8)

Alanine transaminase (U/l) 34.3 (14.7–54.2)

Alkaline phosphatase (U/l) 120.6 (35.1–206.8)

Total Protein (g/dl) 6.4 (5.3–8.0)

Albumin (g/dl) 3.6 (2.7–4.3)

Globulines (g/dl) 2.8 (1.8–3.9)

Total Bilirubin (mg/dl) 0.3 (0.2–0.5)

Direct Bilirubin (mg/dl) 0.1 (0.1–0.2)

Indirect Bilirubin (mg/dl) 0.2 (0.0–0.3)

Gamma-glutamyl transpeptidase (U/l) 75.3 (42.4–112.0)

Aspartate aminotransferase (U/l) 56.1 (27.1–109.2)

Lactate dehydrogenase (U/l) 348.4 (221.7–477.2)

Creatine kinase (U/l) 330.3 (289.0–415.0)

Calcium (mg/dl) 7.8 (6.5–8.7)

Phosphorus (mg/dl) 3.7 (2.6–4.5)

Glucose (mg/dl) 79.9 (59.1–97.4)



Teixeira et al. Hematologic and blood chemistry of Cebus flavius

Discussion

Although all New World Monkeys species are directly

or indirectly threatened, the species C. flavius stands out

for being included on the IUCN Red List of Threatened

Species, one step away from the extinction in the wildlife

[10, 21]. Because of the limited estimated number of

individuals existing in the entire planet, studies on this

species (from varied areas like biological, behavioral,

and clinical sciences) are compulsory and urgent. Thus,

the knowledge of healthy C. flavius hematologic and

blood chemistry variables is crucial. This information is

necessary to enable the identification of pathological

processes in other captive animals, right from the initial

state of the disease, when there are no other evident

signs. It can help avoiding the evolution of the disease

and the loss of animals, which would contribute to their

extinction.

In the present study, regarding the gender, we found

differences for the hematologic parameters: number of

erythrocytes, hematocrit, hemoglobin, and mean corpus-

cular hemoglobin that were significantly higher in males

in relation to females. These differences are consistent

with studies in other species of the genus Cebus [5, 17, 18,

23]. These variables are influenced by the hematopoietic

system, which regulates the release of erythropoietin, the

bone marrow activity, and iron incorporation in the

erythrocyte. The hematopoietic system is stimulated by

androgens [19]; in addition, the presence of high concen-

trations of natural estrogen in females is demonstrated to

have an inhibiting effect on erythropoiesis, contributing

to lower erythrocyte index [2]. These factors can influence

and contribute to our results.

Regarding the gender, we found statistically signifi-

cant differences in the blood chemistry variable creatine

kinase. This enzyme showed higher values in males than

in females. Because the group males and females include

both ages and this difference is not observed when com-

paring adult male vs. adult females, we believe that this

difference may be due to the age factor.

Table 2 Analytes with statistically significant differences between classes

Median (Min–Max) P

Category Analyte (Conventional Units) Males (N = 12) Females (N = 8)

Sex Hematology

Erythrocytes (9106 cel/mm3) 5.7 (4.9–6.9) 5.4 (4.0–6.2) 0.023

Hematocrit (%) 42.9 (35.0–46.0) 39.6 (33.0–42.0) 0.035

Hemoglobin (g/dl) 12.7 (11.4–13.7) 11.1 (8.7–13.1) 0.041


concentration (%)

30.3 (26.5–36.2) 29.1 (24.9–33.9) 0.043

Biochemistry

Creatine kinase (U/l) 354.0 (289.0–415.0) 321.4 (298.0–341.0) 0.030

Adults (N = 15) Juveniles (N = 5)

Age Biochemistry

Creatinine (mg/dl) 1.2 (0.5–1.9) 0.8 (0.4–2.9) 0.041

Alanine transaminase (U/l) 40.0 (20.0–51.0) 27.30 (21.0–35.0) 0.049


Calcium (mg/d/l) 7.6 (6.9–8.2) 8.3 (8–8.6) 0.004

Adult Males (N = 8) Adult Females (N = 7)

Age/Sex Hematology

Erythrocytes (9106 cel/mm3) 5.1 (4.5–13.8) 5.6 (4–6.2) 0.037

Hematocrit (%) 43.6 (35.0–46.0) 39.4 (33.0–42.0) 0.028

Hemoglobin (g/dl) 12.9 (11.4–13.6) 12.0 (8.7–13.1) 0.044


concentration (%)

30.1 (26.5–36.2) 29.9 (25.6–33.9) 0.049

Adult males (N = 8) Juvenile males (N = 4)

Age/Sex Biochemistry

Creatinine (mg/dl) 1.2 (0.8–1.8) 0.9 (0.7–1.1) 0.036

Alanine transaminase (U/l) 40.3 (31.0–44.0) 24.30 (21.0–35.0) 0.001


Calcium (mg/d/l) 7.5 (7.2–8.1) 8.1 (8.0–8.5) 0.008




Considering age as differential factor, we found no

statistically significant differences in the hematologic

parameters. Regarding the blood chemistry, there were

statistically significant differences between adults and

juveniles concerning creatinine, alanine transaminase,

creatine kinase, and calcium. The same differences were

found when we analyzed only the group formed by

males (removing the influence of different sexes in the

same group), which corroborates these results.

Creatinine was significantly higher in adults than in

juveniles. This difference was also found in other studies

made in Cebus monkeys [12, 23]. This enzyme is a prod-

uct of the conversion of phosphocreatine present in

muscle and it is filtered in the kidney [9]. Once adults

have a larger muscular mass than juveniles, adult ani-

mals have higher levels of creatinine [1,11].

The enzyme alanine transaminase was higher in adults

than in juveniles. We did not find similar results in the

consulted bibliography on the genus Cebus. One of the

authors’ assumptions was that this result may be due to

the feeding behavior of this species. Adults eat before

the young animals, selecting the food that they prefer

first. This behavior can lead to the ingestion of particu-

lar aliments (such as seeds) that may be toxic potential

for the hepatocyte membrane and be no longer accessi-

ble to young animals. However, because this is the first

study on hematologic and blood chemistry variables of

the species C. flavius, we cannot exclude the possibility

that these differences are possibly typical of this species.

Thus, more studies are needed to clarify these differ-

ences.

Creatine kinase values were higher in juveniles than in

adults. One study in the Iberian lynx justified these dif-

ferences arguing that young animals present a greater

physical activity, which results in further release of this

enzyme from the muscle [8]. It is possible that a similar

mechanism occurs in C. flavius.

Calcium presented higher values in young animals

than in adult animals. This difference was also verified

in other studies in Cebus monkeys [5, 17, 23]. Some

authors justify the existence of higher amounts of cal-

cium in young dogs with the existence of higher growth

hormone levels and a greater bone fixation activity. It

contributes to the formation of nuclei of ossification,

bone longitudinal growth, and bone maturation (result-

ing in higher levels of calcium) [3,4]. It is possible that a

similar mechanism may be present in these primates.

The hematologic and blood chemistry values obtained

in this study are, to the best authors’ knowledge, the first

determinations for the C. flavius monkey, an endan-

gered species. We strongly believe that present results

can be applied to wild populations of C. flavius, because

all the animals used in this study come from the Wild

Animals Screening Center (CETAS), Jo~ao Pessoa,

which is located inside of an Atlantic Forest. Therefore,

it provides these animals the same conditions that they

would be subject in the wild (i.e., climatic conditions,

alimentation).

Although further studies are needed to assess the clin-

ical or biological relevance of the differences observed

between the subgroups considered, we believe that the

differences found should be taken into consideration in

the evaluation of the health and physiological status of

the C. flavius species.

Acknowledgments

We thank the technical staff of Centro de Triagem de

Animais Silvestres and Centro de Primatas do Brasil for

help in collecting and processing samples and Dr. Andr�e

Braga for allowing the use of the Laboratory of Clinical

Pathology, University of Pernambuco. We are very

grateful to Thomas Flanigan for help in reviewing the

language. We would also like to thank to Foundation of

Science and Technology, Portugal, for supporting the

study (project_PEst-OE/AGR/UI0772/2011).

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