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Hematological parameters in Oreochromis niloticus cultivated in tropical

conditions in experimental farm Santo Domingo of University of Amazonia,
Florencia, Caquetá, Colombia.

Article in Scientia et technica · March 2019

DOI: 10.22517/23447214.20391

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Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira. ISSN 0122-1701 y ISSN-e: 2344-7214 126

Hematological parameters in Oreochromis

niloticus cultivated in tropical conditions in
experimental farm Santo Domingo of University
of Amazonia, Florencia, Caquetá, Colombia
Parámetros hematológicos en Oreochromis niloticus cultivada in condiciones
tropicales en la Granja Experimental Santo Domingo de la Universidad de la
Amazonia, Florencia- Caquetá, Colombia

L. V. Galindo-Peña , F.D. Pérez-Cuervo , A. M. Poche-Ceballos , E. Martinez-Moyano

, J. H. Hernandez-Sanchez , B. Murcia-Ordoñez , L. C. Chaves-Moreno

Abstract— The hematological parameters were evaluated in the Index Terms—Oreochromis niloticus, Leukogram, Eritogram,
Oreochromis niloticus species, weighing between 120 and 375 g, Anemia, Ema staining color.
where chemical standards of water were included (T °, pH and
OD), morphometry and haematological diagnosis, carried out at Resumen— Se evaluaron los parámetros hematológicos en la
the Santo Domingo Experimental Farm from the University of the especie Oreochromis niloticus, con peso entre los 120 y 375 g, donde
Amazonia, Florencia - Caquetá-Colombia. A directed and se incluyeron estándares químicos del agua (T°, pH y OD), la
completely random sampling of 32 individuals was used, the blood morfometría y el diagnóstico hematológico, realizados en la
was extracted by cardiac puncture and placed in Eppendorf tubes Granja Experimental Santo Domingo de la Universidad de la
with EDTA. Blood smears were stained with Ema staining color Amazonia, Florencia- Caquetá-Colombia. Se utilizó un muestreo
for its laboratory analysis. The InfoStat was applied as a statistical dirigido y completamente al azar de 32 individuos, la sangre fue
method for the analysis of the variables to be measured. A total of extraída por punción cardiaca y colocada en tubos Eppendorf con
leukocytes of 1.11 celx105 / mm3 was found, predominating EDTA. Los frotis sanguíneos se tiñeron con coloración Ema color
neutrophils with 49.3% followed by lymphocytes with 38.8%, tinción para su análisis en laboratorio. Se aplicó el InfoStat como
monocytes with 5.9%, eosinophils with 4.3%, basophils with 1.7 % método estadístico para el análisis de las variables a medir. Se
encontró un total de leucocitos de 1,11 celx105/mm3,
and thrombocytes with 63.8% as an independent series. For the
predominando los neutrófilos con 49,3% seguido de linfocitos con
red series, an average of erythrocytes of 1.5 celx106 / mm3,
38,8%, monocitos con 5,9%, eosinófilos con 4,3%, basófilos con 1,7
hemoglobin of 7.9 g / dL; hematocrit of 23.3%, plasma proteins 3.3 % y trombocitos con 63,8 % como serie independiente. Para la
g / dL, mean corpuscular volume 165 (u3), mean corpuscular serie roja se encontró un promedio de eritrocitos de 1,5 celx10 6
hemoglobin 55 (uug) and mean corpuscular hemoglobin /mm3, hemoglobina de 7.9 g/dL; hematocrito de 23.3%, proteínas
concentration of 33.3%. In conclusion, it was determined that plasmáticas 3,3 g/dL, volumen corpuscular medio 165 (u3),
some individuals presented Leukopenia with Lymphopenia and hemoglobina corpuscular media 55 (uug) y concentración de
thrombocytosis. In addition, two individuals presented hemoglobina corpuscular media de 33.3%. Como conclusión se
Normochromic Microcytic Anemia (AMN) and 19 individuals determinó que algunos individuos presentaron Leucopenia con
presented Normochromic Normocitic Anemia (ANN). The Linfopenia y trombocitosis. Además, dos individuos presentaron
analysis of Total Plasma Proteins (PPT) determined that the high Anemia Microcítica Normocrómica (AMN) y 19 individuos
mortality rate was not due to nutritional deficiency. There was a presentaron Anemia Normocitica Normocrómica (ANN). El
positive similarity between the VCM and HCM, and negatively análisis de Proteínas Totales del Plasma (PPT) determinó que la
with the total number of erythrocytes. alta tasa de mortalidad no fue por deficiencia nutricional. Se

This manuscript was sent on December 07, 2019 and accepted on March 28, J. Hernandez-Sanchez, ESP. Computer science engineer.
2019. ([email protected])
L. Galindo-Peña, Biologist, Research group of Biodiversidad y Desarrollo B. Murcia-Ordoñez, Biologist, Research group of Biodiversidad y Desarrollo
Amazónico (BYDA). Universidad of the Amazonia. Florencia-Caquetá. Amazónico (BYDA). Universidad of the Amazonia. Florencia-Caquetá 4MSc
([email protected]) in Sciences, Professor of the Basic Sciencies Faculty, Biology program.
F. Pérez-Cuervo, Biologist, Research group of Biodiversidad y Desarrollo ([email protected])
Amazónico (BYDA). Universidad of the Amazonia. Florencia-Caquetá. L. Chaves-Moreno, Research group of Biodiversidad y Desarrollo Amazónico
([email protected]) (BYDA). Universidad of the Amazonia. Florencia-Caquetá, MSc in Amazonic
A. Poche-Ceballos, Biologist, Research group of Biodiversidad y Desarrollo studies, Professor of the Agricultural Sciences Faculty, Veterinary medicine
Amazónico (BYDA). Universidad of the Amazonia. Florencia-Caquetá Y 5Esp. and Zootechnics program. ([email protected])
Clinical Laboratory. ([email protected])
E. Martinez-Moyano, Biologist, Research group of Biodiversidad y Desarrollo
Amazónico (BYDA). Universidad of the Amazonia. Florencia-Caquetá.
([email protected])
 Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira
127

presentó una similitud positiva entre el VCM y HCM, y de forma ichthyofauna. Its main function lies in the transport of oxygen
negativa con el número total de eritrocitos. to tissues and CO2 to the lungs for proper elimination. On the
other hand, white blood cells or leukocytes are widely used as
Palabras claves— Oreochromis niloticus, Leucograma, an indicator of health in fish because they are the units of
Eritrograma, Anemia, tinción Ema color.
defense against pathogens and are involved "in the
I. INTRODUCTION
immunological regulation" of the organism. Likewise,
thrombocytes act in the coagulation processes [12]. A blood
ILAPIA is the common name of a group of species
T belonging to the family Cichlidae, of which, the genus
Oreochromis represents the main source of income and
count can be very beneficial for the diagnosis of anemia and
stress states, in addition to knowing and evaluating the
conditions of the aquatic environment in which they are found,
therefore is categorized as fish of greater commercial relevance in order to determine a possible bacterial septicemia. A
in aquaculture; Therefore, at the global level, they appear as the characteristic to be taken into account is that erythrocytes and
third most important group, after carp and salmon, and their thrombocytes in fish have a characteristic of being nucleated, a
cultivation presents one of the fastest growing activities feature that does not occur in mammals [9] - [13].
worldwide [1] - [2].
Thus, this study projected to present a hematological analysis
However, the research that has been conducted in areas such in individuals of Oreochromis niloticus, in order to establish
as ichthyophysiology and ichthyopathology of species of their blood values under tropical conditions, as well as the
productive and economic importance (such as Tilapia) under possible pathologies present in individuals.
tropical conditions are very scarce, this has brought serious
consequences in the national fish sector as it locates it at a II. METODOLOGY
certain disadvantage compared to other countries, in which,
A. Study area
research in this area has some relevance and correlation with its
fishing production [3]. Likewise, from the productive point of
The study was conducted at the Santo Domingo fish station
view, it is gradually becoming an alternative source of protein
experimental farm of the University of Amazonia, located
of great relevance for the most vulnerable population, but at the
between the geographical coordinates 1 ° 36'26 "of Latitude
same time it guarantees income and a formal employment to
North, and 75 ° 46 '1.63" of West longitude, 7 km from the City
these people, which is verified in the gradual increase of fish
of Florencia on the road that connects with the municipality of
culture of 12% per year (average) between the years of 1990
Morelia. The region is classified as a tropical humid forest, it
and 2011, data that allow establishing tilapia as the second
has an average annual rainfall of 3600 mm3, an average relative
species of commercial importance [4] - [5] - [6].
humidity between 80% and 85% and an average annual air
temperature of 28 ° C. The fish were cultivated under optimal
However, like any production, fish farming demands "precise,
conditions of oxygen (4.40 mg / L), temperature (26.5 ° C), pH
effective and low-cost tools" that allow a diagnosis and constant
(5.99-7.1) and feeding (4% biomass / daily); Later, they were
monitoring of production indices; for this, the complete and
transferred to the animal physiology laboratory of the
detailed study of the chemical and haematological parameters
University of Amazonia (FA-UA) in Florencia-Caquetá, where
compose an accessible and important strategy that acts as a
the samples were taken and analyzed respectively [14].
bioindicator for the detection of pathologies that come to harm
in fish production [4] - [7], since fish are susceptible to
B. Sampling
problems of nutritional imbalance, anoxic conditions, stress
effects, chemical products, intoxication, genetic variability,
To minimize the stress of the fish at the time of sampling and
attack and invasion of pathogens (bacterial, parasitic, viral), and
change of environment, they were anesthetized with Eugenol in
environmental changes in populations that live in a natural state
relation to 1mg / 20L of water. The extraction of the blood was
or in confinement [4] - [8].
done using the cardiac puncture methodology used by [4], [13],
[15] using disposable syringes of 1 cc, with hypodermic needles
That is why a study of blood physiology is transcendental,
and collected in Eppendorf tubes with EDTA solution for
since changes in the intrinsic and extrinsic character of the
subsequent hematological analysis.
environment are rapidly and efficiently reflected in the blood
[9]. Therefore, it becomes essential, in a first scenario, to
identify and establish the "normal" haematological parameters C. Morphmetric parameters
for the tropics, which will support the examination of the
species, such as Nile Tilapia (Oreochromis niloticus), in order A Ubermann digital caliper and a millimeter ruler were used for
to look for an improvement in the quality and production of measurements of total length, standard length, head width, body
species for the region [3] - [10] - [11]. width, body height and head length for all individuals; In
addition, in order to determine the weight, an Electronic Scale
In the framework of the study of blood physiology, it is was used [16].
essential to evaluate standard parameters that indicate in a
timely and accurate manner the pathological phenomena that
develop in the individual; For example, red blood cells, also
called erythrocytes, are the most abundant blood cells in most
Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira 128

D. Hematological Analysis
E. Statistic analysis
To perform the blood smears the methodology proposed by
[17] was used, a direct total cell count was performed by the For the analysis of the information obtained from the 32 fish,
Hemocytometer method using a dilution of Natt-Herrick diluent a guided sampling and descriptive statistical methods were used
for three minutes and placed in a Neubauer chamber, which to analyze the variables to be measured: hematocrit,
allows to stain the cells differentially to visualize them. The hemoglobin; erythrocytes, MCV, HCM, CHCM, leukocytes;
direct differential cellular study in the blood smear was (heterophiles, lymphocytes, eosinophils, monocytes) and
performed in an optical microscope with a built-in digital thrombocytes used by [9], [18] likewise, the statistical software
camera. The blood smears were stained with Hemacolor
InfoStat was used.
staining as [4] stipulates it. With regard to the indirect count of
leukocytes in the blood smear, the parameters were evaluated
III. RESULTS AND DISCUSSION
according to the methodology proposed by [3].
The individuals studied had an average weight of 208.75 ±
66.73 and an average total length of 22.14 ± 1.98 presented in
Table I coinciding with the values recorded by [4], which in
turn were similar with those reported by [19].
TABLE I
MORPHOMETRIC DATA OF THE O. NILOTICUS INDIVIDUALS.

Weight Total Standard Length Width Width Height

(gr) length length of the of the of the of the
(cm) head head body body
Average 208,75 22,14 19,11 53,47 32,28 28,22 73,48
Máximum 375 26,4 49,6 64,93 39,82 35,27 90,45
Mínimum 120 18,7 14,6 30,51 22,6 23,75 60,62
Standard 66,73 1,98 5,93 6,82 4,08 2,88 7,33
deviation

The analysis of conglomerates by the Ward method and the evidenced the formation of four groups; group number one (1)
Euclidean distance made for the Hematological parameters in with 15 individuals who presented the highest values, group
Nilotic Tilapia (Oreochromis niloticus) individuals cultivated two (2) and three (3) with average values; while group number
in Santo Domingo farm, Florencia- Caquetá, showed that with four (4) presented the lowest values (Figure 1).
a cofenetic distance of 0.54 for morphometric analyzes

Fig 1. The analysis of conglomerates by the Ward method and the Euclidean distance made for the Hematological parameters in Nilotic Tilapia (Oreochromis
niloticus) individuals cultivated in Santo Domingo farm, Florencia- Caquetá.
Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira. ISSN 0122-1701 y ISSN-e: 2344-7214 129

The main component analysis (MCA) performed on the

correlation matrix for the Hematological parameters in According to Figure 2 the first main component (MP1) with a
individuals of Nile Tilapia (Oreochromis niloticus) cultivated contribution of 68.0% of the variability organized 16
in Santo Domingo farm, Florencia- Caquetá showed that the individuals with the highest values of weight, total length, head
first two main components (MP) contribute the 86 % of the total length, head width, body width and body height to the positive
variability, the first 2 components showed characteristic roots end of such component; while the second main component
greater than the unit capturing 86% of the variability. When (MP2) with a contribution of 18% organized the standard length
analyzing the coefficients of the vectors associated with the first with an individual to the positive end of such component
two main components, it was found that the variables of greatest (Figure 2).
importance in their order were: Total length, weight and height
of the body.

Fig 2. Main components analysis (MCA) carried out for the Hematological parameters in individuals of Nile Tilapia (Oreochromis niloticus) cultivated in Santo
Domingo farm, Florencia-Caquetá.
population, being located behind the lymphocytes
(corresponding about 20% of the surrounding leukocytes)
A. Leucogram demonstrating that this cell is the leukocyte type with the
greatest tendency to variation [24].
On the other hand, with the thirty-two blood samples
analyzed, the presence of erythrocytes, lymphocytes,
Morphologically speaking, in the present work we found cells
monocytes, heterophils, eosinophils, thrombocytes (Figure 4) of medium and oval size, with notorious cytoplasm, slightly
and basophils was evidenced, as has been reported in other basophilic and fine granulations; the nucleus is eccentric,
studies conducted for this species [20], [4] predominating reniform, similar to the data reported by [25]. White cells or so-
heterophiles with an average percentage of 49.3% (Appendix called leukocytes play an important role in immune function,
2), indicating a certain degree of abnormality since it is more and the higher the number of these in blood may indicate a
common to observe lymphocyte predominance. However, some better defense response of the body, since in high-density
studies such as that of [21] coincide in the value of leukocytes production systems are constantly exposed to high bacterial
for the species Oreochromis niloticus and Cyprinus carpio. loads and a poor condition of the body of water [4] and [26]
However, low values for O. niloticus were found in the studies therefore, when performing the respective analysis of the values
of [4] and [22], also indicating that the high percentage of these of this type of cell in our investigation, we obtained an average
leukocytes may be due to low water quality and high content of of 1.11 celx105 / mm3, which according to [4] is not indicative
of a leukocytosis, nor leukopenia with lymphopenia, resulting
circulating organic matter, by stress conditions induced by low
for these authors 1.21 ± 0.07 x 105 / mm³, which indicates
oxygen concentrations or in response to parasitism and similarity between both values.
infection, including exposure to various pollutants as stipulated
by [23]. For [4] the leukocyte average corresponded to 2.18 x 105 /
Regarding the percentage of heterophiles, in a study mm³, a value that is within the range for this species (tilapia).
developed by [22] for the species Oreochromis aureus obtained Likewise [10] obtained an average of 0.082 ± 0.075 leukocytes
an average between 1% and 7% of heterophiles, however [4] x 105 / mm3, a very low value compared to ours. On the other
found a maximum average of 27%; this indicates that for the hand, in a study developed by [13] the individuals of
fish Salmonidae these cells are the second most numerous Chirostoma estor estor presented a number of less than 20,000
Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira 130

cells per mm3 due (possibly) to chronic stress, which indicates species such as Ictalurus punctatus, these values coincide with
a leukopenia with lymphopenia. our study [9].

Taking into account the values of leukocytes in the present The basophils presented an average percentage of 1.71% in
investigation, some authors stipulate that due to the constant this investigation, coinciding with the data of the species
situations to which fish face, for example, stress, leukocyte Pterophyllum scalare [29], however, other authors identified
values are not high to determine leukocytosis (1.11 cel). x 105 these cells with a lower percentage than the one found, for
/ mm3), or low to describe as Leukopenia disease with example [29] obtained 0.0 ± 0.75, [4] with parasitized tilapia
lymphopenia, however, remains controversial because of the obtained 0.0 ± 0.44, [4] found 0.43 ± 3.18 and [3] with 0.35 ±
few studies implemented to this type of species. Although it 0.11%. But other studies carried out by [31] and [28] did not
should be noted that probably the animals are constantly with report the presence of these cells for O. niloticus, and that
the greatest contribution of nutrients by the daily biomass according to [17] the basophils that are observed are in very low
implemented, therefore, they are likely to show a defensive amount in circulating blood representing <1% of total
response to this situation exerted by the environment [27] - [13]. leukocytes; this may be due to problems of exposure to toxic
substances, indicating a decrease in the level of nonspecific
Lymphocytes are present in immune responses or stimulus immunity for fish as reported [22].
immunological, for example in the inflammatory process of
fish; when performing the analysis of these cells in our research, Monocytes are part of the nonspecific immune response and
we found characteristics such as: large, dark purple nucleus, phagocytosis [17] and [4]. The morphological characteristics
covering almost the entire cell, it is irregular and presenting found in the present investigation highlight that these cells are
chromatin (Figure 4). The little cytoplasm that is illustrated in large, irregular and with abundant cytoplasm; the nucleus is
light blue; data similar to those reported by [4] and [24]. The large and kidney shaped, in addition it is eccentric, lobed, blue-
lymphocyte average for this investigation was 38.84%, which violet, occupying much of the cell cytoplasm, this in turn is
is within the range established for the species O. niloticus, irregular, pale gray, contains small granules, coinciding with
however compared to other studies conducted for the same the data reported by [25], [17] y [22]. In this research an average
species is relatively low, for example see [3] - [4] obtained a of 5.9% of monocytes was presented, which according to [32]
percentage of lymphocytes of 52.8%, which were predominant; explains that they comprise less than 10% of the total
in relation to Salmonid fish, these correspond to a domain of production of white blood cells, indicating normality of the
70-80% of these cells according to [24] and for [28] the results and coinciding in works carried out by [23] and [3] with
predominance of circulating lymphocytes in Oreochromis an average percentage of 0-8.0% for this species; likewise [22]
aureus was 53-54%. identified Monocytes with a total percentage of 2-13%. [4]
determined a percentage of 1.48-17.31% and [33] reports
In other studies carried out for species such as Astronotus similar values for adult O. niloticus before and after acclimation
ocellatus, a predominance of lymphocytes was found, which is for seven days to males and females (3.37%, and 5.04 %
consistent with that found in other teleost fish [29] Another case respectively).
in particular is reported for rainbow trout (Oncorhynchus
mykiss) where lymphocytes are the type of leukocyte more The main function of thrombocytes is to control the loss of
frequent (89-98%) as stipulated [17]. fluids from superficial wounds of fish and at the same time to
interact with the defense system through phagocytic and
The primordial functions of eosinophils are associated with bacterial activity [4] - [34] and [17]. In our study, we found a
the antiparasitic response, modulation of allergic reactions and high percentage of thrombocytes (63.8%), which indicates
phagocytosis as described [17] - [4] and [30], in our thrombocytosis possibly due to the high level of stress
investigation we found lobed cells, the eccentric and lobed associated with the medium [35].
nucleus occupying a fourth part of the whole cell, and the
cytoplasm has large granules (orange, purple) coinciding with According to [23] they observed small thrombocytes that
[17] and according to [3], these cells are very rare for this measure 4.95 x 5.87μm, elongated, and grouped, with a dense
species, i. e. they only reach a number lower than 5% of the nucleus of purple color, occupying a large part of the cell, little
total leukocytes, for example the average of eosinophils in this cytoplasm, showing elongations at their ends; coinciding with
investigation was 4.3%, a high value for such species. authors [3].

According to the authors mentioned above, their For other species according to [17] in Salmo Salar, [25]
representation only reached 2.5% as the maximum value for the Rhandia quelen, [36] in Salminus affinis and [13] in
Chirostoma estor estor, such thrombocytes presented an
countdown of white ones; however for [23] these cells were not
average of 14.45%, a value that is within the range indicating
observed and stipulate that the presence of these granulocytes
normality (Appendix 2) ; Besides, other authors obtained
may be related to diseases such as eosinophilia, since under similar percentages, see [3] with (14.53%), [32] with (10.5%),
normal conditions (healthy fish) they are scarce or absent. [4] with (26%) and [37] with (5%) being this last one the lowest.
Similar data reported by [31] show that this type of cells was
not observed in work performed in O. niloticus, and for other For Oreochromis aureus they found a higher value ranging
from 55 to 74% [22], for other species Ictalurus punctatus was
 Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira
131

20%, Micropterus salmoides was close to 19%, in Morone The main components analysis (MCA) performed on the
saxatilis with 54.9% (according to a study developed by [9] - correlation matrix for the Hematological parameters in
[13]) identified a percentage of 14-62% in Chirostoma estor individuals of Nile Tilapia (Oreochromis niloticus) cultivated
estor. Therefore, in relation to the above, thrombocytes in O. in Santo Domingo farm, Florencia- Caquetá showed that the
niloticus have been described as the most abundant blood cells first three main components (MC) contribute the 85 % of the
after erythrocytes [30] and [37]. total variability, the first 4 components showed characteristic
roots greater than the unit capturing 99% of the variability.
According to [4] they include thrombocytes in the differential When analyzing the coefficients of the vectors associated with
count of leukocytes, for the investigation it was taken as an the first two main components, it was found that the variables
independent series, coinciding with other authors such as [36]- of greatest importance in their order were: Hto, Hb and VCM.
[38], since the reagent of Natt and Herrick allowed in a same According to Figure 3, the first main component (MC1) with a
dilution to identify leukocytes and thrombocytes for their total contribution of 49.7% of the variability organized 10
count, noting that when blood is collected with anticoagulant, individuals that presented the highest values of GB, Hb, Hto,
the thrombocytes exhibit an oval shape as obtained in this VCM, HCM and CHCM; while the second main component
investigation (MC2) with a contribution of 20.8% Organized the GR with 3
individuals who presented the highest values for these variables
(Figure 3).

Fig 3. Analysis of main components (MCA) carried out for the Hematological parameters in individuals of Nile Tilapia (Oreochromis niloticus) cultivated in Santo
Domingo farm, Florencia- Caquetá.
mm3, determining values of 256.7 celx106 / mm3 for the hybrid
B. Erythrogram O. urolepishormnorum x Oreochromis mossambicus.
The erythrocytes allow the transport of oxygen bound to
hemoglobin [17] and [39] which, when they are mature, are the
only ones that must be "found in the peripheral blood", because
the presence of these cells, in a low state of maturity indicate
damage in the production of red blood cells. In the present study
characteristics were described that correspond to mature
erythrocytes, i. e. the nucleus is dark, oval and central. The
cytoplasm is light, oval and without granules, coinciding with
that reported by [27] obtaining an average of 1.5 celx106 / mm3
indicating normality, concordant with [39] for a larger species
such as Arapaima gigas and similar values for the species O.
niloticus according to [4] and [3]; also for [35] O. niloticus
showed a higher average in erythrocytes 6.93 ± 8.28 celx106 / Fig 4. Oreochromis niloticus blood cells. A) red blood cells and neutrophils. B
and C.) Eosinophil D) Monocyte. E) Fusiform thrombocyte. F) Elongated
lymphocyte.
Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira 132

x O. mossambicus (red tilapia), [44] found 6 g / dl and [22] 6.2

The concentration of hematocrit obtained in this study shows g / dl for O. aureus (Oreochromis nilotic x O. mossambicus x
an average percentage of 23.3%, indicating normality O. aureus).
(Appendix 1); finding similar values for the species from 27%
-43% in works done by [3], also for [31] the average percentage For other species, hemoglobin concentration values of 9.94-
was 31.85%, for [10] it was 29.1%, see [4] 33.56% and [20] of 11.17 g / dL have been obtained in Colossoma macropomum
24.93%. On the other hand, in a study conducted in the species [7], 4.8 g / 100ml for Christoma estor estor [13] 9.4- 10.5 g / dl
O. aureus, see [22] obtained an average of 26%; for other for tilefish Sorubim cuspicaudus [38], 12.53 g / dL in Salminus
species the reports obtained for Colossoma macropomum date affinis [36], for [9] values ranged between 3.6-16.2 gr / 100 ml
from 30%, 66-36% and 74% for [7] 22.7- 25.5% for the in Salmo trutta L., for Morone saxatilis species was 7.6 g / dl,
blanquillo Sorubim cuspicaudus, [38] in the species Salminus for Micropterus salmoides it was 5.10 g / 100 ml and for [3] the
affines 36 was obtained , 2%, see [36], in Salmo trutta L. the species Colossoma bidens presented 10.40 g / dl, Prochilodus
average corresponds to 34%, in Morone saxatilis 31.19%, in scrofa (9.70 g / dl) and C. macropomum x C. bidens (12.7 g /
Ictalurus punctatus 30.64%, in Micropterus salmoides 28.26% dl).
according to the data obtained by the study of [9], and 33.95%
in Christoma estor estor according to [13]. The concentration of hemoglobin is used as a physiological
indicator of contamination and organic stress dysfunction as
The hematocrits are indicators of physiological and aquatic reported [7], [34] and [45] thus allowing the transport of oxygen
environment alterations as indicated [3], showing that this value according to [17], although the hematimetric indices vary from
is higher in freshwater fish than in marine water fish, the latter one species to another, and even in the same species according
presenting a greater number of red blood cells, which are also to the concentration of dissolved oxygen, activity, gonadal
smaller [13]; and it is noteworthy that these values vary from stage and physiological state of the fish [13] - [37], is usually
one species to another, and even in the same species according high in large fish and air breathing (lentic habitats), however,
to the concentration of dissolved oxygen, activity, gonadal for small fish (which are less active), without air breathing
stage, age, gender, physiological status of the fish, water (usually presented in lotic habitats), the values are lower as
quality, photoperiod and diet as [3] reports it. stated [9].

For our study, this average percentage is within the range The concentration of total proteins showed an average of 3.3
(Appendix 1), but it is a lower value as mentioned above; for gr / dL, value within the range for the species (Appendix 1)
this reason, some authors have established that in the lotic which indicates normality, finding similar values for the O.
environments it is common to see that the hematocrit is greater, niloticus species of 3, 6 g / dL by [31], 3.1 g / dL for [46] 3.86
while in lentic environments a lower value is observed in terms and 3.20 g / dL for [4]. However, some authors found a very
of percentage [36]. However, [9] establishes that the hematocrit small value for the species O. niloticus with 0.433 g / dL
may increase if the individual is in a phase of "moderate according to [47], and 4.3 g / dL according to [32]. For [9] Total
malnutrition", but decreases in "severe malnutrition"; bacteria Plasma Proteins, decrease in early phases, therefore, the period
can also be responsible for the decrease in hematocrit, for of malnutrition is prolonged since the PPT increases, also the
example individuals of Oreochromis niloticus were infected Hemoglobin and the Micro hematocrit decrease, presenting in
with E. tarda and Oreochromis aureus were infected with this period a defined anemic syndrome.
Corynebacterium sp. And this tendency was evidenced, which
is due to an alteration of hematopoiesis by bacteria or their In other species the reports indicate that in Morone saxatilis it
products [20]. On the other hand, if a hematocrit is present with was 4.6 gr / L according to [9] and for Piaractus brachypomus
a higher percentage than the one estimated, it should be it was 27.2 g / L in broodstock with PPT concentration in blood,
determined if there is a polycythemia and if it is accompanied which was relevant due to the affectation by the level of food,
by high hemoglobin values due to dehydration, hypoxia, stress being greater the more food is available [48].
effects or in sexually mature males. However, if there is a
reduction in the hematocrit, it usually indicates a type of anemia The VCM obtained an average of 165 (u3), which is similar
resulting from possible inflammatory, renal or splenic diseases, to that reported by [4] with 165.76 (u³) and similar values were
nutritional disorders, toxins, traumas, skin ulcerations, found for [43] with a volume of 66.38 (u3) in males and 132.23
parasitism, bacterial or viral septicemia [4]. (u3) in females, [33] with 148.80 (u3), for [31] with 175.46
(u3), [37] found 191.2 (u3), for [42] it was 174.59 (u3), [3]
Regarding the concentration of hemoglobin, an average of 7.9 200.47 (u3), for [49] was 143.52 (u3), according to [41] for non-
g / dl was obtained, a value within the range for the species parasitized species it was 153.3 (u3) and 135 (u3) in parasitized
(Appendix 1), however, similar values were found for O. species; on the other hand [32] obtained 226.24 (u3) for O.
niloticus in studies of [32] with an average of 5.8 g / dL in non- aureus, [22] for another species such as Colossoma
parasitized species and 6.54 g / dL in parasitized species, on the macropomum obtained 390.82 (u3), in turn [7] in Astronotus
other hand [40] found a hemoglobin concentration value of ocellatus obtained 93.9 (u3), [38] in Chirostoma estor estor
102.2 g / dl, [41] of 4.05 -10.43 g / dl, [31] of 10.52 g / dl, [42] obtained 183 (u3), and in Salminus affinis 163.8 (u3) according
of 8.2 g / dl, [43] of 6.1 g / dl, [37] of 9.1 g / dl dl, for [49] of to [36].
4.25 - 4.63 g / dl, [4] obtained 9.32-9.94 g / dL, for [3] 5.59-
11.61 g / dl and for other species such as Oreochromis nilótica
 Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira
133

These values are related to the cell size of erythrocytes, and (hypochromia and anisocromia) [13] In this study we obtained
are used to classify them as normocytic, microcytic or a percentage of 33.3%, which indicates that it is within the
macropytic [13] and [34], this hematological index relates to established range shown in Appendix 1, finding similarity in
respiratory function and the middle corpuscular concentration different studies, for example for [43], [37], [31], [41], [42],
of hemoglobin. [49] and [4] obtained values of 24.65, 27.8, 35.24, 41.14, 28.3,
38.18 and 29.14 respectively for the species O. niloticus. In the
Although our results are apparently within the range case of [33] obtained a total of 27.38 for males and 32.75 for
established for the species O. niloticus, they are very low values females. On the other hand, as [32] reported the percentage of
compared to other authors. However, the type of anemia CHCM for non-parasitized tilapia species was 29.7, while for
presented can be established according to the parameters of red, parasitized species it is 24.8. In other species such as
countdown of red ones, blood cell or red cell and hemoglobin Colossoma macropomum the value was 33.32 [7] for Salminus
or hemoglobin concentration. In the present study it was found affinis was 35.5 [36], for Astronotus ocellatus was 33.1 [29],
that 16 of the 32 individuals presented Normochromic for Sorubim cuspicaudus 42.9 [38] and in Chirostoma estor
Normocitic Anemia which according to [24] is generated as a estor was 14.9 [13].
result of hemorrhages in the intestine, liver, pyloric and ocular
caecum, product of endothelial damage or when severe or An element of utmost importance to take into account is the
chronic blood loss occurs, the net loss of iron can cause anemia correlation between the Average Corpuscular Volume and the
due to deficiency of this mineral. They also explain that it has Average Corpuscular Hemoglobin, since they are directly
been associated with environmental stresses (increase in proportional, i. e. if one increases the other, too, however, there
population density or stress). This type of disease is very unique is a negative correlation with the Erythrocytes, since they differ
in the species Oreochromis aureus [20]. On the other hand, two with respect to the value of VCM and HCM [4].
individuals presented Normochromic Microcytic Anemia with
a VCM of 61 u3 and 78 u3 which, compared with the values of The main components analysis (MCA) performed on the
[4], is very low for fish with a weight between 150 gr and 250 correlation matrix for the Hematological parameters in
gr, because the range ranges from 69.57 to 459.46 u3. individuals of Nile Tilapia (Oreochromis niloticus) cultivated
in Santo Domingo farm, Florencia- Caquetá showed that the
In HCM or middle corpuscular hemoglobin an average of 55 first four main components (MC) contribute 84 % of the total
(uug) was obtained, which is within the range according to variability, the first 3 components showed characteristic roots
appendix 1, similarly was found similar values as stipulated greater than the unit capturing 71% of the variability. When
[33] with 47.6 (uug) in males and 21, 27 (Uug) in females. analyzing the coefficients of the vectors associated with the first
Likewise for [43] the value obtained was 35 (uug), 50.50 (uug) two main components, it was found that the variables of greatest
for [3] with 53.9 (uug), [42] with 50.87 (uug), for [4] 40 , 74 importance in their order were: EOS and BASO.
(uug) see [31] with 52.93 (uug) for [41] with 10.69 (uug) for
[49], for the species O.aureus it was 54.4 (uug) according to According to Figure 5, the first main component (MP1) with
[22] and for other species such as Colossoma macropomum the a contribution of 35.2% of the variability organized 9
value was close to 122.46 (uug) according to [7] in Salminus individuals who presented the highest values of HETE (%) to
affinis individuals the HCM value 58.5 (uug) according to [36] the positive end of such component; at the negative end it
for [29] in the Astronotus ocellatus species obtained 31.07 organizes 7 individuals with the variables MONO (%), BASO
(uug) and for Sorubim cuspicaudus in a study developed by [38] (%), LYM (%) and EOS (%). While the second main
such value was 28.4 (uug). component (MP2) with a contribution of 26.5% organized the
GB and PLT with 5 individuals who presented the highest
The percentage value of MCHC is related to the distribution values for these variables, while PT to the negative end of such
of hemoglobin within the erythrocyte [34] indicating a slightly component with 12 individuals (Figure 5).
lower concentration or irregular distribution of Hb
Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira. ISSN 0122-1701 y ISSN-e: 2344-7214 134

Fig 5. Mainl components analysis (MCA) carried out for the Hematological parameters in individuals of Nile Tilapia (Oreochromis niloticus) cultivated in Santo
Domingo farm, Florencia-Caquetá.

IV. CONCLUSION Likewise, it is concluded that the correlation between the

Once the blood studies were carried out, it was possible to variables length and height do not significantly affect
show that two individuals had a Microcytoma Normochromic hematological parameters, however weight will always be a
anemia, since their value of VCM is below the range, in determining factor when relating individuals to blood ranges.
addition to that 16 individuals presented Normocromic In general, our work corresponds to a normal result similar to
Normocitica anemia. These situations can be rooted in those reported with other authors. It would be efficient to
overpopulation in the environment, which generates a decrease consider a study of hemoparasites, to determine whether or not
in oxygen levels (apoxia) and therefore stress generates a lack they influence the hematological values of the species (tilapia),
of appetite in individuals, which triggers anemia. On the other since they are susceptible to presenting such pathogens in some
hand, when performing the analysis of the leucogram, some fish culture media (intensive-semi-intensive).
presented a leukopenia with lymphopenia and thrombocytosis,
which indicates an immune system response to a pathogenic
agent, which is why it is believed to be a bacterial septicemia.

ACKNOWLEDGMENTS experimental piscícola de la universidad de caldas”. Vet. Zootec.

5(1): 47-61, Abril 2011
We thank the different agents for their collaboration in the [4] Hahn Von Hessberg, C., Quiroz-Bucheli, A. y Grajales- Quintero,
analysis of data and review of the article, which made A. “Caracteres hematológicos en individuos de tilapia nilótica
contributions in order to make more valuable the process of (oreochromis niloticus, trewavas 1983) con pesos entre 50-150 g y
150-250 g, estación piscícola, universidad de caldas”. bol. cient.
shaping the work. To the University of the Amazonia and Santo
mus. hist. nat. u. de caldas, 18 (1): 142-157, junio 2014.
Domingo experimental farm for the facilities and individuals
contributed for the study. [5] M. D. Abdul, J.A. Siddiqui Pirzada, A. Ghulam, T. N. Naeem,
Sajjad A Syed, N. K. Shah, D. Ghulam. “Effect of Dietary Protein
Level on Growth Performance, Protein Utilization and Body
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Changes in Nile Tilapia (Oreochromis niloticus) Fed with Varying Leidy Vanesa Galindo Peña. She was
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born on November 02, 1993 in the
Sciences 4 (4): 376-381, 2012
Municipality of Florencia, Caquetá,
Betselene Murcia Ordoñez. Colombia. In 2010 she is an Academic
Biologist with emphasis on Bachelor with Intensification in Natural
Bioresources, Master of Science in Sciences of the Sacred Hearts
Biology, Doctoral student in Natural Educational Institution, with a
Sciences and Sustainable bachelor's degree (holding one of the
Development with experience in first positions at the institutional level).
Animal Science, focused on She is a Biologist at the University of
physiology mainly on nutrition, Amazonia (Public Institution) in Florencia Caquetá. Since 2012
energy, reproduction and fish she is part of the seedling and Research Laboratory in Animal
hematology (among other areas) Physiology "FA-UA" and in the research group on Biodiversity
with field and laboratory experience, and Amazonian Development (BYDA). Since 2016 she has
responsible, competitive, interpersonal and institutional worked as Professor in the areas of Biology, Chemistry, Physics
relationships management, with national training (National and Mathematics in the bipartisan Program between the
University of Colombia and international (INPA, Manaus). Ministries of Education and the Ministry of Defense in the
Director of the research group on biodiversity and Amazonian "Educational Project Military Forces of Colombia",
development BYDA and FA-UA Research Seedling of the Educational Center for Youth and Adults named: Preacher
LUIS DE RIZ - INFORPH OF COLOMBIA. And currently
 Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira
137

developing the Diplomat program in Culture of Peace and Post- well as the co-authorship of 2 science books. His academic
Conflict, for her subsequent publication in the magazine interests are based on the areas of Mycology, Microbiology,
TRASHUMANTE (American Journal of Social History) of the Molecular Biology and Biostatistics.
University of Antioquia and by the Division of Social Sciences ORCID: http://orcid.org/0000-0001-7608-2872
and Humanities of the Autonomous Metropolitan University
(UAM), Cuajimalpa Unit (Mexico City). Her academic José Helí Hernández Sanchez. He
interests are based on the areas of Physiology, Microbiology was born in the inspection The
and Biology. Carbonal, Municipality of San
ORCID: http://orcid.org/0000-0002-2830-1142 Vicente del Caguán, Caquetá,
Colombia. In 1969 she was
Frey David Pérez Cuervo. Biologist Academic Bachelor of Dante
from the University of the Amazonia, Alighieri la Salle (Graduated in
belongs to the Amazonia 1992) Educational Institution. To
Biodiversity and Development advance studies of: Professional
Research Group (BYDA) and the Technician, Professional and
FA-UA seedling since 2011. His Specialist; received the degree of
areas of interest are neurophysiology, Professional Technician in Systems
however he has excellent bases in Engineering in 2000, from the Unified National Corporation
endocrinology, physiology "CUN"; her undergraduate degree was held in the city of
sanguineous and reproductive. He Bogotá at the INCCA University in Colombia, which is a
currently works in the Physiology pioneer of the systems engineers in Colombia; in the year 2003;
Laboratory of the University of the Amazonia. He has worked He graduated as a Systems Engineer. And later, the
as a technical advisor for projects and field in the Committee of Specialization in High Speed Networks and Distributions at the
GANADEROS DEL CAQUETÁ, in a project called "new INCCA University of Colombia and obtained the degree on
territories of peace" in association with the EUROPEAN December 5, 2008. Works in the Government of Caquetá in the
UNION and NATURAL HERITAGE. He has developed Secretariat of Planning and ICT. He has also served as a teacher
studies in application of methodological tools in research: in the bipartisan program in the Ministries of Education and the
scientific publications and SCIENTI platform. Solid Ministry of Defense in the "Educational Project Military Forces
intellectual capacity to understand, advise and execute a wide of Colombia", Educational Center for Youth and Adults named:
variety of work processes that are aimed at good systematic and PADRE LUIS DE RIZ - INFORPH OF COLOMBIA. Diploma
organizational functioning, based on the principle of continuous in culture of peace and conflict, for later publication in the
improvement and self-improvement. magazine TRASHUMANTE (American Journal of Social
ORCID: http://orcid.org/0000-0002-9139-7212 History) of the University of Antioquia and the Division of
Social Sciences and Humanities of the Autonomous
Metropolitan University (UAM), Cuajimalpa Unit (Mexico
D.C).
ORCID: http://orcid.org/0000-0002-8803-1025
Edgar Martinez Moyano. He was
born in the Inspection of Mateguadua, Alba Miriam Poche Ceballos. She was
Municipality of La Montañita, born in the municipality of Belalcazar
Caquetá, Colombia. In 1996 Academic Páez cauca Colombia in 1986, academic
bachelor with emphasis in bachelor of the educational institution
Mathematics and physics from the Barrios Unidos del Sur. She got a degree
Educational Institution Juan Bautista la in veterinary medicine and Zootechnics
Salle (Graduated in 2012), he obtained at the University of Amazonia in 2011,
the title of best bachelor of his specialist in veterinary clinical
generation. He received the degree of laboratory in 2013, currently a professor
Biologist in 2017 from the University of Amazonia, is currently of the subject clinical laboratory, Medical surgeon in Project.
a student of the Master program of Biological Sciences of the She does strengthening actions to reduce canine and feline
same University, and candidate to enter the Specialization in overpopulation in the department of Caquetá, analyst in clinical
Applied Statistics of the University Foundation los laboratory of small animals, linked in 2016 to the BIDA
Libertadores. In 2016, he became a Co-researcher of the research group as a researcher in the area of analysis and
SINCHI Amazonian Scientific Research Institute where he clinical diagnosis in different species of animals. She has 3
currently works. He works at the Laboratory of Mycology and scientific publications in national and international indexed
Phytoprotection of the MACAGUAL Amazon Research Center journals in the area of small animals and wildlife. In addition,
"Cesar Augusto Estrada González" of the University of she participates in the co-authorship of 2 clinical diagnostic
Amazonia. He is part of the Mycology Research Group of the research articles.
University of Amazonia-GINMUA and the Research Group on ORCID: http://orcid.org/0000-0001-9385-3659
Biodiversity and Development-BYDA. He has 10 scientific
publications in national and international indexed journals, as
Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira 138

V. APPENDIX
Appendix I: Hematological valors of Tilapia Nilotica

N° of 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Refere
individu nces
als
Hemato 33 23 23 17 17 28 31 18 18 25 18 28 13 30 24 13 12,5-
crit % 34,1
Hemogl 11 7,7 7,7 5,7 5,7 9,3 10,3 6,0 6,0 8,3 6,0 9,3 4,3 10,0 8,0 4,3 6,89-
obin 8,92
(g/dL)
Erythro 1,69 1,21 1,22 2,19 1,56 1,16 1,96 1,08 1,11 2,17 1,09 1,12 2,12 1,36 1,29 1,07 0,24-
cytes 1,85
(106/mm
3
)
Leukocy
tes 1,61 0,92 1,03 1,76 1,1 1,43 1,89 1,16 1,01 1,74 1,63 1,54 1,56 1,41 0,79 1,39 0,08-
(celx105/ 0,3
mm3)

Plasmap
roteins 3,8 3 2,8 2,8 2,9 3,1 3,3 3 2,5 3,2 3,7 3,2 3,1 3,1 3,2 2,4 3,3-5,0
(gr/dL)
VCM 195 190 189 78 109 241 158 167 162 115 165 250 61 221 186 121 99,28-
(u3) 123,66
HCM 65,1 63,4 62,8 25,9 36,3 80,5 52,7 55,6 54,1 38,4 55,0 83,3 20,4 73,5 62,0 40,5 33,01-
(uug) 55,9
CHCM 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 31,28-
(%) 49,61

N° of 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 Referen
individ cia
ues
Hemat 35 16 30 27 15 21 21 21 21 16 22 32 40 38 19 14 12,5-
ocrit % 34,1
Hemog 11,7 5,3 10,0 9,0 5,0 7,0 7,0 7,0 7,0 5,3 7,3 10,7 13,3 12,7 6,3 4,7 6,89-
lobin 8,92
(g/dL)
Erythr 1,03 1,12 1,13 1,49 1,23 1,32 1,39 1,48 1,9 1,04 1,94 2,31 1,95 2,84 1,1 1,03 0,24-
ocytes 1,85
(106/m
m3)
Leukoc
ytes 0,70 0,84 1,67 1,21 0,88 1,32 1,16 0,68 0,66 0,77 0,55 0,59 0,88 0,70 0,46 0,62 0,08-0,3
(celx10
5
/mm3)

Plasma
protein 2,8 2,2 3,2 3,7 3 2,7 3 4,4 4 3,2 3,4 4,3 4 4,3 4,2 4,3 3,3-5,0
s
(gr/dL)
VCM 340 143 265 181 122 159 151 142 111 154 113 139 205 134 173 136 99,28-
(u3) 123,66
HCM 113, 47,6 88,5 60,4 40,7 53,0 50,4 47,3 36,8 51,3 37,8 46,2 68,4 44,6 57,6 45,3 33,01-
(uug) 3 55,9
CHCM 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 33,3 31,28-
(%) 49,61
 Scientia et Technica. Año XXIV, Vol. 24, No. 01, marzo de 2019. Universidad Tecnológica de Pereira
139

Appendix II: Total and differential count of white blood cells

N° of 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Refere
individu nces
als
neutroph 60 63 65 42 56 31 48 36 65 51 46 39 60 60 49 66 6,77-
ils % 46,64
Lympho 30 27 24 57 35 49 39 48 28 32 37 46 29 33 34 28 48,39-
cytess 75,47
%
eosinoph 1 4 1 0 2 7 3 5 2 8 6 5 3 2 5 2 1,67-
ils % 9,0
monocyt 6 4 6 1 7 8 9 6 5 7 9 7 7 5 8 3 1,48-
es % 17,31
basophil 3 2 4 0 0 5 1 5 0 2 2 3 1 0 4 1 0,43-
s% 3,18
Total 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100

Thromb 64 62 63 107 77 84 104 88 82 98 96 66 99 84 33 55 13,53-

ocytes % 56,8

N° of 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 Refere
individu nces
als
N° of 47 29 38 51 37 39 42 46 51 46 49 60 52 49 56 49 6,77-
individu 46,64
als
neutrop 39 48 49 42 48 45 47 43 38 42 43 34 36 38 39 36 48,39-
hils % 75,47
Lympho 6 9 4 3 8 6 5 5 5 5 3 3 5 6 1 6 1,67-
cytess 9,0
%
eosinoph 8 8 8 4 4 8 3 4 5 7 5 2 7 6 3 8 1,48-
ils % 17,31
monocyt 0 6 1 0 3 2 3 2 1 0 0 1 0 1 1 1 0,43-
es % 3,18
basophil 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100
s%
Total 28 48 83 84 61 95 69 39 27 44 23 27 44 40 32 35 13,53-
56,8

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