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Research Article
Erdem Gülersoy*,Büşra Burcu Erol, Mahmut Ok, Mutlu Sevinç
Evaluation of qSOFA and variation
of hematochemical profile in cats naturally
infected with feline panleukopenia virus
https://doi.org/10.1515/ovs-2022-0118
received November 22, 2022; accepted February 20, 2023
Abstract: Feline panleukopenia (FP)is a fatal viral dis-
ease that predisposes cats to sepsis and organ failure.
Owing to a wide variety of clinical findings, hematochem-
ical examinations are significant for the determination of
early signs of disease-related complications. The aim of
this study is to investigate the diagnostic efficacy of certain
hematochemical parameters together with quick Sepsis-
related Organ Failure Assessment (qSOFA)in cats with
FP. A total of 10 healthy and 30 panleukopenic cats were
included in this study. Physical examinations revealed
that the body temperature was highest in septic panleu-
kopenic cats (p<0.009)and they had higher qSOFA scores
(p=0.000). Hemogram analysis revealed that leukocyte,
lymphocyte, granulocyte, erythrocyte, and hemoglobin
levels were lower in non-septic panleukopenic cats com-
pared with the healthy ones (p<0.030). Also, monocyte
and mean corpuscular hemoglobin levels were lower in
septic ones (p<0.048). Serum biochemistry profiling
revealed higher blood urea nitrogen, creatinine, alanine
aminotransferase, lactate dehydrogenase, total bilirubin,
and C-reactive protein levels in panleukopenic cats
(p<0.033). As a result, it was concluded that although
the qSOFA is not sufficient to distinguish sepsis in cats,
unlike dogs, in order to achieve a positive clinical out-
come, when evaluated together with hematochemical vari-
ables, it may help in making early diagnosis of FP-related
complications.
Keywords: cat, feline panleukopenia, diagnosis
1 Introduction
Feline panleukopenia (FP)is the oldest known viral dis-
ease of cats and has been protected by vaccination since
1934 with formalin-inactivated tissue extracts from
infected cats [1]. Although the incidence of the disease
has decreased with vaccination rates of up to 82% in
2016, sporadic outbreaks still occur in some countries,
including the United Kingdom, Australia, and the United
States of America [1,2].
FP infection often occurs in unvaccinated and/or
incompletely vaccinated cats [3]. The main route of trans-
mission of the feline parvovirus (FPV), which is shed in
high amounts in saliva, urine, feces, and vomitus, is the
orofecal route and, more rarely, inhalation of aerosolized
virus [4]. Since the virus only replicates in actively diving
S-phase cells, it has tropism to lymphoid tissue, bone
marrow, intestinal crypt epithelium, and to Purkinje cells
of the cerebellum in neonatals younger than 10 days old
[5]. In addition to peracute death due to septic shock in
cats younger than 2 months of age, the most common
clinical presentation of FP is fever up to 41°C, lethargy,
anorexia, vomiting, diarrhea, and severe dehydration [6].
Also, hypersalivation due to nausea and thickened intest-
inal loops and enlarged mesenteric lymph nodes can be
detected on abdominal palpation [2]. Hemorrhagic diar-
rhea is very rare in cats compared to parvovirus infection
of dogs [7]. Common laboratory findings in FP-affected
cats are leukopenia (65–75% of cases), thrombocytopenia
(55% of cases)[6], hypoalbuminemia (45–52% of cases),
hypoproteinemia (30% of cases), and elevated liver
enzyme levels (27% of cases)[8]. As reported previously,
the diversity and variable incidences of clinical and
laboratory findings may complicate the early diagnosis
of the disease. In addition, the increased risk of circula-
tory shock, organ dysfunction, sepsis, and disseminated
intravascular coagulopathy (DIC)in cats with FPV makes
clinical diagnosis more difficult because the clinical mani-
festation of septic cats is different from that of septic dogs.
* Corresponding author: Erdem Gülersoy, Department of Internal
Medicine, Faculty of Veterinary Medicine, Harran University,
63000, Şanlıurfa, Turkey, e-mail: egulersoy@harran.edu.tr,
tel: +90-5333344042
Büşra Burcu Erol, Mahmut Ok, Mutlu Sevinç: Department of Internal
Medicine, Faculty of Veterinary Medicine, Selçuk University,
42250, Konya, Turkey
Open Veterinary Science 2023; 4: 20220118
Open Access. © 2023 the author(s), published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 International
License.
This difference also increases the importance of early diag-
nosis [9]. Fecal antigen enzyme-linked immunosorbent
assay (ELISA)test kits developed and frequently used for
diagnostic purposes may cause false positive results after
vaccination with modifiedlive vaccine (MLV)for at least 14
days [10]. Also, commercial polymerase chain reaction
(PCR)assays may not be able to distinguish between feline
and canine parvovirus strains. Moreover, diagnostic methods
such as virus isolation, hemagglutination assays, and immuno-
electron microscopy are time-consuming and require
equipment and expertise [2,11]. For this reason, when rou-
tine laboratory analyses including hemogram and serum
biochemistry variables are evaluated together with clinical
scores such as quick Sepsis-related Organ Failure Assess-
ment (qSOFA), which is frequently evaluated in septic
dogs [12], it can facilitate the diagnosis of complications
such as disease-related organ failure and predict mortality
and length of stay in the intensive care unit (ICU)in the
clinical setting.
FP is diagnosed on the basis of history, clinical, and
hematochemical findings, and by virus detection using
commercial fecal ELISA kits [2]. Even though they may
seem deceivingly basic, routine clinical and laboratory
examinations allow determination of early signs of dis-
ease and severe conditions. Thus, they have an important
role in clinical practice in both diagnosis and manage-
ment. Also, studies conducted under experimental con-
ditions might not represent the findings in naturally
infected cats. Therefore, the aim of this study is to inves-
tigate the diagnostic efficacy of the qSOFA score, which
has been less studied in cats as opposed to dogs, along
with the physical and laboratory examinations including
hemogram and serum biochemistry profile in cats natu-
rally infected with FPV with and/or without sepsis.
2 Materials and methods
The study was designed to include the cats presented to
the Animal Hospital of Veterinary Faculty, Harran University,
Turkey, between 2021 and 2022 that were screened for FPV
infection as part of the medical workup.
2.1 Animals
The Panleukopenia group of the present study consisted
of 30 client-owned unvaccinated cats aged between 1
and 11 months, which were admitted for diagnosis and
treatment purposes with clinical findings compatible with
FP such as diarrhea, vomiting, inappetence, weight loss,
dehydration, and bone marrow suppression (secondary
bacterial infections). The Control group consisted of ten
cats of similarage and body weight, which weredetermined
to be healthy by clinical and laboratory examinations. The
median body weight of the panleukopenic cats was 1.4
(0.8–2.2)and the healthy cats were 1.55 (1–2)kg (p<0.648).
While14ofthepanleukopeniccatsweremaleand16were
female, 5 of the healthy cats were male and 5 were female.
Ethical approval: The research related to animal use has
been complied with all the relevant national regulations
and institutional policies for the care and use of animals.
We informed and received the permission of the owners of
the cats included in this study to take samples used in the
present study. Samples were collected as per standard
sample collection procedure without any harm to animals.
2.2 Physical examinations
Physical examinations, including lung and heart auscul-
tation, evaluation of mucous membrane, capillary refill
time (CRT), palpable lymph nodes, mental state, and sys-
tolic blood pressure (SBP), were performed by the same
personnel with the same examination protocol. Feline
ataxia was not present in any of the cats with suspected
panleukopenia in the present study. Thus, it was ensured
that the diseased cats in the present study were exposed
to the virus naturally via the orofecal route, not in utero.
During SBP measurement, to minimize stress, cats were
allowed to assume a comfortable position with only
gentle restraint by their owners and remained in the
same position throughout the measurement. An infla-
table cuffwas applied to one of the legs of the cats and
the cuffwas temporarily filled with air until the blood
flow was impeded. Cats that needed very strict restrain
or were very aggressive were excluded from the study.
Five to seven consecutive and consistent measurements
were made, all readings were recorded whether or not
used to calculate SBP, and the SBP was calculated as
the mean of these using a multi-parameter veterinary
monitor (BM7Vet Elite, Bionet, USA).
2.3 Sepsis criteria and detection of its
presence
The criteria for the presence of sepsis in the panleuko-
penic cats were as follows: (1)body temperature: >39.7 or
2Erdem Gülersoy et al.
<37.7°C, (2)heart rate: >225 or <140 bpm, (3)respiratory
rate: >40 bpm, and (4)total WBC count: >19,500 cells or
<5,000 cells [13]. Since the classical or hyperdynamic
phase, which is frequently observed in septic dogs, is
rarely observed in cats and, unlike dogs, clinical findings,
such as pale mucous membranes, prolonged CRT, and
weak or absent pulse, are evident in cats [14], these para-
meters were also considered in addition to the sepsis
criteria.
2.4 qSOFA criteria and calculation of scores
Since the Sepsis-3 consensus suggested including the
presence of an organ failure in the presence of sepsis,
three criteria for qSOFA were considered in this study [15].
They are as follows: (1)altered mental state (0=normal;
1=able to stand unaided, alert but stagnant; 2 =able to
stand with assistance, environmentally sensitive but
stagnant; 3 =unable to stand, alert; 4 =unable to stand,
apathetic),(2)respiratory rate >22 breaths/min, and (3)
SBP <100 mmHg. It was reported that the qSOFA score
>2 is associated with higher mortality and longer ICU
duration [16]. Septic cats included in the study were
evaluated based on respiratory rate >22 breaths/min,
SBP <100 mmHg, or presence of altered mental status
in terms of qSOFA evaluation. The qSOFA score was
accepted as 1 for each criterion.
2.5 Application of rapid diagnostic test kits
Fecal samples were obtained from FP suspected cats with
anal or rectal swabs. At first, swabs were wetted with
sterile isotonic and the sample was taken rectally in cases
with no feces in the anus and perineum. Due to its low-to-
moderate sensitivity (50–80%)and good-to-excellent
specificity (94.2–100%), the IDEXX SNAP Parvo test
was used for diagnosis [8,17]and the tests were per-
formed by trained research assistants at the central
laboratory according to the manufacturer’sinstructions.
Positive results were recorded as weakly positive or
positive according to color intensity.
2.6 Inclusion criteria
Inclusion criteria to suspect FP were the presence of clini-
cally compatible findings (absence of diarrhea, vomiting,
lethargy, and fever in kittens; presence of anorexia, hypor-
exia, lethargy, vomiting, and diarrhea in older cats)and
abnormal laboratory findings (leukopenia and anemia)
along with positive fecal IDEXX SNAP Parvo test result [18].
Cats with a previous history of disease or had blood transfu-
sion were not included in the study. All cats included in the
study were examined for feline leukemia virus (FeLV)and
feline immunodeficiency virus (FIV)presence (IDEXX SNAP
FIV/FeLV Combo Test; IDEXX Laboratories)using rapid diag-
nostic test kits measuring p27 antigen for FeLV (sensitivity of
98.6% and specificity of 98.2%)and antibodies for FIV (sen-
sitivity of 93.5% and specificity of 100%).Allcatsweretested
once and cats with insufficient/suspicious results were
excluded from the study. In addition, microscopic fecal
examinations of all the cats were performed and no
parasitesand/oreggswerefound.
2.7 Blood sampling and performing
hemogram and biochemical analyses
Venous blood samples were obtained from all the cats
with minimal restraint and patient stress by vena cephalica
or vena jugularis venepuncture (3–5mL). Hematological
parameters (leukocyte [WBC], lymphocyte, monocyte, gran-
ulocyte, erythrocyte [RBC],meancorpuscularvolume
[MCV],hematocrit[Hct], mean corpuscular hemoglobin
[MCH], mean corpuscular hemoglobin concentration
[MCHC]and hemoglobin [Hb]) were measured from blood
samples with K
3
EDTA using an automated hematology
analyzer (Sysmex poch-100i, Canada)within 5–10 min
after sampling. Serum biochemistry parameters (blood
urea nitrogen [BUN], creatinine, aspartate aminotrans-
ferase [AST], alanine aminotransferase [ALT],alkaline
phosphatase [ALP], lactate dehydrogenase [LDH],phos-
phorous, cholesterol, total bilirubin, albumin, total pro-
tein, and C-reactive protein [CRP]) were measured from
serum samples (after centrifugation of serum tubes at
5,000 rpm for 10 min)using automatic biochemistry analyzer
(Spotchem EZ SP-4430, Arkray, Japan)within 10–20 min
after sampling. All results were compared with laboratory
reference values.
2.8 Statistical analysis
Data analysis was evaluated using SPSS 25.00 (SPSS for
Windows)statistical software and one sample Kolmogorov–
Smirnov test was applied to determine whether all data
were parametric or non-parametric. Non-parametric data
Evaluation of qSOFA and hematochemical profile in cats with FP virus 3
were evaluated as median (min, max)using Mann–Whitney
U, Kruskal–Wallis test. Data analysis of three groups was
performed with one-way ANOVA or Kruskal–Wallis test
depending on the distribution pattern. In addition, in
order to measure the statistical relationship, or associa-
tion, between qSOFA score and the hematochemical pro-
file variables Spearman’s rank correlation coefficient test
was performed. The strength of the correlation was inter-
preted using the following guide for the absolute value of
rs: 0.00–0.19 as very weak, 0.20–0.39 as weak, 0.40–0.59
as moderate, 0.60–0.79 as strong, and 0.80–1.0 as very
strong. In order to investigate how accurately the present
diagnostic tests discriminate the presence of sepsis and to
determine optimal cut-offvalues receiver operating char-
acteristic (ROC)curve analyses were performed. The diag-
nostic performance of clinical and hematochemical vari-
ables was evaluated with parameters, including the
area under curve (AUC, >0.700),pvalue (<0.05),sen-
sitivity and specificity (>70%). Statistical significance
was regarded as p<0.05.
3 Results
3.1 Physical examination findings
Clinical and hematological examinations revealed that 13
of the cats in the Panleukopenia group had sepsis (13 out
of 30, 43%). Mental status change was more evident in
cats with septic FP (mostly unable to stand but alert, n:9;
or unable to stand, apathetic, n:4). Of the palpable
lymph nodes, swelling was evident in all cats with FP,
mainly in the submandibular and popliteal nodules. No
remarkable finding was detected in abdominal palpation.
As a result of physical examination, when healthy,
septic, and non-septic panleukopenic cats were evalu-
ated together, the body temperature was highest in
septic panleukopenic cats (p<0.009).Comparedwith
the healthy cats, all of the panleukopenic cats had
higher respiratory rate, mental status, and qSOFA scores
(p=0.000)and lower SBP values (p=0.000).Inthe
comparison of septic and non-septic panleukopenic cats,
no statistical difference was found in other parameters
(p>0.05)except body temperature (p=0.000).Within
the scope of qSOFA scoring, it was determined that all cats
with FP had a respiratory rate of >22 breaths/min, 15 out of
30 had an SBP of <100 mmHg, and 18 out of 30 were able
to stand with assistance, alert but stagnant. Physical
examination findings and qSOFA scores are presented in
Tables 1 and 2, and qSOFA score evaluation is presented in
Table 3.
3.2 Hemogram analysis findings
As a result of hemogram analysis, it was observed that
WBC, lymphocyte, granulocyte, monocytes, RBC, and
hemoglobin levels of the septic panleukopenic cats were
lower compared with the healthy cats (p<0.016).WBC,
lymphocyte, granulocyte, RBC, and hemoglobin levels
were lower in non-septic panleukopenic cats compared
with the healthy ones (p<0.030). In septic panleukopenic
cats, monocyte and MCH were determined to be lower
(p<0.048).Nostatisticaldifference was determined in
other parameters. Hemogram analysis results are pre-
sented in Tables 4 and 5.
Table 1: Physical examination findings and qSOFA scores
Parameters Control group (n:10)median (min–max)Panleukopenia group (n:30)median (min–max)
Septic FP (n:13)Non-septic FP (n:17)
Heart rate (beats/min)120 (110–134)128 (106–144)120 (100–152)
Body temperature (rectal, °C)38.6 (38.2–39.2)39.9 (39.7–40.5)39.1 (38.3–39.6)
CRT (s)2(2–3)3(1–4)2(1–4)
Respiratory rate (breaths/min)33 (22–44)66 (56–92)72 (58–90)
Systemic blood pressure (mmHg)125 (120–134)102 (90–122)100 (88–112)
Mental state (ranging from 1 to 3)0(0–0)3(2–4)2(2–4)
qSOFA (ranging from 1 to 3)1(1–1)2(2–3)2(2–3)
qSOFA –quick Sepsis-related Organ Failure Assessment.
4Erdem Gülersoy et al.
3.3 Serum biochemistry profiling findings
As a result of serum biochemistry profiling, septic pan-
leukopenic cats had higher BUN, creatinine, ALT, LDH,
total bilirubin, and CRP levels compared with the healthy
cats (p<0.033). Non-septic panleukopenic cats also had
higher BUN, creatinine, AST, ALT, LDH, phosphorus,
Table 2: pValues of intergroup comparison of physical examination findings and qSOFA scores (pvalue <0.05: bold)
Parameters pValues
Control vs septic FP Control vs non-septic FP Septic FP vs non-septic FP
Heart rate (beats/min)0.291 0.801 0.508
Body temperature (rectal, °C)0.000 0.009 0.000
CRT (s)0.356 0.973 0.496
Respiratory rate (breaths/min)0.000 0.000 0.321
Systemic blood pressure (mmHg)0.000 0.000 0.657
Mental state (ranging from 1 to 3)0.000 0.000 0.097
qSOFA (ranging from 1 to 3)0.000 0.000 0.380
qSOFA –quick Sepsis-related Organ Failure Assessment.
Table 3: qSOFA criteria and scoring
Parameters Distribution (%)
Respiratory rate >22 breathgs/min 30 out of 30 (100)
Systemic blood pressure <100 mmHg 15 out of 30 (50)
Mental state =2; 18 out of 30 (60)
=3; 12 out of 30 (40)
Table 4: Hemogram analysis results
Parameters Control group (n:10)median (min–max)Panleukopenia group (n:30)median (min–max)
Septic FP (n:13)Non-septic FP (n:17)
WBC (×10
9
cells/L)10.75 (5.39–18.03)2.48 (0.33–8.04)3.55 (0.4–10.29)
Lym (×10
9
cells/L)4.12 (1.93–9.47)1.6 (0.26–4.74)1.89 (0.32–5.21)
Gran (×10
9
cells/L)4.6 (2.16–8.49)0.59 (0.03–6.62)0.6 (0.01–3.4)
Mon (×10
9
cells/L)0.79 (0.2–2.44)0.14 (0.01–0.99)0.48 (0.03–2.33)
RBC (m/mm
3
)8.64 (3.24–12.7)5.8 (3.33–9.6)5.5 (3.52–12.83)
MCV (fl)45.6 (36.5–66.6)48.9 (37.7–73.7)47.9 (36.1–77.8)
MCH (pg)13.15 (10.2–28)13.2 (7.2–17.1)14.5 (12.1–23.2)
MCHC (g/dL)29 (23.9–42.3)25.3 (16.7–36.1)29.2 (19.3–36.8)
Hb (g/dL)12.7 (9.1–14.7)8.1 (3.8–12.7)9(5.4–17.4)
WBC –leukocyte, Lym –lymphocyte, Gran –granulocyte, Mon –monocyte, RBC –erythrocyte, MCV –mean corpuscular volume,
MCH –mean corpuscular hemoglobin, MCHC –mean corpuscular hemoglobin concentration, Hb –hemoglobin.
Table 5: pValues of intergroup comparison of hemogram analysis results (p<0.05: bold)
Parameters pValues
Control vs septic FP Control vs non-septic FP Septic FP vs non-septic FP
WBC (×10
9
cells/L)0.000 0.000 0.716
Lym (×10
9
cells/L)0.005 0.006 0.785
Gran (×10
9
cells/L)0.001 0.000 0.765
Mon (×10
9
cells/L)0.016 0.425 0.039
RBC (m/mm
3
)0.004 0.030 0.269
MCV (fl)0.248 0.183 0.896
MCH (pg)0.427 0.639 0.048
MCHC (g/dL)0.146 0.930 0.106
Hb (g/dL)0.000 0.023 0.242
WBC –leukocyte, Lym –lymphocyte, Gran –granulocyte, Mon –monocyte, RBC –erythrocyte, MCV –mean corpuscular volume,
MCH –mean corpuscular hemoglobin, MCHC –mean corpuscular hemoglobin concentration, Hb –hemoglobin.
Evaluation of qSOFA and hematochemical profile in cats with FP virus 5
total bilirubin, and CRP levels compared with the healthy
ones (p<0.032). In septic panleukopenic cats, only
albumin level was determined to be lower (p<0.032).
No statistical difference was determined in other para-
meters. Serum biochemistry analysis results are presented
in Tables 6 and 7.
3.4 Spearman’s rank correlation coefficient
test results
Spearman’s correlation test result revealed positive very
strong correlations between WBC and lymphocyte (rs:
0.832), WBC and granulocyte (rs: 0.816); positive strong
correlations between WBC and monocytes (rs: 0.712),
lymphocyte and monocytes (rs: 0.653), hemoglobin and
RBC (rs: 0.762), and LDH and BUN (rs: 0.603). When all
parameters were taken into account, CRP was the only
parameter with which the qSOFA score showed a signifi-
cant correlation and its strength was determined to be
positively strong (rs: 0.687). Spearman’s correlation test
results are presented in the Supplementary file.
3.5 ROC analysis
ROC analysis revealed that body temperature (AUC: 1.000),
WBC (AUC: 0.967), and granulocyte counts (AUC: 0.937)
Table 6: Serum biochemistry profiling
Parameters Control group (n:10)median (min–max)Panleukopenia group (n:30)median (min–max)
Septic FP (n:13)Non-septic FP (n:17)
BUN (mg/dL)16.2 (5.1–20.6)33.4 (19.6–86)30.4 (10.1–114.4)
Crea (mg/dL)0.75 (0.5–1.2)2.3 (0.7–8.1)2.4 (0.4–25.1)
AST (U/L)26.5 (15–55)53 (20–372)50 (17–161)
ALT (U/L)34 (16–76)70 (19–118)54 (19–184)
ALP (U/L)37.5 (12–169)22 (13–116)42 (4–270)
LDH (U/L)101 (38–198)205 (93–1,429)367 (52–750)
Phosphorous (mg/dL)5.55 (2.8–7.3)6.1 (4.2–9.3)6.6 (2.8–14.4)
Cholesterol (mg/dL)143.5 (103–213)153 (107–237)183 (105–431)
Total bilirubin (mg/dL)0.4 (0.1–1.1)0.9 (0.4–2.3)1.1 (0.3–3.9)
Albumin (g/dL)2.9 (2.6–3.7)2.6 (1.4–3.7)3.2 (2.2–4.6)
Total protein (g/dL)6.5 (5.4–7.5)7.3 (4.2–11)7.3 (4.7–12.9)
CRP (mg/L)0.2 (0.1–0.2)0.6 (0.3–1.8)0.8 (0.3–2.1)
BUN –blood urea nitrogen, Crea –creatinine, AST –aspartate aminotransferase, ALT –alanine transaminase, ALP –alkaline phosphatase,
LDH –lactate dehydrogenase, CRP –C-reactive protein.
Table 7: pValues of intergroup comparison of serum biochemistry profiling results (p<0.05: bold)
Parameters pValues
Control vs septic FP Control vs non-septic FP Septic FP vs non-septic FP
BUN (mg/dL)0.001 0.003 0.355
Crea (mg/dL)0.002 0.032 0.570
AST (U/L)0.052 0.022 0.220
ALT (U/L)0.007 0.012 0.958
ALP (U/L)0.504 0.568 0.247
LDH (U/L)0.033 0.000 0.880
Phosphorous (mg/dL)0.198 0.020 0.191
Cholesterol (mg/dL)0.400 0.072 0.263
Total bilirubin (mg/dL)0.004 0.001 0.590
Albumin (g/dL)0.193 0.250 0.032
Total protein (g/dL)0.374 0.083 0.573
CRP (mg/L)0.000 0.000 0.293
BUN –blood urea nitrogen, Crea –creatinine, AST –aspartate aminotransferase, ALT –alanine transaminase, ALP –alkaline phosphatase,
LDH –lactate dehydrogenase, CRP –C-reactive protein.
6Erdem Gülersoy et al.
had excellent efficacy, RBC value (AUC: 0.817)had good
efficacy, mental state evaluation (AUC: 0.798)and CRP level
(AUC: 0.793)had fair diagnostic efficacy for detecting the
presence of sepsis in panleukopenic cats. ROC analysis
results of clinical findings are presented in Table 8;ROC
analysis results of hemogram findings are presented in
Table 9; and ROC analysis results of serum biochemistry
findings are presented in Table 10. In addition, ROC curves
of clinical findings, hemogram and serum biochemistry
parameters are presented in Figure 1(a–c), respectively.
4 Discussion
FP is a fatal, highly contagious, viral disease of cats
caused by FPV with the peculiar clinical and hematolo-
gical alterations [19]. Early detection of FP with accurate
testing methods including point-of-care tests and routine
laboratory analyses such as hematochemical profiling is
very important to identify infected cats as the disease
increases susceptibility to the development of organ dys-
function, sepsis, and DIC. In the present study, it was
determined that sepsis developed in 43% of the panleu-
kopenic cats along with significant clinical and hematochem-
ical alterations such as elevated body temperature, altered
mental state, leukopenia, hypoalbuminemia, and high CRP
levels (p<0.05). Also, it was observed that the qSOFA score
was strongly (positive)correlated only with the serum CRP
level, although it could not differentiate the septic cats from
the non-septic panleukopenic ones (p>0.293).
The most common presentation of FP is characterized
by an acute course of disease over several days with
fever, lethargy, anorexia, vomiting, diarrhea, and severe
dehydration. Only some of these signs may be present,
vomiting usually precedes diarrhea, and in contrast to
dogs with parvoviral enteritis, hemorrhagic diarrhea is
much less common, ranging from 3 to 15% of cats with
Table 8: Clinical examination findings and qSOFA score
Parameter AUC Std. error pValue Asymp. 95% CI Cut-offSensitivity (%)Specificity (%)
Lower bound Upper bound
Heart rate (beats/min)0.603 0.099 0.299 0.409 0.796 119 76.9 40.7
Body temperature (rectal, °C)1.000 0.000 0.000 1.000 1.000 39.65 100 100
CRT (s)0.578 0.094 0.427 0.394 0.763 2.5 53.8 56.6
Respiratory rate (breaths/min)0.613 0.088 0.254 0.440 0.785 59 84.6 44.4
Systemic blood pressure (mmHg)0.352 0.089 0.133 0.177 0.527 101 53.8 33.3
Mental state (ranging from 1 to 3)0.798 0.071 0.003 0.658 0.937 2.5 92.3 74.1
qSOFA (ranging from 1 to 3)0.634 0.086 0.175 0.465 0.803 2.5 30.8 69.4
qSOFA –quick Sepsis-related Organ Failure Assessment, AUC –area under curve, Std. Error –standard error, CI –confidence interval.
Bold rows indicate statistical significance.
Table 9: Hemogram findings
Parameter AUC Std. error pValue Asymp. 95% CI Cut-offSensitivity (%)Specificity (%)
Lower bound Upper bound
WBC (×10
9
cells/L)0.967 0.026 0.000 0.916 1.000 5.37 100 80
Lym (×10
9
cells/L)0.853 0.061 0.001 0.734 0.973 1.91 100 60
Gran (×10
9
cells/L)0.937 0.037 0.000 0.865 1.000 2.02 100 83.3
Mon (×10
9
cells/L)0.725 0.081 0.035 0.565 0.885 0.39 90 56.7
RBC (m/mm
3
)0.817 0.096 0.003 0.628 1.000 6.97 90 80
MCV (fl)0.405 0.097 0.373 0.216 0.594 45.25 60 40
MCH (pg)0.435 0.114 0.542 0.212 0.658 14.3 40 53.3
MCHC (g/dL)0.562 0.101 0.563 0.365 0.759 27.9 70 46.7
Hb (g/dL)0.822 0.065 0.003 0.694 0.950 9.05 100 63.3
WBC –leukocyte, Lym –lymphocyte, Gran –granulocyte, Mon –monocyte, RBC –erythrocyte, MCV –mean corpuscular volume,
MCH –mean corpuscular hemoglobin, MCHC –mean corpuscular hemoglobin concentration, Hb –hemoglobin, AUC –area under curve,
Std. Error –standard error, CI –confidence interval.
Bold rows indicate statistical significance.
Evaluation of qSOFA and hematochemical profile in cats with FP virus 7
FP [7]. The clinical signs of FP are most severe in cats less
than 6 months of age [2]. As previously reported, adult
cats generally manifest a transient fever and depression.
Also, especially in kittens less than 2 months old, disease
can be peracute, resulting in sudden death from septic
shock with no premonitory signs [18]. The most common
clinical findings identified in the cats with FP in the pre-
sent study were fever (n: 22, 73%), lethargy (n: 21, 70%),
anorexia (n: 30, 100%), vomiting (n: 14, 47%), diarrhea
(n: 11, 37%), and severe dehydration (n: 19, 63%). These
findings were more severe in the cats less than 6 months
old (all findings were present in 13 of 30 panleukopenic
cats, 43%)of the present study. Considering the epide-
miological data of the panleukopenic cats of the present
study, the severity of the clinical findings may be related
to early age, being unvaccinated, and immunity gap [3].
Also, the lower respiratory rate (p=0.000)of the septic
panleukopenic cats compared with non-septic ones may
be related to compromised respiratory reflex due to the
development of sepsis, and fever may be associated with
secondary infections due to transient immunosuppression
[14]. Moreover, the fact that no difference was detected
in the CRT and heart rate values between the groups
(p>0.05)supports the fact that hemodynamic changes
in septic cats are different from the classical sepsis mani-
festation, which is frequently accompanied by a hyper-
dynamic phase [13,14]. In the ROC analysis, which was
performed to investigate the presence of sepsis in pan-
leukopenic cats, it was observed that the body temperature
value had excellent performance (AUC: 1.000)and the
mental state evaluation (AUC: 0.798)had good diagnostic
performance. In a previous study, it was reported that
subtle changes in body temperature patterns may be an
early indicator of sepsis [20]. As the rectal temperature in
healthy cats can reach 39.3°C in the veterinary consulta-
tion room due to stress, it was observed that a cut-offvalue
of 39.6°C of the present study was related to infection/
inflammation [6]. It is a fact that sepsis is often character-
ized by an acute brain dysfunction associated with
increased morbidity and mortality. In the majority of
panleukopenic cats (60%)of the present study, mental
status was characterized by being able to stand with
assistance and environmentally sensitive but stagnant.
These findings may be related to excessive microglial
activation, impaired cerebral perfusion, blood–brain-bar-
rier dysfunction, and altered neurotransmission caused by
panleukopenia [21,22].
Following the orofecal transmission, viral replication
in oropharyngeal lymphoid tissue occurs within 18–24 h
and viremia can be detected within 2–7 days post-infec-
tion. Clinical disease occurs after an incubation period of
2–10 days [2]. FPV infects and kills cells that are asso-
ciated with replication and causes cytopathic effects of
rapidly growing and dividing, such as those in the bone
marrow, lymphoid cells, and intestines [23]. As the virus
infects all tissues, including lymphoid tissue, with cell-
free viremia, cellularity decreases [1,2,23]. In most cats,
gastrointestinal (GI)signs coincide with severe leuko-
penia, with early neutropenia from neutrophil losses
into the GI tract, followed by leukopenia from bone
marrow suppression [7]. In addition, as the GI barrier is
often destroyed in panleukopenic cats, intestinal
Table 10: Serum biochemistry findings
Parameter AUC Std. error pValue Asymp. 95% CI Cut-offSensitivity (%)Specificity (%)
Lower bound Upper bound
BUN (mg/dL)0.591 0.091 0.331 0.412 0.770 22 76.5 41.8
Crea (mg/dL)0.634 0.096 0.151 0.447 0.822 2.05 70.6 65.2
AST (U/L)0.529 0.096 0.753 0.341 0.717 44 58.8 56.5
ALT (U/L)0.606 0.092 0.256 0.426 0.787 41.5 70.6 52.2
ALP (U/L)0.526 0.099 0.784 0.332 0.719 25.5 64.7 47.8
LDH (U/L)0.670 0.092 0.069 0.490 0.850 163.5 70.6 47.8
Phosphorus (mg/dL)0.706 0.087 0.028 0.534 0.877 6.15 82.4 65.2
Cholesterol (mg/dL)0.646 0.090 0.119 0.469 0.823 149.5 70.6 47.8
Total bilirubin (mg/dL)0.712 0.083 0.023 0.550 0.874 0.6 88.2 56.5
Albumin (g/dL)0.662 0.090 0.082 0.485 0.840 2.95 70.6 59.9
Total protein (g/dL)0.624 0.092 0.185 0.443 0.805 7.2 64.7 59.9
CRP (mg/L)0.793 0.072 0.002 0.651 0.935 0.65 82.4 73.9
BUN –blood urea nitrogen, Crea –creatinine, AST –aspartate aminotransferase, ALT –alanine transaminase, ALP –alkaline phosphatase,
LDH –lactate dehydrogenase, CRP –C-reactive protein, AUC –area under curve, Std. error –standard error, CI –confidence interval.
Bold rows indicate statistical significance.
8Erdem Gülersoy et al.
ROC cu
examina
and qSO
rves of phys
tion parame
FA score
ical
ters
Heart rate
Body tempe
CRT
Respiratory
SBP
Mental state
qSOFA
Reference li
rature
rate
e
ne
ROC cu
hemogra
ROC cu
biochem
rves of
m paramete
rves of serum
istry variabl
rs
es
WBC
Lymphocyte
Granulocyte
Monocyte
RBC
MCV
MCH
MCHC
Hb
Reference lin
BUN
Creanine
AST
ALT
ALP
LDH
Phosphorous
Cholesterol
Total Bilirubi
Albumin
Total protein
CRP
Reference lin
ne
s
n
n
ne
Figure 1: ROC curves of clinical findings, hemogram and serum biochemistry parameters.
Evaluation of qSOFA and hematochemical profile in cats with FP virus 9
bacteria can invade the bloodstream and bacteraemia
combined with neutropenia can lead to sepsis in these
immunocompromised animals [18]. Thus, abnormal hema-
tological findings such as leukopenia, which is character-
ized by neutropenia and lymphopenia, are frequently
encountered in cats with FP [2,6,9]. In the present study,
the panleukopenic cats had lower WBC, lymphocyte, and
granulocyte levels than the healthy cats (p<0.006).When
considering the presence of sepsis, the monocyte levels of
the septic panleukopenic cats were lower than the non-
septic ones (p<0.039). The abnormal leukogram patterns
detected in the present study can be explained by the
direct cytopathic effects of the FPV on the bone marrow.
In addition, conditions that contribute to the development
of cytopenia, persistent or cyclic neutropenia, and lym-
phopenia may include thymic atrophy, myelosuppressive
syndrome, and depletion of the paracortical regions of the
lymph nodes [22]. Also, leukopenia which is not generally
considered a normal response to infection could be as a
sign of sepsis-defining hematological organ dysfunction
within the Sepsis-3framework[24]. Several mechanisms
such as increased use in tissue, bone marrow damage, lack
of neutrophil production, and sequestration of neutrophils
as a result of endotoxemia are reported for the develop-
ment of neutropenia in FP [6].Duringsepticconditions,
neutrophils experience highly dysregulated functions such
as recruitment of immature cells, impaired migration, inef-
ficient pathogen recognition, and tissue damage [25].In
addition to the notorious effects of neutropenia, monocy-
topenia also contributes to the increased risk of mortality,
bacteremia rate, myelotoxicity, and development of organ
dysfunction, especially in septic patients [6].Intheseptic
panleukopenic cats of the present study, monocytopenia
was possibly due to the relative lack of monocytopoiesis
related to septic insults [26]. In previous studies, it was
reported that the presence of neutropenia, monocyto-
penia, lymphopenia, and leukopenia both at first admis-
sion and during hospitalization were prognostic indicators
of poor outcome for FP [6]. Although the diagnosis of FP is
made by the detection of FP antigen in feces, evaluation of
clinical findings and hematochemical abnormalities is
essential in the early diagnosis of fatal complications asso-
ciated with FP rather than diagnosis [18]. In the ROC ana-
lysis of the hemogram parameters in the present study,
WBC (AUC: 0.967)and granulocyte (AUC: 0.937)values
were found to have excellent diagnostic performance in
detecting the presence of sepsis. As the cytopenias during
sepsis may result from decreased bone marrow production
or increased destruction, evaluation of these parameters
can help both the diagnosis of sepsis/sepsis-related pos-
sible complications and the prediction of prognosis.
Anemia is commonly associated with feline inflam-
matory diseases, and its pathogenesis in cats with sepsis
is complex and multifactorial [13]. It was reported that
anemia occurs in 50% of FP cases and is usually mild due
to the long lifespan of erythrocytes unless there is severe
GI blood loss [2]. Nevertheless, non-regenerative anemia
is a common finding for FP [8]. In the present study, it
was determined that the panleukopenic cats had lower
RBC and Hb levels compared with the healthy cats
(p<0.030). As a result of the comparison based on the
presence of sepsis, MCH levels of the septic panleukopenic
cats were lower than the non-septic ones (p<0.048).
These findings may be associated with the suppression
of bone marrow, immune system, and inflammation due
to opportunistic infections. Other possible mechanisms
causing lower RBC, Hb, and MCH levels are structural
changes of the bone marrow due to cytokines or direct
cytopathic effects of the FPV [27].Gooddiagnosticper-
formance of RBC (AUC: 0.817)value, which was deter-
mined as a result of the ROC analysis, along with the fact
that erythrocytes are very sensitive to sepsis-related
damage [28], may provide an early warning signal of
sepsis and are a factor in the microvascular dysfunction
that has been associated with organ dysfunction. There-
fore, these findings should be evaluated and must be
considered as severe complications that affect the prog-
nosis of FP [16].
Biochemical abnormalities such as azotemia, increased
serum activities of AST or ALT, or hyperbilirubinemia are
typically non-specificincatswithFP[22]. Icterus is rare.
However, hypoalbuminemia, which is considered a nega-
tive prognostic indicator, is the most common abnormality
detected and usually occurs due to decreased protein intake
and increased GI losses. Azotemia can occur from prerenal
causes, such as dehydration [18,27].Itisreasonabletospec-
ulate that frequent feline viral rhinotracheitis/calicivirus/
panleukopenia vaccinations in cats might induce antibo-
dies that bind to kidney tissues, leading to kidney diseases
characterized by azotemia [29]. Nevertheless, it is well
established that the kidney is a commonly affected organ
during sepsis, and its involvement carries a high mortality
risk. The pathophysiology of kidney injury in sepsis is
complex and multi-factorial and includes intrarenal hemo-
dynamic changes, endothelial dysfunction, infiltration of
inflammatory cells in the renal parenchyma, intraglomer-
ular thrombosis, and obstruction of tubules with necrotic
cells and debris [30]. Therefore, elevated BUN and creati-
nine levels (p<0.003)of the panleukopenic cats of the
present study may be associated with hypoperfusion due
to dehydration and anorexia, since all of the cats included
in the study were unvaccinated.
10 Erdem Gülersoy et al.
The liver enzymes such as ALT and AST are sensitive
indicators of liver disease or injury but are not specific
and do not offer any precise indication of liver function-
ality. In cats, even a small increase in ALT is considered
an indicator of liver injury, due to the limited serum half-
life of ALT, and an increase in AST could imply significant
liver injury, due to its mitochondrial localization [31].
During the course of sepsis, the liver contributes actively
to host defense and tissue repair through crosstalk between
hepatic cells and blood cells. Hepatocytes will shift their
metabolic pathway toward upregulation of the inflamma-
tory response, which is responsible for an increase in the
synthesis of acute-phase proteins mediated predominantly
by interleukin 6 [32]. This shift leads to increases in cyto-
kines such as CRP and decreases in albumin. Also, the
metabolic changes and inflammatory response lead to a
decrease in biotransformation liver function, especially a
reduction in cytochrome P450 activity. As the feline liver
is susceptible to disease and has limited conjugation cap-
abilities, in addition to the adhesion of neutrophils to sinu-
soidal endothelial cells, promoting thrombi formation in the
sinusoids and impairing liver microvascular perfusion, lim-
ited protein intake cause and worsen the hepatic injury [33].
For this reason, although the elevated AST, ALT, and total
bilirubin levels (p<0.022)of the panleukopenic cats in the
present study can be associated with hepatic function loss,
FPV-related gastroenteritis causing diarrhoea, dehydration,
malnutrition, and circulatory and metabolic dysfunction
can contribute to the elevation of the aforementioned para-
meters [34].
Decreased albumin levels (p<0.032)of the septic
panleukopenic cats compared with the non-septic pan-
leukopenic cats may be associated with hepatic dysfunc-
tion as well as decreased protein intake and increased GI
losses [27]. In addition, the severity of hypoalbuminemia
in sepsis may increase as a result of downregulated
hepatic production and leak through a damaged endothe-
lial barrier due to FPV-related gastroenteritis [13].There-
fore, assessment of kidney and liver parameters may help
to evaluate the prognosis by providing information about
the severity of pathological changes that increase mor-
tality. It is a well-known fact that critical illness predis-
poses patients to serum phosphate disturbances. Even
though hypophosphatemia may develop as a result of
decreased intake or absorption, increased renal excretion,
hyperphosphatemia occurs as a consequence of renal dys-
function,hemolysis,rhabdomyolysis, or lactic ketoacidosis
[35]. In the present study, the statistically significantly
higher phosphorus levels of non-septic panleukopenic
cats compared with the healthy cats and the numerically
higher phosphorus levels of septic panleukopenic cats
compared with the healthy ones, may be associated with
lactic ketoacidosis due to renal dysfunction and anorexia,
considering the results of the related biochemical para-
meters [27,35].
CRP, a positive acute phase protein (APP), is synthe-
sized primarily in liver hepatocytes and its concentration
increases during inflammatory events [36]. It is an acute
marker for inflammation, and its levels have been shown
to increase in several diseases, including sepsis and viral
and bacterial infections [37]. In studies conducted in
dogs with parvoviral enteritis, it was reported that CRP
level was higher in non-survivor dogs, and higher CRP
level was associated with increased mortality [38,39].In
the present study, elevated CRP levels (p=0.000)of the
panleukopenic cats compared with the healthy cats were
associated with the host’s acute phase response to FPV.
The acute phase response is highly non-specific because
it develops secondary to numerous conditions such as
infection and trauma that can produce tissue injury. In
addition, it was reported that production and response of
APPs vary depending on the species. For example, in the
dog, a strong response occurs with CRP; however, in cats,
significant increases of CRP have not been detected after
an inflammatory stimulus [40]. In line with these data,
the elevated CRP levels of the panleukopenic cats of the
present study and the strong positive correlation with the
qSOFA score (rs: 0.687)can be associated with the fact
that FPV is an important pathogen that strongly stimu-
lates the immune system (considering that the time of
onset of symptoms and admission to hospital of the pre-
sent study is between 1 and 3 days)and causes multiple
organ damage [41]. CRP, which was determined to have a
fair diagnostic performance (AUC: 0.793)in the ROC ana-
lysis, can be used for diagnostic and prognostic purposes
for sepsis in panleukopenic cats, especially in triage,
since its level increases 2 h after the triggering event
and peaks at 48 h [42].
Fundamentally, the host immune response is designed
to localize, confine, and destroy pathogens while repair
mechanisms are activated. Sepsis is a dysregulated form
of this response, and alterations can manifest as endothe-
lial cell damage, coagulopathies, microcirculatory and
hemodynamic alterations, metabolic and neuroendocrine
immune network abnormalities, endoplasmic reticulum
stress, autophagy, and many other pathophysiological
processes leading to vascular leakage and organ failure
[15]. As the incubation period of FPV infection is 2–14
days, exposed cats that are clinically healthy but incu-
bating the infection might not show clinical signs until
days after they have arrived at a shelter or an adoptive
home [43]. For this reason, quick clinical evaluation/
Evaluation of qSOFA and hematochemical profile in cats with FP virus 11
scoring along with routine hematochemical parameters
can help in early diagnosis of possible fatal complications
related to FP. In addition, clinical and laboratory evalua-
tions are even more important in critical feline diseases, as
feline sepsis differs from classic hemodynamic changes
[13]. Although there are studies evaluating the effective-
ness of qSOFA scoring in critically ill dogs [44],nostudy
has been found that evaluated qSOFA score in naturally
developed FP cases, which is an important sepsis model.
In the present study, as a result of qSOFA evaluation, it
was determined that the panleukopenic cats had lower
SBP value (p=0.000), respiratory rate (p=0.000),mental
status (p=0.000), and total qSOFA scores (p=0.000)
compared with the healthy cats. Although the qSOFA score
was observed to be insufficient to distinguish between
septic and non-septic panleukopenic cats, it may have
clinical prognostic value when evaluated together with
serum CRP level [15].
FP has noticeably worse prognosis than CPV enteritis
[29]. Outbreaks can result in high mortality, euthanasia,
and shelter closures. Rapid and accurate diagnosis is
therefore essential, but this remains a challenge due to
a wide variety of clinical findings and false positive test
fecal antigen results after vaccination with MLV for at
least 14 days [10]. In addition, PCR results are obtained
after a waiting period of 1–3 days [17]. For this reason,
further prospective investigations are warranted in cats,
because, in the retrospective feline study, the mortality
rate was high (80%)and cats that died before completion
of the 3-day course of therapy were included in the ana-
lyses [9]. Thus, together with the physical and laboratory
examinations mentioned above, qSOFA evaluation, which
can be performed quickly at the bedside, besides the ICU,
can provide important diagnostic and prognostic informa-
tion for the development of FPV-related complications in
multi-cat households or shelters, and may enable early
treatment interventions.
This study has some limitations. The first is the wide
age range of the cats included in the study (1–11 months),
which can cause variation in clinical findings. The second
is the low number of animals due to the fact that the
panleukopenic cats of the present study consist of the
cats which were admitted to the animal hospital for diag-
nosis/treatment purposes. Therefore, investigating the
aforementioned parameters and correlations in a cat
population with a similar nutritional status and habitat
with a larger number of animals may better demonstrate
the diagnostic and prognostic efficacy of the qSOFA score
together with the hematochemical variables.
Septic cats often present with a very different clinical
manifestation than non-septic dogs. This can make rapid
recognition of the septic cat challenging. Rapid identifi-
cation of these patients and determination of the under-
lying cause are essential for the outcome of these cases.
Initial diagnostics in these cases generally consist of a
hemogram analysis and serum biochemistry profiling.
Although often frustrating, these cases can also be
rewarding. Therefore, it was concluded that although
the qSOFA score evaluation is not sufficient to distin-
guish sepsis in cats, unlike dogs, in order to both protect
the cat population and achieve a positive clinical out-
come, when evaluated together with the aforementioned
hematochemical variables, it may help in making early
diagnosis of complications such as disease-related organ
failure, deciding to initiate appropriate vaccination pro-
grams and isolation protocols in panleukopenic cats.
Acknowledgments: The authors thank to their faculties
and institutes.
Funding information: The authors state no funding
involved.
Author contributions: EG and BBE conceived and designed
this study. EG, BBE, and MO conducted the systematic
literature review. EG and MS conducted the meta-analyses.
EG and MO reported findings from the review and ana-
lyses. EG and BBE drafted the manuscript and all other
authors revised it critically for important intellectual con-
tent. All authors read and approved the final article.
Conflict of interest: The authors state no conflict of
interest.
Data availability statement: All data generated or ana-
lyzed during this study are included in this published
article
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