51
Clinical/paraclinical of canine visceral leishmaniasis
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Neotropical Helminthology
Neotropical Helminthology, 2025, vol. 19 (1), 51-64
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
CLINICAL/PARACLINICAL FINDINGS IN DOGS WITH
LEISHMANIA
INFANTUM
(ROSS, 1903) IN TRANSMISSION AREAS, URUGUAY
HALLAZGOS CLÍNICOS/PARACLÍNICOS EN PERROS CON
LEISHMANIA
INFANTUM
(ROSS, 1903) EN ÁREAS DE TRANSMISIÓN, URUGUAY
Zully Hernández-Russo
1
*; Martín Scayola Xamo
2
& Juan Cedano
3
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.62429/rnh20251911907
Este artículo es publicado por la revista Neotropical Helminthology de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico
Villarreal, Lima, Perú auspiciado por la Asociación Peruana de Helmintología e Invertebrados Af nes (APHIA). Este es un artículo de acceso abierto,
distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/
deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original.
ABSTRACT
Canine visceral leishmaniasis (CVL), caused by
Leishmania infantum
(Ross, 1903), is an emerging disease in Uruguay,
posing signif cant public and animal health challenges. T is study aimed to evaluate the relationship between clinical
signs and hematological, hepatic, and renal alterations in dogs seropositive for
L. infantum
in Uruguay. Canids
were classif ed according to the absence/presence of clinical signs as asymptomatic (no apparent signs of disease),
oligosymptomatic (less than three clinical signs compatible with CVL), polysymptomatic (three to six clinical
signs), and hypersymptomatic (with more than six clinical signs). Laboratory analysis revealed signif cant alterations
in hematological, hepatic, and renal parameters as the number of clinical signs increased. Polysymptomatic and
hypersymptomatic dogs exhibited signif cant decreases in erythrocytes, hemoglobin, hematocrit, mean corpuscular
hemoglobin (MCH), and mean corpuscular hemoglobin concentration (MCHC), alongside increased segmented
neutrophils and decreased lymphocytes. Hepatic function tests showed reductions in total and direct bilirubin,
albumin, and the albumin/globulin ratio, while renal parameters such as urea and creatinine increased signif cantly
with clinical severity. T e multidimensional analysis highlighted distinct clusters of clinical signs and laboratory
parameters that ref ect the systemic ef ects of the disease. T ese f ndings highlight the progressive nature of CVL,
characterized by worsening of erythropoiesis, hepatic dysfunction, and renal impairment. T e study emphasizes the
importance of early diagnosis and monitoring of clinical and laboratory parameters to manage this emerging disease
1
Parasitología Veterinaria, Cenur Litoral Norte Salto, Universidad de la República, Salto, Uruguay. zhernan@unorte.edu.uy
2
Liberal exercise of the profession, Salto, Uruguay
. martsca1@hotmail.com
3
Instituto de Biotecnología y Biomedicina, Departamento de Bioquímica y Biología Molecular, Universidad Autónoma de
Barcelona, España
. juanantonio.Cedano@uab.cat
* Corresponding author: zhernan@unorte.edu.uy
Zully Hernández-Russo:
https://orcid.org/0000-0003-0136-6330
Martín Scayola Xamo:
https://orcid.org/0000-0003-0629-9077
Juan Cedano:
https://orcid.org/0000-0003-1380-8036
52
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Hernández-Russo
et al.
efectively. Te emergence of CVL in Uruguay calls for increased surveillance and control measures to mitigate its
impact on both canine and human populations.
Keywords
: Canines – visceral leishmaniasis – clinical status –hematological/biochemical profles – global behavior –
Uruguay
RESUMEN
La leishmaniasis visceral canina (LVC), causada por
Leishmania infantum
(Ross 1903), es una enfermedad emergente
en Uruguay que plantea importantes desafíos para la salud pública y animal. Este estudio tuvo como objetivo evaluar la
relación entre los signos clínicos y las alteraciones hematológicas, hepáticas y renales en perros seropositivos a
L. infantum
en Uruguay. Los cánidos se clasifcaron según la ausencia/presencia de signos clínicos como asintomáticos (sin signos
aparentes de enfermedad), oligosintomáticos (menos de tres signos clínicos compatibles con LVC), polisintomáticos
(tres a seis signos clínicos) e hipersintomáticos (con más de seis signos clínicos). El análisis de laboratorio reveló
alteraciones signifcativas en los parámetros hematológicos, hepáticos y renales a medida que aumentaba el número de
signos clínicos. Los perros polisintomáticos e hipersintomáticos exhibieron disminuciones signifcativas en eritrocitos,
hemoglobina, hematocrito, hemoglobina corpuscular media (HCM) y concentración de hemoglobina corpuscular
media (HCCM), junto con un aumento de neutróflos segmentados y una disminución de linfocitos. Las pruebas
de función hepática mostraron reducciones en la bilirrubina total y directa, la albúmina y la relación albúmina/
globulinas, mientras que los parámetros renales como la urea y la creatinina aumentaron signifcativamente con la
gravedad clínica. El análisis multidimensional destacó grupos distintos de signos clínicos y parámetros de laboratorio
que refejan los efectos sistémicos de la enfermedad. Estos hallazgos resaltan la naturaleza progresiva de la LVC,
caracterizada por el empeoramiento de la eritropoyesis, la disfunción hepática y el deterioro renal. El estudio enfatiza
la importancia del diagnóstico temprano y el monitoreo de los parámetros clínicos y de laboratorio para manejar esta
enfermedad emergente de manera efectiva. La aparición de LVC en Uruguay requiere una mayor vigilancia y medidas
de control para mitigar su impacto tanto en las poblaciones caninas como humanas.
Palabras clave:
Caninos – leishmaniosis visceral – estado clínico – perfles hematológicos/bioquímicos – comportamiento
global – Uruguay
INTRODUCTION
Canine visceral leishmaniasis is a parasitic zoonosis
primarily transmitted by vectors. Although vectorial
transmission remains the main route of infection, other
forms of transmission have been identifed, such as blood
transfusions, and maternal-fetal transmission, albeit
with a lesser epidemiological impact. Te presence of
green areas, gardens, and abandoned lots in cities, along
with the growing pet population, is contributing to the
spread of this traditionally rural disease into urban areas
(Organización Panamericana de la Salud, 2023). In the
Americas, the epidemiology is linked to the etiological
agent
Leishmania infantum
(Ross, 1903), the vector
Lutzomyia longipalpis
(Lutz & Neiva, 1912) — preferred
due to its wide distribution and adaptation to peridomestic
environments — and the dog (
Canis familiaris familiaris
,
Linnaeus, 1758), which represents the quintessential
domestic-urban reservoir (Quinnell & Courtenay, 2009;
Romero & Boelaert, 2010; Organización Panamericana
de la Salud, 2023). Symptomatic or asymptomatic
infected dogs can be infectious to sandfies and thus play
a key role in maintaining transmission (OPS – OMS,
2019).
Canine visceral leishmaniasis is considered a systemic
disease, generally chronic in its progression, and its clinical
manifestations are notable for their variety and extent,
depending, among other factors, on the predominant
immune response of the infected animal (Ciaramella &
Corona, 2003; Solano-Gallego
et al
., 2011; Scayola
et
al
., 2024). Cutaneous lesions are reported as the most
frequent and include scaly dermatitis, onychogryphosis,
nasal and footpad hyperkeratosis, alopecic areas,
and ulcerations. Additionally, general signs such as
lymphadenomegaly, weight loss, mucosal pallor, ocular
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Clinical/paraclinical of canine visceral leishmaniasis
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
lesions, bleeding disorders, locomotor abnormalities,
renal involvement, and others are prominent (Solano-
Gallego
et al
., 2011; Solano-Gallego, 2013; Scayola
et
al
., 2019).
T
he progression of the infection involves serological,
parasitological, hematological and biochemical profle
alterations. In this regard, Reis
et al
. (2006) report a
direct correlation between these changes and the clinical
stage of the disease. Tey demonstrated that the severity
of clinical signs was related to the parasitic density in
diferent tissues, such as skin, bone marrow, and spleen,
as well as to higher antibody titers in symptomatic
dogs, resulting in a lower albumin/globulin ratio
compared to asymptomatic and uninfected controls.
For their part, Giunchetti
et al
. (2008) observed more
intense hepatic infammatory reactions in symptomatic
dogs, associated with a higher frequency of parasitism
compared to asymptomatic dogs. Tey also reported an
association between hepatic histological changes and the
progression of biochemical alterations according to the
clinical forms of the infection. Although hematological
and biochemical parameters are not pathognomonic
for CVL, they are useful in assessing clinical status and
can serve as prognostic indicators. Laboratory fndings
include dysproteinemia, anemia, thrombocytopenia,
and azotemia (Reis
et al
., 2006; da Costa-Val
et al
., 2007;
Scayola
et al
., 2024).
Considering the epidemiological relevance of canine
involvement in the transmission of visceral leishmaniasis
and as a holistic approach to evaluating the infection,
the objective was proposed to relate and visualize the
global behavior of clinical signs and hematological and
biochemical profles in
L. infantum
-seropositive canids in
areas with transmission in Uruguay.
MATERIALS AND METHODS
Study area description and involved animal population
Te study took place in areas where the disease is actively
spreading, meaning these are regions where both dogs
and humans have been reported to contract the infection
locally. Tese areas are located in the capital city of
the Salto department, Uruguay, in the western littoral
region on the eastern bank of the Uruguay River (31°
23’ 18.0” S, 57° 57’ 38.0” W). Te climate is temperate
subtropical, with average annual temperatures and rainfall
of approximately 18-19 °C and 1400 mm, respectively
(Red Académica Uruguaya, 2024).
A cross-sectional study was conducted on an estimated
subpopulation (Yofre
et al
., 2012) that included 43 dogs
(
C. familiaris familiaris
) with a mean age of 4.9 years,
diagnosed with naturally acquired visceral leishmaniasis.
Diagnosis was made by the presence of anti-
Leishmania
antibodies using the immunochromatographic technique
with the recombinant antigen rK39 (Kalazar Detect
Canine Rapid Test, InBios).
Te dogs were classifed based on the absence/presence
of clinical signs as asymptomatic (no apparent signs of
disease) or symptomatic (with clinical signs compatible
with CVL). Te symptomatic group was further divided
into oligosymptomatic (fewer than three clinical signs),
polysymptomatic (three to six clinical signs), and
hypersymptomatic (more than six clinical signs) subgroups
(modifed from Pozio
et al
., 1981). Te frequency of
clinical signs was recorded and these were grouped
into the main clinical presentations: visceral (anorexia,
vomiting, sneezing, diarrhea, lameness, fever), circulatory
(mucosal pallor, conjunctivitis, lymphadenomegaly),
and cutaneous (alopecia, onychogryphosis, nasal and
footpad hyperkeratosis, pruritus, petechiae). Te clinical
groups were established based on the results of the
multidimensional scaling.
Analysis of hematological and biochemical profles
Two blood samples (5 mL total) were collected from each
animal via the cephalic vein using sterile 21G butterfy
needles (Experimental Protocol No. 2/15, approved
by the Ethics Committee on Animal Use, CEUA, and
the Council of Cenur Litoral Norte, Universidad de la
República, on 24/06/2015), with prior consent from the
owners or caretakers. One sample was collected in a tube
containing ethylenediaminetetraacetic acid (EDTA)
anticoagulant for hematological analysis, which included
the study of the red blood cell series, white blood
cell series, and platelet count. Within the red blood
cell series, the number of erythrocytes, hemoglobin,
hematocrit percentage, and hematimetric indices—
mean corpuscular volume (MCV), mean corpuscular
hemoglobin (MCH), and mean corpuscular hemoglobin
concentration (MCHC)—were determined. For the
white blood cell series, total and diferential leukocyte
counts were performed, including relative and absolute
counts of neutrophils, lymphocytes, monocytes, and
eosinophils.
Te other sample was collected in a dry tube containing
separation gel, without anticoagulant, for biochemical
evaluation of liver and kidney function. Te hepatic
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Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Hernández-Russo
et al.
biochemical profle included measurements of direct,
indirect, and total bilirubin; cholesterol; total proteins,
albumin, globulins, and the albumin/globulin ratio; and
the enzymes alanine aminotransferase (ALT), aspartate
aminotransferase (AST), alkaline phosphatase (ALP),
and gamma-glutamyl transferase (GGT). Te renal
biochemical profle included serum urea and creatinine
levels.
Analyses were performed at a private clinical laboratory
using the Horiba ABX Pentra 60 (Japan) analyzer for
red blood cell, white blood cell, and platelet counts,
hemoglobin, hematocrit, and hematimetric indices.
Diferential leukocyte counts were performed by
microscopic examination of blood smears stained with
May Grünwald-Giemsa. Automated analysis of hepatic
and renal biochemical parameters was conducted using
the AMS Alliance SAT 450 (Italy) analyzer.
Statistical analysis
Te relationship between hematological and biochemical
parameters and the number of clinical signs was evaluated
using Student’s t-test, grouping dogs into asymptomatic
and oligosymptomatic versus polysymptomatic and
hypersymptomatic categories. Additionally, the
relationship between these parameters and the number of
clinical signs, both overall and categorized into visceral,
circulatory, and cutaneous presentations, was assessed
using Pearson correlation (Sokal & Rohlf, 2002). A
Pearson correlation coefcient (r) of 0.35, with 41 degrees
of freedom, was considered the threshold for signifcance.
A 95% confdence level was used, and statistical analyses
were performed using Microsoft Excel 2016, Minitab 11,
and R Package ggplot2 and scales.
For a global visualization of how clinical signs relate
to each other and to hematological and biochemical
parameters, multidimensional scaling was performed.
Distance matrices were constructed using squared
correlation coefcients (r²) of clinical signs relative to
parameters, and vice versa, for all 43 dogs, using the
Perceptual Mapping (PERMAP) 11.6 software.
Ethic aspects
: Te experimental protocol was appproved
by the Ethics Committee in the Use of Animals of the
University of the Republic (CEUA/CENUR Litoral
Norte, protocol N°2/15).
RESULTS
Description of clinical manifestations
Based on the classifcation considering the number of
clinical signs in the dogs, 14% were asymptomatic, 21%
oligosymptomatic, 30% polysymptomatic, and 35%
hypersymptomatic. Te main clinical signs recorded
included skin lesions in 78.38% of cases, weight loss in
72.97%, mucosal pallor in 56.76%, lymphadenomegaly
in 51.35%, conjunctivitis and polyuria/polydipsia in
45.95%, lethargy in 43.50%, petechiae in 32.50%, and
anorexia in 28.50% of symptomatic dogs.
Relationship between hematological, hepatic, and renal
parameters in Leishmania-seropositive dogs with the number
of clinical signs and clinical presentations
When comparing asymptomatic and oligosymptomatic
animals with polysymptomatic and hypersymptomatic
ones (Table 1), variations in hematological, hepatic,
and renal parameters were observed as the number of
clinical signs increased. In the red blood cell series, there
was a signifcant decrease in erythrocytes, hemoglobin,
hematocrit, MCH, and MCHC as the number of clinical
signs increased.
In the white blood cell series, polysymptomatic and
hypersymptomatic dogs showed a signifcant increase in
the relative values of segmented neutrophils and a relative
and absolute decrease in lymphocytes (Table 1).
I
n liver function tests, total and direct bilirubin, albumin,
and the albumin/globulins ratio decreased signifcantly
in dogs with more than three clinical signs. However,
no signifcant variation was observed in total proteins
or globulins levels, despite being elevated in most cases;
nor in the activities of the enzymes ALT, AST, ALP and
GGT in relation to the number of clinical signs (Table
1).
Regarding the renal profle, both urea and creatinine
increased signifcantly with the greater the number of
clinical signs in the dogs (Table 1).
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Clinical/paraclinical of canine visceral leishmaniasis
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Table 1.
Relationship between hematological, hepatic, and renal parameters in asymptomatic and oligosymptomatic
dogs compared to polysymptomatic and hypersymptomatic dogs. Signifcance level.
Parametersp-valueParametersp-value
Red blood cells
6.54131e-06 (
↓
)
Total bilirubin
0.00615069 (
↓
)
Hemoglobin
1.55078e-06 (
↓
)
Direct bilirubin
7.1157e-05 (
↓
)
Hematocrit
2.26542e-06 (
↓
)
Indirect bilirubin0.06627826
MCV0.09968413
AST0.15712271
MCH
0.0176781 (
↓
)
ALT0.48862227
MCHC
0.00296652 (
↓
)
GGT0.14019129
Platelet count0.37199956
ALP0.2093285
White blood cells0.90943021
Total proteins0.27730504
Segmented neutrophils (%)
0.02027718 (
↑
)
Albumin
0.0311152 (
↓
)
Eosinophils (%)0.87756432
Globulins0.3914846
Lymphocytes (%)
0.00129336 (
↓
)
Albumin/globulins ratio
0.000624886 (
↓
)
Monocytes (%)0.96856919
Urea
0.01786212 (
↑
)
Segmented neutrophils0.23938512
Creatinine
0.04866968 (
↑
)
Eosinophils0.65318959
Lymphocytes
0.00350947 (
↓
)
Monocytes0.23014687
p = signifcance value: (
↑
) = signifcant increase, (
↓
) = signifcant decrease.
Table 2 shows the relationship between hematological,
hepatic, and renal parameters according to clinical
presentation (visceral, cutaneous, and circulatory) and
the total number of clinical signs. A signifcant decrease
in red blood cells, hemoglobin, hematocrit, and MCHC
was observed as the number of clinical signs increased in
the overall afected dogs, as well as in those with cutaneous
and circulatory presentations. In the latter, a decrease in
MCH and a near-signifcant decrease in MCV were also
noted.
Table 2.
Relationship between hematological, hepatic, and renal parameters according to clinical presentation and the
total number of clinical signs in
Leishmania
-positive dogs
ParameterVisceralCutaneous CirculatoryOverall
Red blood cells
-0.251
-0.45 (
↓
)-0.63 (
↓
)-0.5 (
↓
)
Hemoglobin
-0.264
-0.5 (
↓
)-0.67 (
↓
)-0.54 (
↓
)
Hematocrit
-0.261
-0.49 (
↓
)-0.67 (
↓
)-0.54 (
↓
)
MCV
-0.069-0.23-0.35-0.28
MCH
-0.093-0.32
-0.41 (
↓
)
-0.34
MCHC
-0.16
-0.43 (
↓
)-0.4 (
↓
)-0.37 (
↓
)
Platelet count
0.1980.2320.320.261
White blood cells
0.0740.1610.230.153
Segmented neutrophils (%)
0.0640.264
0.38 (
↑
)
0.276
(Continúa Table 2)
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Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Hernández-Russo
et al.
ParameterVisceralCutaneous CirculatoryOverall
Eosinophils (%)
0,257 0,108-0,07 0,146
Lymphocytes (%)
-0.246
-0.42 (
↓
)-0.45 (
↓
)-0.45 (
↓
)
Monocytes (%)
0,039 0,065 0 0,027
Segmented neutrophils
0,025 0,045 0,14 0,088
Eosinophils
0,139-0,05-0,11 0,028
Lymphocytes
-0,152
-0,38 (
↓
)
-0,34-0,35
Monocytes
0,017-0,1-0,14-0,1
Total bilirubin
-0,19-0,24
-0,41 (
↓
)
-0,27
Direct bilirubin
-0,329
-0,37 (
↓
)-0,51 (
↓
)-0,42 (
↓
)
Indirect bilirubin
-0,097-0,14-0,32-0,16
AST-0,059 0,172 0,34 0,14
ALT-0,168-0,01 0,12-0,04
GGT 0,16 0,253 0,1 0,222
ALP-0,06 0,025 0,1 0,028
Total proteins 0,132 0,263 0,2 0,225
Albumin-0,184-0,31
-0,44
(↓
)-0,36 (
↓
)
Globulins-0,104 0,1240,1 0,029
Albumin/globulins ratio-0,153
-0,48 (
↓
)-0,49 (
↓
)-0,44 (
↓
)
Urea 0,312 0,299
0,36 (
↑
)
0,352
Creatinine 0,338 0,247 0,27 0,328
Values (
↑
) = signifcant increase, values (
↓
) = signifcant decrease.
(Continúa Table 2)
In the white blood cell series, an increase in segmented
neutrophils was observed in dogs with circulatory
presentations, while a decrease in lymphocytes was noted
in the overall group and in those with cutaneous and
circulatory involvement. Tis trend was also observed
in absolute lymphocyte counts for the cutaneous
presentation and was nearly signifcant in the overall
group (Table 2).
Regarding liver function, a decrease in total bilirubin
was detected in dogs with circulatory presentations,
and a decrease in direct bilirubin was observed in those
with cutaneous and circulatory presentations, as well as
in the overall group. Te albumin/globulins ratio also
decreased signifcantly in the overall group and in dogs
with cutaneous and circulatory presentations. However,
albumin levels decreased only in the overall group and
in dogs with circulatory presentations. Serum urea
was signifcantly increased in dogs with circulatory
involvement and was near the signifcance threshold
in the overall group. As in the previous analysis, no
signifcant increases in total proteins or globulins were
observed across diferent clinical presentations or with an
increasing number of clinical signs in the overall group
(Table 2).
Global behavior of clinical signs and hematological, hepatic
and renal profles in Leishmania-seropositive dogs
Tis multidimensional scaling analysis allowed for
the visualization of how clinical signs and laboratory
parameters behaved collectively in a 2D graph, showing
proximity relationships and the emergence of pseudo-
axes that provided physiological meaning to the data
distribution. Based on these premises, the results are
interpreted in two ways.
1-
Relationships between clinical signs and laboratory
parameters in Leishmania-seropositive dogs
T
he clinical signs observed in
Leishmania
-seropositive
dogs were grouped into distinct presentations based on
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Clinical/paraclinical of canine visceral leishmaniasis
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
their pathophysiological signifcance, as illustrated in
Fig.
1:
•
Circulatory presentation: Enlarged lymph nodes,
conjunctivitis, and mucosal pallor. Tese signs
are related to systemic immune responses and
hematological alterations.
•
Cutaneous presentation: Alopecia, onychogryphosis,
nasal and footpad hyperkeratosis, pruritus,
and petechiae. Tese fndings highlight dermal
involvement and localized immune responses.
•
Visceral presentation: Fever, anorexia, vomiting,
sneezing, lameness, and diarrhea. Tese signs refect
the systemic dissemination of the parasite.
•
Renal involvement: Polyuria/polydipsia, indicative of
renal dysfunction likely caused by immune-mediated
glomerulonephritis and tubular damage.
•
Independent signs: Lethargy and weight loss, which
did not integrate into any specifc group, are general
manifestations of chronic systemic disease.
Tese clinical patterns demonstrate the multisystemic
nature of leishmaniasis, driven by immune dysregulation,
chronic infammation, and parasite dissemination.
Figure 1
. Relationship between clinical signs in
Leishmania
-seropositive dogs and hematological, hepatic, and renal
parameters
2- Relationships between laboratory parameters and clinical
signs in Leishmania-seropositive dogs
Fig. 2 illustrates the clustering of hematological,
hepatic, and renal parameters into four distinct sectors,
highlighting their associations with the clinical signs:
•
Liver/Red Blood Cells Group: Tis group includes red
blood cells, hemoglobin, hematocrit, hematimetric
indices (MCV, MCH, MCHC), albumin, the
albumin/globulins ratio, and platelets. It refects the
liver’s role in erythropoiesis and protein synthesis.
•
Immune System/Liver Group: Located at the center,
this group includes immune system cells such as white
blood cells, neutrophils, eosinophils, monocytes, and
lymphocytes, along with hepatic enzymes (AST,
ALT, GGT, and ALP). Cholesterol lies between this
group and the liver/red blood cells group, indicating
its relationship with both. Tese fndings underscore
the liver’s critical role in maintaining immune and
metabolic homeostasis.
•
Liver/Hemoglobin Group: Tis group comprises
total bilirubin, indirect bilirubin, direct bilirubin,
and globulins, refecting the liver’s role in bilirubin
metabolism and globulin production.
•
Renal Group: Urea and creatinine were clustered
separately, forming the renal group, which underscores
the kidney’s role in waste product elimination and
its vulnerability to immune-mediated damage in
leishmaniasis.
•
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Hernández-Russo
et al.
Te visualization highlights the distinct clustering
of laboratory parameters and their associations with
clinical signs, providing a comprehensive understanding
of the pathophysiological relationships in
Leishmania
-
seropositive dogs.
Figure 2.
Relationship between hematological, hepatic and renal parameters with respect to clinical signs in
Leishmania
-
seropositive dogs
DISCUSSION
Regarding the clinical manifestations of dogs seropositive
for
L. infantum
, it was found that 14% showed no
signs compatible with the disease. However, these
asymptomatic animals exhibited decreased platelet counts
and increased total proteins and globulins. Te primary
clinical manifestations recorded align with reports from
various studies (Ciaramella & Corona, 2003; Dias
et al
.,
2008; Perego
et al
., 2014; Sales
et al
., 2017).
Hematological parameters
In the analysis of hematological parameters relative to the
number of clinical signs present, a signifcant decrease
in erythrocyte count, hemoglobin, and hematocrit was
observed in dogs with three or more clinical signs. Tis
relationship has been described by Reis
et al
. (2006),
Nicolato
et al
. (2013), and Dodovski
et al
. (2020).
Conversely, Freitas
et al
. (2012) noted reductions in
erythrocytes, hematocrit, and hemoglobin in animals
with clinical manifestations but found no signifcant
diferences compared to asymptomatic dogs and negative
controls. It is suggested that the clinical severity of the
disease is signifcantly associated with the erythrogram,
and a factor limiting the erythropoietic response may
be linked to higher parasite loads in the bone marrow as
well as elevated uremia levels (Reis
et al
., 2006; Ribeiro
et
al
., 2013; Waugh
et al
., 2024). In contrast, da Costa-Val
et al
. (2007) found no correlation between hematocrit
values and the intensity of clinical signs in dogs. Tey
also identifed anemia as responsible for classic clinical
manifestations of canine leishmaniasis, such as lethargy,
weakness, and weight loss, which, alongside other
protozoan actions and the host’s immune response,
defne case presentations. Additionally, anemia leads
phlebotomines to feed for longer periods or ingest more
blood from animals, both factors contributing to higher
infection rates. Te decrease in MCH concentration
would indicate impaired iron homeostasis (Meléndez-
Lazo
et al
., 2018).
Platelet counts showed no signifcant alterations as
the number of clinical signs increased. Tis is because
thrombocytopenia was recorded in 83.33% of
asymptomatic dogs. In this regard, Foglia-Manzillo
et al
.
59
Clinical/paraclinical of canine visceral leishmaniasis
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
(2013) reported thrombocytopenia and anemia as the
most common early alterations, while da Costa-Val
et al
.
(2007) found no correlation between clinical status and
platelet count. However, Sales
et al
. (2017) described a
trend toward decreased platelet counts in advanced stages
of infection and Muniz dos Santos
et al
. (2023) concluded
that the evaluation of thrombocytopenia is important in
the follow-up of CVL.
Regarding white blood cell parameters, no signifcant
relationship was found between total leukocyte count
and the number of clinical signs. Tis, along with normal
leukocyte counts in most
Leishmania
-positive dogs,
indicates the disease’s minimal infuence on this parameter
(Ribeiro
et al
., 2013). Conversely, Reis
et al
. (2006)
documented a signifcant decrease in absolute leukocyte
counts in symptomatic animals, while Sales
et al
. (2017)
reported an increase. Notably, although eosinophils
showed no changes with increasing clinical signs,
eosinopenia was observed in all animals, reaching 83% in
asymptomatic cases. Absolute neutrophil concentration
remained unchanged as clinical signs increased, consistent
with Reis
et al
. (2006), but Sales
et al
. (2017) detected
neutrophilia in poly- and hypersymptomatic dogs.
Signifcant lymphopenia in poly- and hypersymptomatic
dogs compared to asymptomatic and oligosymptomatic
ones was also observed by Reis
et al
. (2006), da Costa-
Val
et al
. (2007), and Sales
et al
. (2017), attributed to
the disease’s immunosuppressive efect and compensatory
lymphocyte migration to lymphoid organs increased in
advanced stages, serving as a marker of poor prognosis
(Geisweid
et al
., 2012; Nicolato
et al
., 2013; Muniz dos
Santos
et al
., 2023).
Hepatic and renal parameters
Evaluation of liver function via enzymatic activity showed
no diferences with increased clinical signs. In this regard,
Kiral
et al
. (2004) and Freitas
et al
. (2012) observed
no signifcant elevations of transaminases compared
to negative controls and Baxarias
et al
. (2023) found
increases in liver enzymes in 13.2% of cases.
Te signifcant decrease in total and direct bilirubin
with three or more clinical signs may relate to reduced
erythrocyte production (Shcherbinina, 2007). Despite
increased total proteins and globulins in 76.74%
and 93.02% of seropositive animals, respectively, no
diferences were found relative to the number of clinical
signs, likely because these parameters were already
elevated in 66.67% of asymptomatic dogs. Similarly,
Argôlo- Montargil
et al
. (2018) and Baxarias
et al
. (2023)
observed hyperproteinemia in asymptomatic dogs. In
contrast, Freitas
et al
. (2012) recorded signifcantly higher
total protein and globulin levels in the symptomatic
group compared to asymptomatic and negative control
grups. Hyperproteinemia and hyperglobulinemia are
considered among the most common alterations in CVL
(Kiral
et al
., 2004; Sales
et al
., 2017; Camoletto
et al
.,
2020), possibly associated with elevated anti-
Leishmania
antibody levels (Câmara
et al
., 2017).
Te signifcant decrease in albuminemia and albumin/
globulins ratio with a greater number of clinical signs
aligns with fndings by Reis
et al
. (2006), Giunchetti
et
al
. (2008), and Sales
et al
. (2017). Tese fndings were
reported by Amusategui
et al
. (2003) in advanced stage
patients and by Foglia-Manzillo
et al
. (2013) in dogs after
12 months of infection. However, Ribeiro
et al
. (2013)
found no correlation between the number of clinical
signs and proteinogram parameters.
Elevated urea and creatinine levels in infected canines
(Alves
et al
., 2013; Câmara
et al
., 2017) were signifcantly
higher in poly- and hypersymptomatic dogs and are
considered indicators of poor prognosis. Te signifcant
increase in urea would refects early renal damage, as
creatinine changes occur when most nephrons become
dysfunctional (Abbehusen
et al
., 2017; Paludo
et al
.,
2013).
Clinical evolution and disease progression
Te presentation of clinical signs and laboratory
parameters in asymptomatic and oligosymptomatic
infected dogs compared to poly- and hypersymptomatic
ones may represent disease progression. In this sense,
Foglia-Manzillo
et al
. (2013) proposed that infection
gradually progresses from a seemingly normal, temporary
clinical state to an active intermediate stage with few
clinical manifestations, evolving to the classic, severe,
terminal form with more clinical signs and altered blood,
hepatic, and renal parameters. Meanwhile, Donato
et al
.
(2024) demonstrated the relevance of blood cell index
measurements in asymptomatic and symptomatic dogs.
Clinical staging revealed distinct patterns. Te circulatory
presentations included signs visible through mucous
membranes and lymphadenomegaly, involving peripheral
and lymphatic circulation, respectively. A right-to-left axis
was observed, progressing from superfcial mucosal pallor
to deeper conjunctival infammation and ending with
lymphatic system alterations. Te renal presentations
were found to be separate, acting individually but closely
with the circulatory presentations and the proximity to
the lymphadenomegaly may be related to the excessive
60
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Hernández-Russo
et al.
circulation of antibodies through the lymphatic system
that transit to the kidney participating in the renal
alteration (Verde
et al
., 2016).
Te cutaneous presentations showed clinical signs
distributed along an axis from external to deeper skin
layers (Harvey & Mckeever, 2001). Tis axis begins with
superfcial alopecia, onychogryphosis, and nasal/plantar
hyperkeratosis, progressing to deeper vascular damage
evident in petechiae.
Visceral manifestations studied here were limited to those
assessed clinically, excluding signs requiring complex
analyses. Many visceral signs are regulated by the central
nervous system (e.g., hypothalamus and brainstem),
such as diarrhea, sneezing, vomiting, anorexia, and
fever. Tese also result from interrelated factors, such as
chronic infammatory efects on appetite control centers
and high TNF-
α
, IL-1, and IL-6 levels inducing cachexia
(Radostits
et al
., 2007; Costa
et al
., 2023).
Relationships between hematological, hepatic, and renal
parameters in seropositive dogs and clinical signs revealed
hepatic involvement in systemic alterations except renal
function. An inverse relationship between red blood
cell components and bilirubin was observed, separating
erythrocyte formation (liver/red blood cell group: Fig.
2 upper end) and destruction (liver/hemoglobin group:
Fig. 2 lower end), as bilirubin is a hemoglobin catabolite.
Albumin, responsible for bilirubin transport (Hayes,
2004), was located between these groups. Proximity of
erythrocytes, hemoglobin, and hematocrit was logical, as
decreases in these parameters manifest as anemia. Nearby
hematimetric indices refected anemia type. In the liver/
red blood cells group, the location of platelets was also
highlighted, since thrombocytopenia can cause bleeding,
altering erythrocyte counts, with both parameters at
opposite ends. In the center of Fig. 2, the relationship
between the liver and its connection to the immune
system is represented (Aguilar, 2010; Bevilacqua &
Canziani, 2014; Waugh
et al
., 2024).
Te study on CVL caused by
L. infantum
provides crucial
insights into the systemic efects of the disease, combining
fndings from Uruguay with a multidimensional analysis
of clinical and laboratory data. Laboratory analyses
showed progressive alterations in hematological, hepatic,
and renal parameters as clinical severity increased.
Polysymptomatic and hypersymptomatic dogs showed
afected erythropoiesis, characterized by decreases in
red blood cells, hemoglobin, hematocrit, MCH, and
MCHC, as well as increases in segmented neutrophils
and decreases in lymphocytes. Liver function tests
indicated reductions in total and direct bilirubin,
albumin, and the albumin/globulins ratio, while
renal parameters such as urea and creatinine increased
signifcantly with clinical severity. Te multidimensional
analysis highlighted distinct clusters of clinical signs and
laboratory parameters that refect the systemic efects of
the disease. Clinical signs were grouped into circulatory,
cutaneous, visceral, and renal presentations, emphasizing
the multisystemic nature of CVL. Te liver emerged
as a key organ involved in erythropoiesis, immune
regulation, protein synthesis, and bilirubin metabolism.
Renal involvement, characterized by elevated urea and
creatinine, highlighted the role of immune-mediated
glomerulonephritis and tubular damage in disease
progression. Te progressive nature of CVL, from an
asymptomatic state to a severe form with worsening
clinical and laboratory manifestations, emphasizes the
importance of early diagnosis and close monitoring
of hematological, hepatic, and renal parameters. Tis
analysis also highlights the utility of integrating clinical
and laboratory data to comprehensively characterize
disease progression, providing a framework for improved
diagnostic and therapeutic strategies.
In conclusion, CVL represents an emerging health threat
in Uruguay and other endemic regions, characterized
by worsening of erythropoesis, hepatic dysfunction,
and renal impairment as clinical severity increases. Te
fndings emphasize the importance of implementing
control measures, increasing surveillance, and advancing
clinical management strategies to mitigate the disease’s
impact on canine and human populations.
Author contributions: CRediT (Contributor Roles
Taxonomy)
ZHR = Zully Hernández-Russo
MSX = Martín Scayola-Xamo
JC = Juan Cedano
Conceptualization
: ZHR, MSX, JC
Data curation
: ZHR, MSX, JC
Formal Analysis
: ZHR, MSX, JC
Funding acquisition
: ZHR, MSX, JC
Investigation
: ZHR, MSX, JC
Methodology
: ZHR, MSX, JC
Project administration
: ZHR
Resources
: ZHR, MSX, JC
61
Clinical/paraclinical of canine visceral leishmaniasis
Neotropical Helminthology, Vol. 19, Nº1, jan - jun 2025
Software
: ZHR, MSX, JC
Supervision
: ZHR, JC
Validation
: ZHR, MSX, JC
Visualization
: ZHR, JC
Writing-original draft
: ZHR, MSX, JC
Writing-review & editing
: ZHR, MSX, JC
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