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Cotton-top tamarins (Saguinus oedipus oedipus) Hematologic reference values and hemopathologic responses.

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American Journal of Primatology 5:231-239 (1983)
Cotton-top Tamarins (Saguinus oedipus oedipus):
Hematologic Reference Values and Hemopathologic
Department of Veterinary Science, Institute of Zoology, Zoological 5'ociet.y of London,
London, England
Hematologic reference values have been established for captive adult cottontop tamarins (Saguinus oedipus oedipus) by carrying out full blood counts
and fibrinogen estimation on 43 clinically normal animals. Females were
shown to have significantly lower hemoglobin levels, red cell counts and
packed cell volumes, and higher reticulocyte counts than males. The reference values were used to identify abnormal changes in the blood of 13
clinical cases. Marked neutrophilia was found in animals with localized
bacterial infections, and a degenerative left shift was recorded in an individual with streptococcal septicemia. Three cases of unexplained progressive
muscle wasting showed Heinz body anemia and abnormal white cell
changes. These hematologic responses have been compared where possible
with those recorded in other species of Callithricidae.
Key words: Cotton-top tamarin, Saguinus oedipus oedipus, bacterial infections, Heinz
bodies, wasting marmoset syndrome, hematuria, myocardial degeneration
Clinical hematology provides a useful aid to differential diagnosis in man and
domesticated animals and should also be of value i n other species including small
primates. Unfortunately lack of normal reference values and of information about
species variations in the response of the circulating blood to different disease processes can make the interpretation of blood counts on sick animals difficult. This
has prevented the utilization of clinical hematology t o its full potential.
Attempts are now being made to remedy this situation. Normal hematologic
reference values have been reported for cotton-top tamarins (Saguinus oedipus
oedipus) [Anderson et al, 1967; Burns et al, 19671, Panamanian tamarins (5'. geoffioyi) [Porter, 19701, white-lipped tamarins (S. nigricollis) [Anderson et al, 19671, red
bellied tamarins (S. Labiatus) [Wadsworth et al, 1982; Hawkey et al, 19831, golden
Received January 27, 1983; accepted June 21, 1983.
Address reprint requests to Dr. C.M. Hawkey, Department of Veterinary Science, Institute of Zoology,
Zoological Society of London, London NW1 4RY, England.
CCJ 1983 Alan R. Liss, Jnc.
Hawkey et a1
lion tamarins (Leontopithecus rosalia) [Bush et al, 19821, and common marmosets
(Callithrix jaccus) [Eccleston, 1977; Sanderson and Phillips, 1981; Hawkey et al,
1982; McNees et al, 19821. Hemopathologic responses have been investigated for
three of these species: the golden lion tamarin [Bush et al, 19821; the red bellied
tamarin [Hawkey et al, 19831; and the common marmoset [Hawkey et al, 19821.
This study reports the results of a further study on cotton-top tamarins in which
abnormalities in the blood count of 13 ill individuals were identified by comparison
with reference values obtained from 43 normal animals and were related when
possible to the clinical diagnosis and/or pathologic findings. In order to begin to
define basic hemopathologic responses in marmosets and tamarins, the abnormal
findings in bacterial infections and wasting syndromes have been compared between
species when appropriate.
Blood samples were obtained from S. oedipus in the collection of the Zoological
Society of London and from animals housed in the Institute of Zoology for reproductive studies. The group included 43 clinically normal adult ( > 1 year) animals and
13 ill individuals admitted to the Animal Hospital for diagnosis and treatment.
Clinical normality was established by careful examination a t the time of sampling
and from knowledge of previous and subsequent clinical histories.
Blood Samples
Using a plastic disposable syringe and disposable 23-gauge needles, 1.0 ml blood
was collected from a femoral vein of each manually restrained or sedated animal.
Sedation was by intramuscular injection of ketamine hydrochloride (Vetalar, Parke
Davis) a t a dose rate of 25-30 m g k g body weight. No significant differences were
found between hematologic values of conscious and sedated animals. The blood was
placed immediately in commercially available plastic tubes containing 1.75 mg of
the dipotassium salt of ethylenediamine tetraacetic acid (EDTA).Tests were carried
out within four hours of obtaining the sample.
Laboratory Methods
These were based on techniques described for use on human blood [Dacie and
Lewis, 19751 and have been detailed elsewhere [Hawkey et al, 19821. Fibrinogen
was estimated as protein precipitated a t 56°C by the micromethod of Millar et a1
Calculation of Reference Values
Values for clinically normal adult males and females were compared by calculating the t statistic for two means. Where no significant sex difference was apparent, results on males and females were combined for calculation of means and
standard deviations (SD). Values falling outside the range of & 2 x SD were
considered to be abnormal [Hawkey et al, 19821.
Normal Blood Cell Morphology
On blood films stained by the May-Grunwald-Giemsa method, red cells of normal animals usually showed slight anisocytosis, poikilocytosis, and polychromasia.
In a few individuals, a small number of nucleated red cells (< 0.02 x 109m were
found. In one clinically normal adult female, Heinz bodies were recorded in 5% of
the red cells. Since there were no associated hematologic abnormalities and the
individual remained healthy, it was included in the reference group.
Cotton-top Tamarin Hematology
The neutrophils were regular, round cells (average diameter 13.0 pm) with welllobulated nuclei (three t o seven lobes, averaging five) and colorless cytoplasm containing numerous small pink or red granules. Eosinophils were similar in size with
irregularly lobed nuclei and pale blue cytoplasm closely packed with small, spherical, strongly eosinophilic granules. The basophils were smaller cells (average diameter 12.1pm) with large, spherical, or oval purple granules completely filling the
cytoplasm. Lymphocytes averaged 12.2 pm in diameter, with round nuclei and pale
blue cytoplasm sometimes containing one or several small azurophilic granules.
Monocytes were larger cells (average diameter 15.8 pm) with indented nuclei and
slightly opaque, blue-grey, sometimes vacuolated cytoplasm. The platelets averaged
3.5 pm in size and contained distinctive basophilic granules.
A small number of microfilaria, thought to be Dipetalonema sp., were found in
the blood of eight of the clinically normal animals. There were no associated hematologic or clinical abnormalities.
Reference Values
Adult males had significantly higher hemoglobin (Hb), red cell counts (RBC),
packed cell volume (PCV), mean cell hemoglobin (MCH) levels, and mean cell
hemoglobin concentrations (MCHC), and lower reticulocyte counts than adult females. The relative (%) but not the absolute number of lymphocytes was significantly
higher in females than in males. Females also had higher absolute eosinophil counts
than males. Neither of these white cell differences was considered to be of biological
Sex differences and calculated reference values for adult males and females and
for the group as a whole are shown in Table I.
Clinical Cases
Blood tests were carried out on 13 animals admitted to the Animal Hospital for
diagnosis and treatment of disease (Table 11). Hematologic abnormalities in these
cases were identified by comparison with the reference values given in Table I. One
of the animals (case 8) was a juvenile for which adult reference may not be valid.
However, the anemia and abnormalities in red cell and neutrophil morphology
recorded in this case were considered unlikely to be related to an age effect. It has
therefore been discussed with the adult group.
For analysis of the hematologic abnormalities identified, the cases have been
grouped according to clinical signs and response to treatment.
Bacterial infections. Bacterial infection as the primary cause of illness was
confirmed in three animals (cases 1, 2, 5) and suspected in another four (cases 3, 4,
5, 7) (Table 11).In four of these cases (1-4), the lesions were localized, the red cells
were normal, but the total white cell counts (WBC) were raised. In cases 1,2, and 4
the leucocytosis was mainly a result of increased neutrophil numbers, although the
neutrophil morphology was normal. Lymphocytosis was the only abnormal finding
in case 3 and was also present in cases 1 and 2. Monocytosis, basophilia, raised
fibrinogen, and thrombocytopenia were each recorded in a single animal (Table 11).
Localized bacterial infection was also suggested by the clinical signs in cases 6
and 7. These two cases showed white cell changes similar to those in cases 1, 2 and
4, but additional minor red cell abnormalities were found. Case 6, although not
anemic, showed Hb, RBC, and PCV levels below the reference ranges, probably due
to chronic blood loss from the skin lesions. In case 7, the increased RBC could be
attributed to hemoconcentration through excessive fluid loss from the gastrointestinal tract.
Hawkey et a1
TABLE 1. Hematologic Reference Values for Adult Cotton-Top, Tamarins
( S a p i n u s oedipus oedipus)
No. and sex
Hemoglobin (g/dl)
25, M
18, F
25, M
18, F
25, M
18, F
25, M
25, M
18, F
25, M
18, F
25, M
18, F
25 M, 18 F
25 M, 18 F
25 M, 18 F
25 M, 18 F
25, M
18, F
25 M, 18 F
25 M, 18 F
25, M
25 M, 18 F
25 M, 18 F
25 M, 18 F
15 M, 13 F
13 M, 11F
Red cell count ( X lO''/L)
Packed cell volume (LA)
Mean cell volume (fl)
Mean cell hemoglobin (pg)
Mean cell hemoglobin
concentration (gidl)
Reticulocytes (%f
ESR (mm in 1 hr)
White cell count ( x lo9&)
Neutrophils ( x lo9/%)
Lymphocytes ( x lo9&)
Monocytes ( x 109/L)
Eosinophils ( X lo9&)
Basophils ( x 109/L)
Neutrophils (%)
Lymphocytes (Q)
Monocytes (%,)
Eosinophils (%)
Basophils (%)
Platelets ( x 1 0 ' 1 ~ )
Fibrinogen (gidl)
0.52"* *
T 1.4
i 1.4
+ 0.03
k 1.3
k 1.3
k 1.5
k 1.1
15.5 - 20.1
13.3 - 18.8
5.7 - 7.7
5.4 - 7.2
0.5 - 0.58
0.3 - 0.53
70.0 - 83.2
23.8 - 28.7
22.2 - 28.1
31.9 - 36.8
31.8 - 35.0
0.7 - 6.2
0.4 - 11.5
4.2 - 11.1
2.10- 8.68
0.91- 4.28
0 - 0.34
0 - 0.30
0 - 0.30
0 - 0.26
53 - 78
10 - 56
15 - 55
0 - 5
0 - 0
0 - 4
195 -607
2.5 - 5.2
Abbruuiatcons: ESR, erythrocyte sedimentation rate [Wintrobe, 19671.
*P < 0.05, **P < 0.01, ***:P< 0.005.
In case 5, a n animal which was tested immediately before it was euthanized
for humane reasons, the WBC and neutrophil counts were within normal limits,
but the neutrophils showed a left shift, and the fibrinogen level was raised. By
analogy with C. jacchus [Hawkey et al, 19821 the results suggested an overwhelming bacterial infection, and this diagnosis was confirmed by the postmortem finding
of streptococcal septicemia. The possible significance of the presence of Heinz bodies
in a small number of red cells in this animal is discussed below.
Generalized wasting. Three animals (cases 8-10) were studied in which the
main abnormal signs were progressive muscle wasting and loss of condition (Table
11). These cases were of particular interest because, as well as having similar
presenting signs, they also showed several features in common with each other and
with S. labiatus and C. jacchus which may have been suffering from wasting
marmoset syndrome (WMS) [Shimwell et al, 1979; Hawkey et al, 1982, 1983). All
three cases showed reduced Hb, RBC, and PCV levels, red cells containing Heinz
bodies, and neutrophilia with a left shift. All three animals died or were euthanized
Cotton-top Tamarin Hematology
in extremis and in two (cases 8 and 9) the cause of the wasting illness was not
found. The third (case 8 ) showed postmortem evidence of peritonitis but this was
considered unlikely to have been the cause of the progressive muscle wasting and
loss of condition. The hematologic findings in these cases are compared with those
on S. labiatus and C. jacchus with generalized signs of wasting in Table 111.
Miscellaneous clinical cases. An adult female (case 11)in which intermittent
hematuria had been noticed for 3 weeks following a cesarian section for removal of
a dead fetus showed red cell abnormalities consistent with compensated chronic
blood loss. Blood coagulation screening tests were normal. Exploratory laparotomy
revealed enlarged blood vessels on the wall of the bladder and adhesions between
the bladder and the wall of the peritoneal cavity. The neutrophilia and monocytosis
seen in this case were not explicable in terms of a concurrent infection. There was
no further hematuria after surgical removal of the adhesions and recovery was
uneventful. A second animal (case 12) in which hematuria was reported showed a
normal blood count and in this case, no abnormalities were detected a t laparotomy.
A male (case 13)which had been successfully treated for severe osteodystrophy five
years previously and which was tested after sudden collapse showed lymphopenia,
neutrophils with a left shift, and a significant number of circulating nucleated red
cells. This animal was euthanized after sampling. A t postmortem examination
there was a large amount of pericardial fat and the myocardium appeared congested. Histologic examination showed evidence of moderate myocardial fibre degeneration; this finding was substantiated by acid fuchsin staining and was
considered to be a contributory cause of morbidity.
The normal adult S. labiatus tested in this survey had lower neutrophil counts
than those studied by Burns et a1 [1967] but otherwise the reference values were
generally similar to those reported for other Callitrichid species [Anderson et al,
1967; Porter, 1970; Eccleston, 1977; Sanderson and Phillips, 1981; Bush et al, 1982;
Hawkey et al, 1982; Wadsworth et al, 19821. The sex differences in Hb, RBC, and
PCV levels are similar to that found in L. rosalia and some other species of primates
[Bush et al, 19821 including man. The validity of the reference values is illustrated
by the fact that they have provided the basis for identification of abnormalities in
the blood of all but one of the clinical cases examined. The single case in which the
blood count was normal was a n animal with transient hematuria in which an
exploratory laparotomy also failed to show any abnormalities (case 12).
As well as the need for valid reference values, a second prerequisite for the
interpretation of blood counts on ill animals is a n understanding of the range and
specificity of hemopathologic responses likely to occur. This information is difficult
to obtain because detailed case histories including hematologic data are rarely
reported. However, the present study of S. oedipus, together with recent surveys
relating blood findings to diagnosis in C. jacchus, L. rosalia, and S. labiatus provides
material for a preliminary comparison of hemopathologic responses in marmosets
and tamarins. Although it is often difficult to find exact clinical parallels between
the species, some apparent similarities and differences are worthy of note.
The group of S. oedipus tested included several animals with localized bacterial
infections in which marked neutrophilia was the most significant finding. Neutrophi1 counts of up to 21 x 109A have been recorded in these individuals, indicating
that the quantitative leucocyte response to infection in S. oedipus can be relatively
large and that white cell counts can be useful in the differential diagnosis of
infection in this species. A similar degree of neutrophilia has been reported in S.
labiatus with infectious conditions [Hawkey et al, 19831 whereas in C. jacchus and
Clinical observations
WBC 21.7t, neutros 12.81,
lymphs 7.8t, monos 0.781
WBC 29.3t, neutros 19.6t,
lymphs 6.2T, basos 0.3t (fibrinogen ND)
WBC 13.7t, lymphs 8.4t
WBC 32.3t, neutros 18.7t,
lymphs 12.61, platelets
11OL, fibrinogen 6.41
Neutros left shift, fibrinogen
5.21, occasional Heinz body
WBC 22.5T, neutros 16.21,
lymphs 5.4t, monos 0.5t,
Hb 14.61, PCV 0.441, MCV
65.51, MCH 21.71 (fibrinogen ND)
WBC 21.71, neutros 16.91,
monos 0.41, RBC 8 . l t , MCV
65.81, MCH 21.71, (fibrinogen ND)
WBC 25.77, neutros 21.9t,
left shift, RBC 3.01, Hb
7.31, PCV 0.231, target
cells +, Heinz bodies 2% of
RBC, retics 9.81, platelets
Recurrent face abscess
Abscess, forelimb
Abscess, face
Abscess, neck
Infected dermatitis, self-inflicted exacerbation
Diarrhea 9/12, proteinuria
Diarrhea, muscle wasting,
loss of condition, alopecia
of tail region
Ad, F
Ad, M
Ad, M
Ad, M
Ad, M
14 Y, M
11-12 y, M
Hematologic abnormalities
Ad, M
Age and
TABLE 11. S. oedipus-Clinical
Euthanasia i n extremis. Peritonitis.
Mesenteric lymph nodes enlarged and
No pathogens isolated from feces. Recovered without treatment.
Euthanasia. Streptococcal septicemia.
Fusion of mandibular joint.
Not known
Staphylococcus aureus and Candida
parupsilosis isolated from lesion. Recovered after antibiotic treatment.
Klebsiella pneumoniae isolated from lesion. Recovered after antibiotic
No organisms isolated. Recovered after
antibiotic treatment.
No organisms isolated. Recovered after
antibiotic treatment.
Transient hematuria
Ad, M
Ad, M
Neutros left shift, lymphs
0.41. nucleated RBC 0.3T
WBC 27.31, neutros 11.71,
lymphs 15.0t, RBC 5.41, Hb
13.61, PCV 0.441, MCHC
30.91, Heinz bodies 2.8% of
WBC 5 6 . l t , neutros 40.47,
left shift, lymphs 15.7t,
RBC 4.81, Hb 12.21,PCV
0.391, MCHC 31.31, retics
8.8t, Heinz bodies 10%of
WBC 16.5t, neutros 11.7t,
monos 0.81, RBC 5.21, Hb
12.91, PCV 0.381, MCHC
31.61, retic 11.3t, nucleated
RBC 0.8t
None (fibrinogen ND)
WBC 22.9t, neutros 15.01,
left shift, lymphs 8.0t, RBC
5.41, Hb 11.81, PCV 0.361,
occasional Heinz body, fibrinogen 7.27, platelets 682T
WBC 3.51, neutros 1.81, RBC
4.21, Hb 8.81,retics 10.4T
Exploratory laparotomy. No abnormalities detected.
Euthanasia. Myocardial failure,
Exploratory laparotomy. Surgical removal of adhesions. Recovered.
Died next day. Generalised muscle
wasting. Lymph nodes enlarged, adrenals congested. Cause of death not
Euthanasia in extremis. Minimal hemorrhagic bladder necrosis. Cause of
morbidity not apparent.
Treated with antibiotics, multivitamins.
Condition improved after antibiotic
Abbreuiations: basos, basophils ( x lo9 L); Hb, hemoglobin (g/dl); lymphs, 1 mphocytes ( x lo9 L);MCH, mean cell volume (fl); MCHC, mean cell hemoglobin
concentration (gidl); MCV, mean cell volume (fl); monos, monocytes ( X 10B L); ND, not done; neutros, neutrophils ( X lo9 L); PCV, packed cell volume (LLL);
RBC, red cell count ( x 10l2L); WBC, white cell count ( X lo9 L); t values above normal; 1 values below normal.
Hematuria, 4 wec--s. Previous cesarian section.
Weight loss. Collapse 6
weeks later.
Loss of condition
Collause. 2 weeks later.
Collapse, loss of condition,
diarrhea. Twin of case 8.
1 Y, M
Hawkey et a1
TABLE 111. Hematologic Abnormalities in S. oedipus, S. labiatus, and C. jacchzts With
Progressive Wasting
No. tested
No. with
Heinz bodies
Left shift
Raised fibrinogen
No. deadb
S. oedipus
S. labiatus
C. jacchus
"Not all animals tested.
bDied or euthanased in extremis.
L. rosalia the neutrophil response to infection is apparently qualitative rather than
quantitative and has been described in terms of a n increased number of band forms
in L. rosalia [Bush et al, 19821 and as a shift to the left in C. jacchus IHawkey et al,
19821. A degenerative shift to the left was found in a n S. oedipus with streptococcal
septicemia (case 5 ) and provided a situation analogous to that described in C. jacchus
with overwhelming infections [Hawkey et al, 19821. Monocytosis and increased
fibrinogen levels have been associated with bacterial infections in all four species
and high platelet counts appear to be a particularly characteristic response in C.
The occurrence of unexplained weight loss and muscle wasting in three of the
S. oedipus studied suggests a parallel with the condition known as WMS described
in C. jacchus [Shimwell et al, 1979; Hawkey et al, 19821 and other related species
[King, 1976; Morin and Spiegler, 1982; Hawkey et al, 19831. Although WMS is
considered to be a n important cause of death among captive marmosets, the clinical
signs of the disease have not yet been defined satisfactorily and the etiology is not
known. Thus, hematologic pointers could be of great value in elucidating this
condition. Our comparisons of blood counts on the three S. oedipus with signs of
wasting with those on S. labiatus and C. jacchus with similar clinical signs confirms
the claim by Shimwell et a1 [19791 that Heinz body anemia is a common finding in
WMS. However, in the present survey, Heinz bodies were found in one healthy
animal and in one ill animal (case 5) in which wasting was not apparent and have
also been reported in normal C. jacchus [Sanderson and Phillips, 1981; Hawkey et
al, 19821. Their presence is therefore apparently not pathognomic for WMS. The
alternative possibility that a shared feature of marmoset and tamarin red cells
renders them particularly susceptible to Heinz body formation and that conditions
triggering the mechanism occur in WMS is currently under investigation.
The white cell changes associated with wasting in the three marmoset and
tamarin species show no consistent pattern. However, the relative frequency of both
quantitative and qualitative neutrophil abnormalities, high fibrinogen levels, and
increased platelet counts suggests that infection may be involved, either as a triggering factor or as a terminal event.
Cotton-top Tamarin Hematology
Taken as a whole, t h e findings reported in this study confirm that normal blood
values in closely related species are similar but that interspecies differences in
hemopathologic responses occur. Further analysis of blood findings on carefully
documented clinical cases is needed to clarify these differences.
1.Hematologic findings on 43 clinically normal adult Saguinus oedipus oedipus
have provided reference values for the identification of hemopathologic changes in
13 ill individuals.
2. Adult females normally have lower Hb levels, RBC, and PCV and higher
reticulocyte counts than adult males.
3. Marked neutrophilia was characteristic of localized bacterial infection. A case
of streptococcal septicemia showed a degenerative left shift of the neutrophils.
4. Three animals with unexplained progressive muscle wasting showed Heinz
body anemia, neutrophilia with a left shift, and several other white cell and platelet
abnormalities. The hematologic findings in these cases were generally similar to
those recorded in S. labiatus and Callithrix jacchus which may have had wasting
marmoset syndrome.
We wish to thank Mr. S. Pugsley and Mr. R. Parsons for postmortem and
microbiological studies and Mrs. B. Murrill and her staff for day to day care of the
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