Evaluation of frequency and intensity of asymptomatic anisocytosis in the Japanese dog breeds Shiba, Akita, and Hokkaido

Abstract

Microcytosis is observed in healthy Japanese breed dogs. The aim of the study was to evaluate the frequency and intensity of asymptomatic anisocytosis using a three-grade scale in Japanese dog breeds with special emphasis on the following indices: mean cell volume, mean cell haemoglobin, mean cell haemoglobin concentration, and red blood cell distribution width. The retrospective study included analyses of blood morphology and blood smear for clinically healthy Japanese dog breeds Shiba, Akita, and Hokkaido aged from 6 months to 14 years, performed as a part of preventative care. A total of 74 dogs of both sexes were qualified for the study. The group included both neutered and non-neutered animals (Akita – 17 females, 12 males, Shiba – 24 females, 18 males, Hokkaido – 2 females, 1 male). The blood smear revealed significant anisocytosis in 60.8% and mild anisocytosis in 28.4% of the tested dogs – 89.2% in total. Microcytosis was reported for 25.7% of the tested Japanese breed dogs. Reduced mean cell haemoglobin and mean cell haemoglobin concentration were diagnosed in 75.7% and 40.5% of dogs, respectively. Red blood cell distribution width as an anisocytosis indicator exceeded the norm in 12% of the tested dogs. Compared to mixed breed dogs, the Japanese breeds had a reduced mean cell volume, mean cell haemoglobin concentration and significant anisocytosis in the blood smear as well as a higher red blood cell distribution width indicator. Veterinarians should consider these differences when interpreting the results of morphological blood tests.

Full text

Evaluation of frequency and intensity of asymptomatic anisocytosis
in the Japanese dog breeds Shiba, Akita, and Hokkaido
Olga Aniołek1,2, Agnieszka Barc3, Anna Jarosińska3, Zdzisław Gajewski1,2
Warsaw University of Life Sciences – SGGW, Faculty of Veterinary Medicine,
1Department of Large Animal Diseases, 2Veterinary Research Centre,
3Scientic Circle of Veterinary Students,
Warsaw, Poland
Received May 4, 2017
Accepted December 19, 2017
Abstract
Microcytosis is observed in healthy Japanese breed dogs. The aim of the study was to
evaluate the frequency and intensity of asymptomatic anisocytosis using a three-grade scale in
Japanese dog breeds with special emphasis on the following indices: mean cell volume, mean
cell haemoglobin, mean cell haemoglobin concentration, and red blood cell distribution width.
The retrospective study included analyses of blood morphology and blood smear for clinically
healthy Japanese dog breeds Shiba, Akita, and Hokkaido aged from 6 months to 14 years,
performed as a part of preventative care. A total of 74 dogs of both sexes were qualied for
the study. The group included both neutered and non-neutered animals (Akita – 17 females, 12
males, Shiba – 24 females, 18 males, Hokkaido – 2 females, 1 male). The blood smear revealed
signicant anisocytosis in 60.8% and mild anisocytosis in 28.4% of the tested dogs – 89.2% in
total. Microcytosis was reported for 25.7% of the tested Japanese breed dogs. Reduced mean cell
haemoglobin and mean cell haemoglobin concentration were diagnosed in 75.7% and 40.5%
of dogs, respectively. Red blood cell distribution width as an anisocytosis indicator exceeded
the norm in 12% of the tested dogs. Compared to mixed breed dogs, the Japanese breeds had
a reduced mean cell volume, mean cell haemoglobin concentration and signicant anisocytosis
in the blood smear as well as a higher red blood cell distribution width indicator. Veterinarians
should consider these dierences when interpreting the results of morphological blood tests.
MCH, MCHC, red blood cell distribution width
Red cell distribution width (RDW) as an anisocytosis indicator is a quantitative measure
of the range of variation of the circulating red blood cells (Nei ger et al. 2002; Ho dge s
and Ch ris t oph er 2011; Mo nta g nan a et al. 2012; Ma zzo t ta et al. 2016). It is a routinely
measured indicator by haematology analysers (Li p pi and P leb a ni 2014). This indicator
is usually elevated when insucient total red blood cell count (RBC) production is
observed as a result of e.g. vitamin B12 or iron deciency, exacerbated red cell destruction,
haemolysis, after a blood transfusion or in severe inammatory states. Changes in this
indicator are observed in the course of numerous systemic conditions such as renal diseases
or nutrition shortages (He llh a mme r et al. 2016). Increased RDW is also observed in cases
of RBC deformability (Patel et al. 2013). It is also treated as an indicator for evaluation
of red blood cell functionality (Pate l et al. 2013; Lip p i et al. 2014). Red cell distribution
width is a valuable prognostic lethality marker for humans in the course of heart diseases
(Cam por a et al. 1987; Felke r et al. 2007; Au n g et al. 2013). Changes in the haematology
for dierent dog breeds have been documented. Separate referential values were
established for Greyhounds, which have higher haematocrit (HCT), mean cell volume
(MCV) and haemoglobin (HGB) concentration and a lower total platelet count (PLT) and
total white blood cell (WBC) count compared to other breeds (Por t er and Ca nad a y 1971;
Sullivan et al. 1994; Guyton and Hall 2006; Campora et al. 2011; Zaldivar-Lopez
et al. 2011). Physiological macrocytosis was diagnosed in miniature breeds and standard
ACTA VET. BRNO 2017, 86: 385–391; https://doi.org/10.2754/avb201786040385
Address for correspondence:
Olga Aniołek
St. Nowoursynowska 100
02-797 Warsaw, Poland
Phone +48 (22) 593 60 92
E-mail: olgaaniolek@op.pl
http://actavet.vfu.cz/

poodles (Schal m 1976). Compared to mixed breed dogs, Dachshunds have a higher
mean platelet volume (MCV), HCT, RBC and a higher HGB concentration (Torr e s et al.
2014). Idiopathic thrombocytopaenia connected to beta-tubulin mutation in Cavalier King
Charles Spaniels (S ingh and La mb 2005; Davi s et al. 2008) or microcytosis in Asian
dog breeds reported in literature (Tanabe 2006; B a tti son 2007) can serve as another
example. Increased popularity of breeds such as Shiba or Akita has been recently observed
in Poland, sparking the need to analyse asymptomatic microcytosis in more detail. The
aim of the study was to evaluate the frequency and intensity of asymptomatic anisocytosis
using a three-grade scale in Japanese dog breeds with special emphasis on the indices of
MCV, mean cell haemoglobin (MCH), mean cell haemoglobin concentration (MCHC),
and RDW.
Materials and Methods
Sample collection
Blood samples were taken from clinically healthy dogs aged 6 months to 14 years (median 2.5 years; Akita –
median 2 years; Shiba – median 4 years; Hokkaido – median 5 years) as a part of animal preventative care. The
study was conducted at the Department of Animal Diseases with Clinic of Warsaw University of Life Sciences,
in the years 2016–2017. The majority of dogs were born on breeding farms and had appropriate documents
certifying their breed. The dogs came from both Polish and foreign breeders. A total of 74 dogs of both sexes,
neutered and non-neutered, were qualied for the study (Akita – 17 females, 12 males, Shiba – 24 females, 18
males, Hokkaido – 2 females, 1 male). Their health condition was conrmed by a veterinarian based on an overall
clinical examination following an interview with special emphasis on the history of diseases and undergone
treatments. The blood samples for haematological analysis were collected into tubes with ethylenediamine
tetraacetic acid (EDTA) anticoagulant from the cephalic vein. The storage time for the samples before analysis
did not exceed 4 h.
Haematological analysis
Quantitative examination of the peripheral blood was performed using a veterinary haematology analyser
(Mindray, BC- 2800 Vet). The following indices were evaluated: total white blood cell count (WBC),
lymphocytes (LIMF), monocytes (MON), granulocytes (GRAN), total red blood cell count (RBC), haemoglobin
(HGB), haematocrit (HCT), mean cell volume (MCV), mean cell haemoglobin (MCH), mean cell haemoglobin
concentration (MCHC), red cell distribution width (RDW), total platelet count (PLT), mean platelet volume
(MPV), platelet distribution width (PDW), platelet haematocrit (PCT).
Qualitative study was performed after staining the samples using Hemacolor® (HEMAVET, Kolchem Polska).
Stained blood smears were evaluated under a light microscope equipped with a camera (Olympus, BX 43)
and photographic documentation was created (Olympus, cellSens Standard). The rst stage of the qualitative
evaluation involved estimating the number of leukocytes with regard to the populations as well as estimating the
platelet count and platelet morphology. Subsequently, attention was focused on the qualitative evaluation of the
erythrocytic system. The erythrocyte morphology evaluation involved evaluation of the erythrocyte size, shape,
colouring and presence of possible cell inclusions. Thereafter, the microcytes visible in the standard eld of view
at × 100 magnication were counted. The following assumptions were made: up to 3 microcytes in the standard
eld of view – no anisocytosis, up to 7 – mild anisocytosis, more than 7 – signicant anisocytosis. Qualication
of the red blood cell as microcytes was performed on the basis of comparison of the erythrocyte’s diameter to the
mean erythrocyte diameter – normocyte – in the observer’s standard eld of view.
Statistical analysis
The statistical analysis was performed using statistical software. The MCH indicator was characterised by
normal distribution. Kruskal-Wallis nonparametric test was applied for indices characterised by non-normal
distribution, that is: MCH, MCHC, RDW and anisocytosis. The analysis of the selected indices of the erythrocytic
system (MCH, MCHC, RDW, anisocytosis) was performed in total for all the qualied samples as well as with
regard to the breed, sex and age within the given breed.
Results
Qualitative evaluation of blood smears revealed signicant anisocytosis in 60.8% and
mild anisocytosis in 28.4% of the tested dogs. Mild and signicant anisocytosis was
diagnosed in 33.3% and 50% of Shiba males, respectively. In females, this percentage was
equal to 33.3% and 50%. Mild anisocytosis was diagnosed in 33.3% of Akita males and
386

in 17.64% of females. Signicant anisocytosis was observed in 76.47% of Akita females.
Microcytosis diagnosed on the basis of the MCV indicator evaluation was present in 25.7%
of the cases (referential range 62–72 , minimum: 55.7 , maximum: 79.9 , median: 64.3
, standard deviation: 5.117), whereas anisocytosis indicator RDW exceeded the norm
for 12% of the dogs (referential range: 11–15.5%, minimum: 11.7%, maximum: 17.1%,
median: 14%, standard deviation: 1.135). A reduced MCV value for the Shiba breed was
conrmed in 22.2% of males and 20.8% of females; for the Akita breed in 29.4% of females
and 25% of males. For the Hokkaido breed, the values were reduced for 66% of females.
Anisocytosis identied using the RDW indicator was conrmed for 11.6% of males and
16.6% of females of the Shiba breed and for 5.88% of females and 8.3% males of the Akita
breed.
Reduced MCH and MCHC values were noted for 75.7% and 40.5% dogs, respectively
(MCH referential range: 20–25 pg, minimum: 17.3 pg, maximum: 22.4 pg, median: 19.1
pg, standard deviation: 1.092; MCHC referential range: 300–380 g/l, minimum: 232 g/l,
maximum: 340 g/l, median: 301 g/l, standard deviation: 20.255). Mean cell haemoglobin
was noted for 44.4% Shiba males and 79.1% Shiba females; 82.5% females and 100%
males of the Akita breed; and 100% Hokkaido females. Reduced MCHC was diagnosed
in 33% Shiba males and 61.1% Shiba females, 47% Akita breed females and 33% Akita
males, and 33% Hokkaido females. Dogs under the age of 1 year showed no statistically
signicant dierences in the values of the erythrocytic system. All results are listed in the
Table 1.
Discussion
The Japanese dog breeds Akita, Shiba and Hokkaido belong to the ancient Spitz
type, relatively untouched by human breeding. In this study, the blood samples
were taken from clinically healthy dogs aged from 6 months to 14 years. Even
though the age distribution in the tested animals was wide, a recent study did not
demonstrate a signicant RDW dierence between puppies and adult dogs (R ort v eit
et al. 2015). However, no data on RDW changes in old dogs are available. A MCV-
based microcytosis was detected in 25.7% of the tested animals, which constitutes
a signicant percentage of the Japanese dog breed population. The results of the test
including various dog breeds, indicated that the percentage of dogs with microcytosis
is equal to 8.5% (86/1012). In cases where other indices of the erythrocytic system
were also reduced, indicating anaemia, the percentage was equal to 47.8% of 86 cases
(Per uzz i et al. 2010). Possible causes of microcytosis in dogs may be chronic iron
deciency, portacaval shunt, anaemia caused by inammatory processes, prolonged
treatment using recombined erythropoietin, copper deciency, medicinal preparations
or components inhibiting hem synthesis, myeloproliferative disorders with iron
metabolism impairment, pyridoxine deciency, and hereditary elliptocytosis in dogs.
The test group for this study consisted of clinically healthy dogs, whose condition
was assessed on the basis of an interview and a clinical test. The RDW was correlated
negatively with haematocrit and haemoglobin concentration. No correlation between
RDW and MCV was noted by M azz o tta et al. (2016), in contrast to the previous
studies by other authors (Fig. 2), both in humans and dogs (Ha mpol e et al. 2009;
Gug lie l min i et al. 2013; Swan n et al. 2014). Reasons for this divergence remain
unclear. The presented study methods have their limitations. The obtained data (apart
form MCV) are not characterised by normal distribution, therefore in order to identify
separate referential values, it is necessary to test a larger group of Japanese breed
dogs. Vitamin B12 concentration as well as serum iron concentration levels were not
evaluated. It is known that the red blood cell count and HGB concentration were lower
387

388
Indicator Breed N Mean ± SD Min Max Range
WBC (109/l) Akita 29 12.4 (±5.9) 5.5 28.2 6.0-17.0
Shiba 42 11.6 (±3.2) 5.8 21.2
Hokkaido 3 11.8 (±4.6) 6.5 15
LYMPH (109/l) Akita 29 3.6 (±2.4) 1 11.5 0.8-5.1
Shiba 42 2.7 (±1.3) 0.9 7.7
Hokkaido 3 3.1 (±1) 2 3.8
MON (109/l) Akita 29 0.6 (±0.3) 0.2 1.2 0.0-1.8
Shiba 42 0.5 (±0.2) 0.2 1.3
Hokkaido 3 0.7 (±0.1) 0.6 0.8
GRAN (109/l) Akita 29 8.3 (±4.3) 3.4 19.8 4.0-12.6
Shiba 42 8.4 (±2.2) 3.9 15.6
Hokkaido 3 8.0 (±3.6) 3.9 10.5
%LYMPH (%) Akita 29 28.6 (±10.8) 8.8 52.9 12.0-30.0
Shiba 42 21.8 (±7.5) 3.4 41.8
Hokkaido 3 27.5 (±3.2) 25.6 31.2
%MON (%) Akita 29 4.7 (±1.3) 2 7.7 2.0-9.0
Shiba 42 4.6 (±0.9) 2.8 7.4
Hokkaido 3 6.7 (±2.4) 4.9 9.4
%GRAN (%) Akita 29 66.7 (±11) 43.1 89.2 60.0-83.0
Shiba 42 72.9 (±7.3) 54.1 85.9
Hokkaido 3 65.8 (±5.6) 59.4 69.5
%EOS (%) Akita 29 2.9 (±2.9) 0.5 13.7
Shiba 42 3.6 (±7.9) 0.6 50.8
Hokkaido 3 1.4 (±0.1) 0 2.2
RBC (1012/l) Akita 29 7.4 (±0.1) 5.2 8.9 5.50-8.50
Shiba 42 7.9 (±1.2) 4.5 10.3
Hokkaido 3 7.8 (±3) 4.5 10
HGB (g/l) Akita 29 138.9 (±20.2) 97 174 110-190
Shiba 42 156.8 (±20.1) 119 187
Hokkaido 3 147.0 (±54.3) 85 186
HCT (%) Akita 29 46.8 (±6.3) 34.3 59.5 39.0-56.0
Shiba 42 52.7 (±6.1) 41.4 64.9
Hokkaido 3 48.3 (±17.6) 28.4 61.6
MCV () Akita 29 63.8 (±4.5) 55.7 79.9 62.0-72.0
Shiba 42 66.6 (±5.8) 55.7 79.6
Hokkaido 3 61.8 (±1.9) 55.9 63.6
MCH (pg) Akita 29 18.8 (±0.8) 17.3 20.4 20.0-25.0
Shiba 42 19.3 (±2) 8.7 22.4
Hokkaido 3 18.7 (±0.3) 18.5 19
MCHC (g/l) Akita 29 296.2 (±13.1) 251 312 300-380
Shiba 42 292.3 (±36.9) 113 340
Hokkaido 3 303.0 (±5.3) 299 309
Table. 1 Haematologic indices of the Akita, Shiba, and Hokkaido breeds.

than those in mixed breed dogs with high potassium concentration (HK), whereas
MCV was higher when compared with dogs with low potassium concentration (LK)
belonging to the same family (Ma ede et al. 1983). The HGB concentration, PCV,
389
Indicator Breed N Mean ± SD Min Max Range
RDW (%) Akita 29 13.7 (±1.1) 12 15.6 11.0-15.5
Shiba 42 14.6 (±1.5) 11.7 21.3
Hokkaido 3 13.8 (±0.8) 13.4 14.7
PLT (109/l) Akita 29 185.0 (±80.8) 28 342 117-460
Shiba 42 290.6 (±71) 143 461
Hokkaido 3 303.0 (±178.4) 108 458
MPV () Akita 29 9.4 (±1.1) 7.6 11.1 7.0-12.9
Shiba 42 9.4 (±0.7) 8.2 10.9
Hokkaido 3 8.0 (±0.9) 7.3 9
PDW (%) Akita 29 16.4 (±0.4) 15.8 17.3
Shiba 42 16.0 (±0.3) 15.5 16.8
Hokkaido 3 15.9 (±0.6) 15.5 16.6
PCT (%) Akita 29 0.2 (±0.1) 0.1 0.3
Shiba 42 0.3 (±0.2) 0.2 0.4
Hokkaido 3 0.2 (±0.1) 0.1 0.4
Table. 1 Haematologic indices of the Akita, Shiba, and Hokkaido breeds.
WBC – total white blood cell count; LYMPH – lymphocytes; MON – monocytes; GRAN granulocytes;
% LYMPH – % lymphocytes; % MON – % monocytes; % GRAN – % granulocytes; % EOS – % eosinophils;
RBC – total red blood cell count; HGB – haemoglobin; HCT – haematocrit; MCV - mean red blood cell volume;
MCH – mean cell haemoglobin; MCHC – mean cell haemoglobin concentration; RDW – red cell distribution
width; PLT – total platelet count; MPV – mean platelet volume; PDW – platelet distribution width; PCT – platelet
haematocrit; SD – standard deviation
B
A
Fig. 1. The results of mean red blood cell volume (MCV) for (A) the Shiba, Akita, and Hokkaido breeds; and (B)
all the breeds combined

RBC and MCHC were signicantly lower with HK in comparison with LK dogs and
often were lower than the referential values (Conra do et al. 2014). Mean MCV in HK
dogs was signicantly higher than in LK dogs, nonetheless, the values were within
the referential range (K ane k o et al. 2008). The HK phenotype dog studies revealed
that HGB, PCV, RBC and MCHC values may be lower in those animals. This suggests
that the increase in intracellular uids may cause lower MCHC and higher MCV in
those animal in regard to the normal range of the other variables (Ma ede et al. 1983;
Bat tis o n 2007). This may also lead to osmotic changes within red blood cells. In this
study, the reduced values of MCH and MCHC indices were diagnosed in 75.7% and
40.5% dogs, respectively. Up to this point, HK phenotype was described in 10 out of
13 Japanese breeds and the frequency of its occurrence in the Akita breed is equal to
26.3% (Tana b e 2006) and 20% according to F ujis e et al. (1997) and C onra do et al.
(2014). This study did not evaluate K and Na ion concentrations, though it is known
that Akita HK phenotype is distributed worldwide. In comparison to mixed breed dogs,
dogs of the Japanese breeds have reduced MCH, MCHC and signicant anisocytosis
in the blood smear and a higher RDW indicator. Veterinarians should consider those
dierences when interpreting blood morphology test results.
Conict of interest
The authors have no aliations or nancial involvement with any organization or entity with a nancial
interest in, or in nancial competition with the subject matter or materials discussed in this article.
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Fig. 2. Correlation between mean red blood cell volume (MCV) and anisocytosis. Correlation r = -0.2342;
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