Erythrocyte sedimentation rate, C-reactive protein, and interleukin-6 as inflammatory biomarkers in dogs naturally infected with Ehrlichia canis
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Veterinary World, EISSN: 2231-0916 RESEARCH ARTICLE
Available at www.veterinaryworld.org/Vol.14/September-2021/5.pdf Open Access
Erythrocyte sedimentation rate, C-reactive protein, and interleukin-6 as
inflammatory biomarkers in dogs naturally infected with Ehrlichia canis
Thanaporn Asawapattanakul1 , Tanagorn Pintapagung2 , Supawadee Piratae3 , Siriluck Juntautsa4 and
Pawarat Chancharoen4
1. Oxidative Stress Research Unit, Faculty of Veterinary Sciences, Mahasarakham University, Maha Sarakham 44000,
Thailand; 2. Veterinary Clinic Research Unit, Faculty of Veterinary Sciences, Mahasarakham University, Maha Sarakham
44000, Thailand; 3. One Health Research Unit, Faculty of Veterinary Sciences, Mahasarakham University, Maha Sarakham
44000, Thailand; 4. Faculty of Veterinary Sciences, Mahasarakham University, Maha Sarakham 44000, Thailand.
Corresponding author: Thanaporn Asawapattanakul, e-mail: thanaporn.a@msu.ac.th
Co-authors: TP: tanagorn.p@msu.ac.th, SP: supawadee.p@msu.ac.th, SJ: siriluck.j@msu.ac.th,
PC: pawarat.c@msu.ac.th
Received: 11-05-2021, Accepted: 29-07-2021, Published online: 04-09-2021
doi: www.doi.org/10.14202/vetworld.2021.2325-2331 How to cite this article: Asawapattanakul T, Pintapagung T,
Piratae S, Juntautsa S, Chancharoen P (2021) Erythrocyte sedimentation rate, C-reactive protein, and interleukin-6 as
inflammatory biomarkers in dogs naturally infected with Ehrlichia canis, Veterinary World, 14(9): 2325-2331.
Abstract
Background and Aim: Canine monocytotropic ehrlichiosis (CME), a tick-borne disease, leads to a systemic inflammatory
response syndrome; it is thus important to assess the intensity of inflammation in order to treat it appropriately. The current
study was designed to evaluate hematological, biochemical, and inflammatory parameters in dogs naturally infected with
Ehrlichia canis compared with those in healthy dogs. We also assessed the relationship among several inflammation-related
parameters and considered these parameters for use as inflammatory biomarkers of CME.
Materials and Methods: Twenty-eight dogs were divided into two groups based on the results of nested polymerase
chain reaction for detecting E. canis, comprising a healthy group (n=11) and an infected group (n=17). A blood sample
was collected from each dog to evaluate hematological, biochemical, and inflammatory parameters, with the obtained
results being statistically compared between the groups. Moreover, the correlations of erythrocyte sedimentation rate (ESR),
C-reactive protein (CRP), and interleukin-6 (IL-6) were investigated in the 28 dogs.
Results: In the infected group, the mean levels of red blood cells, hemoglobin, and hematocrit were significantly lower than
in the healthy group, while the mean lymphocyte and monocyte counts were higher. The mean levels of ESR and CRP were
significantly higher (pAvailable at www.veterinaryworld.org/Vol.14/September-2021/5.pdf
postoperative monitoring [13-17]. ESR has rarely been dogs) of either sex and any breed, weighing >5 kg, and
analyzed in dogs, but it has been found to be useful in aged between 1 and 5 years. However, we excluded
cases of canine rheumatoid arthritis, osteoarthritis, and any patients if they presented infection with Babesia
babesiosis [18-20]. Moreover, acute-phase proteins, spp. or Anaplasma spp., or exhibited inflammatory
especially C-reactive protein (CRP), produced and conditions such as liver disease, renal disease, derma-
released by the liver, are also used for the clinical diag- titis, wound, or skin neoplasia [27].
nosis and monitoring of inflammatory diseases. CRP All dogs that fulfilled the specific criteria were
levels are known to increase significantly during acute evaluated for their hematological and biochemical
inflammatory processes and host responses to infec- profiles, and were analyzed for E. canis infection
tion [21]. In dogs with acute CME, CRP concentra- using clinical signs, thin blood smear, rapid enzyme-
tions were reported to increase dramatically between linked immunosorbent assay (ELISA, SNAP® 4Dx®
days 4 and 16, peaking at 1-6 weeks after inoculation Plus; IDEXX Laboratories, Westbrook, ME, USA),
with E. canis in dogs; similarly, most dogs with chronic and nested polymerase chain reaction (PCR) using
CME from natural infection presented an increase of E. canis-specific primers (16s rRNA gene). The dogs
CRP levels. Thus, CRP concentration may increase in were then divided into two groups: a healthy group
CME-affected dogs with both acute and chronic clini- and an infected group. The criteria for inclusion in
cal signs [11,22]. Interleukin-6 (IL-6) is a cytokine or each group in this study were as follows:
inflammatory mediator that can be used as a biomarker The healthy group: The dogs showed no notable
of various diseases. Measurement of its level can be clinicopathological signs of E. canis infection, normal
useful for diagnosis and prognostication in both infec- hematological and biochemical profiles, and negative
tious and non-infectious inflammatory diseases, in results for E. canis by thin blood smear, SNAP 4DX®
humans (COVID-19 and total knee replacement sur- Plus test (IDEXX Laboratories, USA), and PCR assay
gery), and animals (canine end-stage renal disease and (n=11).
babesiosis) [23-26]. Although IL-6 has been shown to The infected group: The dogs with and without
have many positive effects on various inflammatory clinical signs showed positive results for E. canis by
diseases in animals, studies on this issue in CME have thin blood smear, SNAP 4DX® Plus test (IDEXX
been limited. It was previously reported that CRP can Laboratories), and PCR assays (n=17).
be useful for tracking inflammation as a parameter for Blood collection and hematological and plasma bio-
predicting severity in various canine inflammatory dis- chemistry profiles
orders including CME [11,12,22]. ESR and IL-6 (IL-6 Blood samples were collected from the cephalic
stimulating the hepatic synthesis of CRP) have not vein and then divided into ethylenediaminetetraacetic
often been considered for use as clinical inflammatory acid (EDTA) tubes and blood serum separator tubes.
biomarkers of animals, and there have been few pub- Each EDTA whole-blood sample was separated for
lications on these parameters in CME-affected dogs. PCR (frozen at -20°C), and the remaining blood was
This study was established to compare hemato- prepared within 2 h for CBC and ESR tests, while
logical and serum biochemistry indices, as well as the plasma serum samples from blood serum separator
intensity of inflammation, using ESR, CRP, and IL-6 tubes were used for biochemical analysis (measure-
levels, between dogs naturally infected with E. canis ments of CRP and IL-6 levels). Hematological and
and healthy dogs. We also assessed the relationship plasma biochemical profiles were analyzed using an
among several inflammatory parameters and consid- IDEXX ProCyte Dx® automated hematology ana-
ered the value of using these parameters as inflamma- lyzer (IDEXX Laboratories) and the TC200 Fully
tory biomarkers of CME. Automatic Chemistry Analyzer (TECOM TC220;
Materials and Methods
TECOM, Jiangxi, China).
Molecular detection of E. canis
Ethical approval and Informed consent
The research protocol and animal experiments For molecular detection in this study, nested
were granted ethical approval by the Institutional PCR was used following a previously reported pro-
Animal Care and Use Committee of Mahasarakham tocol [4]. DNA was extracted from 200 µL of each
University, Thailand (Ethics approval number: EDTA whole-blood sample with the GF-1 Blood DNA
IACUC-MSU-10/2021), and written informed consent Extraction Kit (Vivantis, Malaysia). The concentration
of owners was obtained before starting the research. of extracted DNA was measured using a NanoDrop
1000 spectrophotometer (Thermo Scientific,
Study period and location
Wilmington, DE, USA) at a wavelength of 260 nm.
The study was conducted from October to May A set of oligonucleotide primers for nested PCR was
2021 in the district of Mueang, Maha Sarakham prov- used to amplify the 16s rRNA gene sequences of E.
ince, Thailand. canis, as previously described by Bulla et al. [28].
Patients The nucleotide sequences of the universal primers
The inclusion criteria for animal selection in this of rickettsia for the initial reaction were as follows:
study were as follows: canine patients (client-owned ECC 5’- AGAACGAACGCTGGCGGCAAGCC-3’
Veterinary World, EISSN: 2231-0916 2326Available at www.veterinaryworld.org/Vol.14/September-2021/5.pdf and ECB 5’-CGTATTACCGCGGCTGCTGGCA-3’. Statistical analysis For the later step of PCR, the following Data analysis was performed using IBM SPSS E. canis-specific primers were used: CANIS Statistics Version 22 (IBM, Chicago, IL, USA). The 5’-CAATTATTTATAGCCTCTGGCTATAGGA-3’ obtained data, including hematological and biochem- and HE3 5’-TATAGGTACCGTCATTATCTTCCCTA ical profiles, ESR levels, and the concentrations of T-3’ [4,28]. In the first step of PCR, the PCR mix- CRP and IL-6 were calculated and presented as mean ture with a volume of 25 μL consisted of 50 ng of the ± standard error for each variable and group of dogs. purified DNA, 10 pmol of each primer, 200 μM each Independent t-tests were performed to compare and dNTP, 1.5 mM MgCl2, and 1 U of Taq DNA poly- evaluate the statistical significance of the differences merase (Vivantis). PCR amplification for the identi- in means between the infected group (E. canis-in- fication of E. canis was performed using a Biometra fected dogs) and the healthy group. Correlations GmbH thermocycler (Germany) and consisted of the among inflammatory markers were calculated using following schedule: 2 min at 95°C; 35 cycles of 45 s Pearson’s correlation
Available at www.veterinaryworld.org/Vol.14/September-2021/5.pdf
Figure-1: Comparison of inflammatory biomarkers comprising ESR, serum CRP, and IL-6 in the healthy group and infected
group (Ehrlichia-infected dogs).
Table-1: Hematological and plasma biochemistry indices of healthy and infected groups.
Parameters Unit Healthy group Infected group p-value
Mean±SE Mean±SE
WBC ×103/µL 12.34±0.94 14.17±0.79 0.153
RBC ×106/µL 7.44±0.29 5.42±0.28 0.000*
Platelet ×103/µL 195.09±20.93 47.24±13.15 0.000*
Hemoglobin g/dL 16.60±0.66 11.46±0.61 0.000*
Hematocrit % 46.74±2.00 33.09±1.67 0.000*
MCV fL 62.75±0.83 61.24±0.75 0.196
MCH pg 22.31±0.24 21.16±0.30 0.010*
MCHC g/dL 35.55±0.23 34.55±0.24 0.008*
Neutrophil ×103/µL 7.26±0.69 6.73±0.44 0.502
Lymphocyte ×103/µL 2.92±0.41 4.79±0.46 0.009*
Monocyte ×103/µL 0.69±0.08 1.55±0.19 0.002*
Eosinophil ×103/µL 1.41±0.20 1.16±0.19 0.388
Basophil ×103/µL 0.05±0.01 0.06±0.01 0.775
ALT/SGPT U/L 33.00±8.73 34.81±3.39 0.828
creatinine mg/dL 1.45±0.06 1.25±0.06 0.944
*pAvailable at www.veterinaryworld.org/Vol.14/September-2021/5.pdf
Table-3: Correlations among clinical inflammatory tick-borne diseases [40,41]. In our study, there was no
marker levels in healthy and CME-infected dogs.
significant difference (p>0.05) in serum IL-6 concen-
Measure Statistical values (r) p-value tration between the healthy and CME-infected groups.
ESR-CRP 0.531 0.004* Moreover, the previous studies reported no increases
ESR-IL6 −0.233 0.232 in IL-6 level in CME dogs, in line with our study.
CRP-IL6 0.015 0.941 This may have been caused by the strain-specific
*pAvailable at www.veterinaryworld.org/Vol.14/September-2021/5.pdf
the CME-affected dogs into three subgroups as fol- 2. Mylonakis, M.E., Kritsepi-Konstantinou, M., Dumler, J.S.,
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Authors’ Contributions Vet., 45(1): 1-7.
9. Ziliani, T.F., Castilho, A.R., Poletto, D., Mendonça, A.J.,
TA: Designed and performed the experiment, Sousa, V.R.F., Dutra, V. and de Almeida, A.B.P. (2019)
collected and analyzed the data, and wrote the man- Kidney disease in natural infection by Ehrlichia canis in
uscript. TP: Designed and performed the experiment, dogs. Semin. Cienc. Agrar., 40(2): 981-986.
checked the data analysis, and revised the manuscript. 10. Lachungpa, C.G., Chandrasekaran, D., Thilagar, M.B.
and Kumar, T.S. (2020) Treatment of idiopathic immune
SP: Performed the experiment, revised the method, mediated hemolytic anaemia in dogs. J. Anim. Res., 10(3):
and critically revised the manuscript. SJ: Performed 433-440.
the experiment and critically revised the manuscript. 11. Shimada, T., Ishida, Y., Shimizu, M., Nomura, M.,
PC: Performed the experiment and critically revised Kawato, K., Iguchi, K. and Jinbo, T. (2002) Monitoring
C-reactive protein in beagle dogs experimentally inoculated
the manuscript. All authors read and approved the with Ehrlichia canis. Vet. Res. Commun., 26(3): 171-177.
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Moritz, A., Roth, J. and Peeters, D. (2018) Inflammatory
Acknowledgments
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