https://doi.org/10.52973/rcfcv-e34371
Received: 20/12/2023 Accepted: 06/02/2024 Published: 01/05/2024
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Revista Científica, FCV-LUZ / Vol. XXXIV, rcfcv-e34371
ABSTRACT
Periodontal disease, which is dened as inammation of the tissues and
supporting structures surrounding the teeth, can be observed in cats
starting from the age of 2. Periodontal diseases start with Gingivitis,
which is the early stage of periodontal disease. Gingivitis can arise
from inammation of the gums due to plaque, a white or yellowish
biolm of bacteria on the tooth surface, and the toxins produced by
these bacteria. It can also result from inammation of the periodontal
tissues, including dental calculus or other periodontal tissues. A total
of 242 cats were brought to the clinic for surgical diseases and 14 cats
(5.78%) were found to have periodontal diseases. Although there have
been several studies on oxidative stress, there are very few publications
investigating the relationship between oxidative stress and periodontal
diseases in cats. The aim of this study is to measure serum MDA, IMA
and GSH concentrations and SOD and CAT activities in cats with
periodontal diseases and to evaluate the relationship between oxidant
and antioxidant status, which are indicators of oxidative stress. In the
study, blood samples taken from cats with periodontal disease were
centrifuged and serum was removed. MDA and IMA levels of cats with
periodontal disease were found to be signicantly higher than in cats
that recovered after treatment (P<0.001). SOD, CAT and GSH levels were
determined to be signicantly lower cats with periodontal disease than
recovered cats (P<0.001). In conclusion, this study reveals that there is
a relationship between periodontal diseases and oxidant/antioxidant
balance in cats and it shows that the oxidative stress develop due to
the increase of free radicals.
Key words: Cat; dental calculus; Gingivitis; oxidative stress
RESUMEN
La enfermedad periodontal, que se define como la inflamación
de los tejidos y estructuras de soporte que rodean los dientes, se
puede observar en gatos a partir de los 2 años. Las enfermedades
Periodontales comienzan con la Gingivitis, que es la etapa inicial de la
enfermedad Periodontal. La Gingivitis puede surgir de la inamación
de las encías debido a la placa, una biopelícula de bacterias blanca o
amarillenta en la supercie del diente y las toxinas producidas por
estas bacterias. También puede resultar de la inamación de los tejidos
periodontales, incluido el cálculo dental u otros tejidos Periodontales.
Un total de 242 gatos fueron llevados a la clínica por enfermedades
quirúrgicas y se encontró que 14 gatos (5,78 %) tenían enfermedades
Periodontales. Aunque se han realizado varios estudios sobre el
estrés oxidativo, existen muy pocas publicaciones que investiguen la
relación entre el estrés oxidativo y las enfermedades Periodontales
en gatos. El objetivo de este estudio es medir las concentraciones
séricas de MDA, IMA y GSH y las actividades de SOD y CAT en gatos
con enfermedades Periodontales y evaluar la relación entre el estado
oxidante y antioxidante, que son indicadores de estrés oxidativo. En
el estudio, se centrifugaron muestras de sangre tomadas de gatos
con enfermedad periodontaly se eliminó el suero. Se encontró que
los niveles de MDA e IMA de gatos con enfermedad periodonta fueron
signicativamente más altos que en los gatos que se recuperaron
después del tratamiento (P<0,001). Se determinó que los niveles de SOD,
CAT y GSH eran más bajos en gatos con enfermedad periodontalque en
gatos recuperados (P<0,001). En conclusión, este estudio revela que
existe una relación entre las enfermedades Periodontales y el equilibrio
oxidante/antioxidante en gatos y muestra que el estrés oxidativo se
desarrolla debido al aumento de radicales libres.
Palabras clave: Gato; cálculo dental; Gingivitis; estrés oxidativo
Evaluation of the relationship between periodontal diseases and oxidative
stress parameters in cats
Evaluación de la relación entre las enfermedades periodontales
y los parámetros de estrés oxidativo en gatos
İbrahim Yurdakul* , Mehmet Akif Çatak
Sivas Cumhuriyet University, Faculty of Veterinary Medicine, Department of Surgery. Sivas, Turkey.
*Corresponding Author: iyurdakul@cumhuriyet.edu.tr
FIGURE 1. Gingivitis in the upper premolars of case 4, appearance before and after scaling of dental calculus
Periodontal diseases and oxidative stress parameters in cats / Yurdakul and Çatak ________________________________________________
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INTRODUCTION
Periodontal disease, which is dened as inammation of the tissues
and supporting structures surrounding the teeth, can be observed in
cats (Felis catus) starting from the age of 2 old year [1, 2, 3]. Periodontal
disease is a patology of the oral cavity caused by the inammatory
response to bacterial plaques on the tooth surface [1, 2, 3].
Periodontal disease is reported to be the disease that most
frequently causes health problems in cats, with a prevalence of
2.8–24% [4]. Clinical signs of periodontal disease in cats include
anorexia, halitosis, salivation, diculty swallowing, Gingivitis, dental
calculus accumulation, mobile teeth, and tooth loss [5, 6].
Periodontal diseases start with Gingivitis, which is the early stage
of periodontal disease. Gingivitis can arise from inammation of the
gums due to plaque, a white or yellowish biolm of bacteria on the
tooth surface, and the toxins produced by these bacteria. It can also
result from inammation of the periodontal tissues, including dental
calculus or other periodontal tissues [7, 8]. Gingivitis and dental
calculus can cause destruction of teeth and surrounding tissues,
leading to serious periodontal diseases and tooth loss [9].
Active oxygen derivatives of free radicals are called oxidants [10].
In living organism, oxidants and antioxidants are in balance [10]. This
balance is disturbed in favour of oxidants in conditions that prevent the
uptake of antioxidants, such as malabsorption, inammation, infection,
stress and environmental factors, and leads to cellular damage in the
organism, this situation is dened as oxidative stress [11].
Various defence mechanisms have been developed in the organism
to prevent damage to cellular structures by free radicals, more
specically (Reactive Oxygen Species) ROS, These mechanisms are
called antioxidant defence systems [10, 11].
This study aimed to determine the oxidative stress status of dental
calculus and Gingivitis, which cause periodontal diseases in cats.
MATERIAL AND METHODS
Animal material
Between July 2023 and January 2024, a total of 242 cats with
various complaints, different ages, races, and genders were brought
to the Surgical Clinic of the Animal Hospital at Cumhuriyet University
Faculty of Veterinary Medicine in Sivas. The study material consisted
of a total of 14 cats of different weights (3–6 kg, PNR, Istanbul, Turkey),
races and genders, aged between 2–5 years, with complaints of
halitosis, salivation and anorexia, out of 242 cats. Information about
the cat was recorded according to the clinical ndings obtained by
gathering disease occurrence details from the owners of the patients.
Each case was examined in terms of body temperature, pulse and
respiration. In accordance with the anamnesis obtained from the patient
owner, the oral cavity was examined clinically for the presence of halitosis,
plaque, dental calculus and gingival lesions. Detailed examination of the
oral cavity of the cats with halitosis, dental calculus and Gingivitis was
performed after sedation following intramuscular injection of Xylazine
hydrochloride (1.1–2.2 mg·kg
-1
, Alfazyne, Ege Vet, Turkey) and Ketamine
(0.2–0.5 mg·kg
-1
, Alfamine, Ege Vet, Turkey). The cats under sedation
with detected dental calculus underwent dental scaling using a cavitron
device (Hasvet VDU Portable Dental Unit, Shanghai Greeloy Industry Co.,
Ltd., Shanghai, China) to remove the dental calculus (FIGS. 1 and 2). Each
case was classied in terms of detailed calculus and Gingivitis (TABLEI).
Gingivitis cases were treated with oral 0.2% chlorhexidine gluconate
spray (Kloroben 30 mL, Drogsan A.Ş, Ankara, Turkey) at 12 hour intervals
for one week. In the post–treatment controls, it was determined that the
Gingivitis cases were cured.
Collection of blood samples
Pre–post treatment, 2 mL blood samples were taken from the cats'
antebrachial cephalic vein of cats and added to sterile tubes without
anticoagulant. The samples taken were kept at room temperature for
FIGURE 2. Gingivitis in the upper premolars of case 9, appearance before and after scaling of dental calculus
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30 min and then centrifuged at 3000 G·15 min
-1
(Nüve NF 800, Nüve
Laboratory & Sterilization Technology, Turkey), and the resulting
sera were stored at -20°C until analysis (Haier, DW–86L828S, China).
Serum biochemical analysis
The levels of MDA, IMA, GSH, SOD and CAT from the serums obtained
were measured using a biotek ELISA reader (Bio Tek μQuant MQX200
Elisa reader/USA) in accordance with the procedure.
Statistical analysis
Statistical analyses were performed using the 23.0 SPSS package
programme (Statistical Package for Social Sciences, Chicago, IL).
Shapiro Wilk–Smirnov was used to assess the study's numerical data's
distribution. Since the data did not show a normal distribution, they
were analyzed with the Wilcoxone test. For all comparisons, P values
less than 0,05 were considered as signicant (TABLE II).
RESULTS AND DISCUSSION
A total of 242 cats were brought to the clinic for surgical diseases
and 14 cats (5.78%) were found to have periodontal diseases. When
assessed based on races for periodontal disease, it was observed
that the domestic cat breed had 8 cases (57.14%), the British race had
5 cases (35.71%), and the Scottish race had 1 case (7.14%). In terms
of gender, 7 were males (50%) and 7 were females (50%). Regarding
body weight, it was found that Periodontally affected cats weighed
between 3.15 and 6 kg (TABLE I).
TABLE I
Distribution and treatment of cases according to race, age, weight and gender
Case Race
Age
(year)
Gender
Weight
(kg)
Diagnosis Treatment
1 Tekir 2 Female 3.15 Gingivitis Kloroben spray for 7 days
2 Tekir 3 Male 4.00 Gingivitis Kloroben spray for 14 days
3 British 2 Female 4.20 Calculus+ Gingivitis Dental scaling + Kloroben spray 14 days
4 Tekir 4 Male 3.50 Calculus+ Gingivitis Dental scaling + Kloroben spray 14 days
5 Tekir 2 Male 3.50 Gingivitis Kloroben spray for 7 days
6 British 4 Female 4.00 Gingivitis Kloroben spray for 14 days
7 British 2 Male 5.40 Gingivitis Kloroben spray for 7 days
8 Tekir 3 Female 3.50 Calculus+ Gingivitis Dental scaling + Kloroben spray 7 days
9 British 2 Male 3.50 Calculus+ Gingivitis Dental scaling + Kloroben spray 7 days
10 Tekir 4 Female 5.20 Calculus+ Gingivitis Dental scaling + Kloroben spray 14 days
11 Tekir 3 Female 4.30 Calculus+ Gingivitis Dental scaling + Kloroben spray 7 days
12 British 5 Male 6.00 Calculus+ Gingivitis Dental scaling + Kloroben spray 7 days
13 Scottish 4 Male 5.10 Calculus+ Gingivitis Dental scaling + Kloroben spray 7 days
14 Tekir 4 Female 4.20 Calculus+ Gingivitis Dental scaling + Kloroben spray 7 days
!%
!%
%
%
""$ $ !#$"$ $
FIGURE 3. Data are presented as mean and standard deviation. Statistical evaluation
of the data was performed with the Wilcoxon test and P values (***
P<0.001) are
depicted above the bars
Periodontal diseases and oxidative stress parameters in cats / Yurdakul and Çatak ________________________________________________
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In only 5 cases, Gingivitis was identied, while in 9 cases, both
dental calculus and Gingivitis were diagnosed together (FIGS. 1 and2).
Dental calculus was frequently detected in premolar and molar teeth
in the lower and upper jaw. Lesions related to Gingivitis cases were
identiedas hyperaemic areas with smooth borders at the gum margin
of the teeth where the dental calculus was located.
Cases diagnosed with dental calculus and Gingivitis were underwent
cleaned for dental calculus under sedation. For the treatment of
Gingivitis, 0.2% Chlorhexidine gluconate spray (Kloroben 30mL, Drogsan
A.Ş, Ankara, Turkey) was recommended for at 12–hour intervals for one
week. In cases where Gingivitis did not healing during the one–week
follow–up, this duration was extended to two weeks, examinations at
the end of this period revealed that all cases had recovered.
Serum MDA, IMA, CAT, GSH and SOD levels of periodontal disease
cats diagnosed with dental calculus and Gingivitis before and after
treatment are given in TABLE II.
that this situation may be related to the fact that there are many Tekir
(Domestic) cats in this Country and cats with different homeland
such as British and Scottish cats are slowly being adopted in Turkey.
It has been reported that oxidative stress, resulting from the
increase in excessive free radical production that causes cellular
damage in the organism and the weakening of antioxidant defense
as a result of exposure of living beings to various stress factors
such as infection, inammation, and unbalanced nutrition plays an
important role in the pathogenesis of many diseases [13]. Although
there are various studies on oxidative stress, there are very few
publications investigating the relationship between oxidative stress
and periodontal diseases of cats. Therefore, this study was conducted
to measure serum MDA, IMA and GSH concentrations, SOD and
CAT activities and to evaluate oxidative stress status in cats with
periodontal diseases.
When oxidant substances are overproduced in the organism for
any reason, they cause cell damage and cell death by accelerating
the peroxidation of lipids, which are very important for the biological
membrane [10, 11, 13].
MDA, which is an important biochemical marker in determining
the degree of cellular damage in tissues, increases in the presence
of various stress factors such as unbalanced nutrition, inammation
and infection [14, 15]. Wu et al. [16] stated that MDA level will increase
due to oxidative stress in periodontal diseases. In the present study,
serum MDA levels were signicantly (P<0.001) increased in cats with
periodontal disease compared to cats that recovered after treatment.
This increase in MDA levels can be interpreted as an indicator of
excessive free radical production that causes cellular damage in tissues.
Albumin is a plasma protein synthesized primarily in the liver. Many
conditions such as ischemia cause a decrease in the metal ion binding
capacity of albumin and metabolically different protein production
[17, 18]. This change is known as ischemic modied albumin (IMA)
[17]. IMA levels increase due to inammation and reactive oxygen
radicals (ROS) production and are shown as a marker of oxidative
TABLE II
Signicance of Dierences Between Groups that
before and after treatment in cats
Pre treatment Group
(n:14; x̄ ± Sd)
Post treatment Group
(n:14; x̄ ± Sx)
P value
MDA (mmol·mL
-1
) 23,09 ± 0,92
b
13,65 ± 0,29
a
***
IMA (ABSU) 1,51 ± 0,10
b
1,01 ± 0,077
a
***
GSH (mmol·mL
-1
) 1,046 ± 0,05
b
1,83 ± 0,039
a
***
SOD (U·mL
-1
) 30,73 ± 0,53
b
33,34 ± 0,33
a
***
CAT (kU·L
-1
) 60,01 ± 1,22
b
72,81 ± 0,49
a
***
a,b
:Dierent superscripts letters indicate statistically signicant dierences (
***
P< 0.001)
The biochemical analysis revealed that the serum levels of MDA and
IMA in cats diagnosed with periodontal disease signicantly increased
before treatment compared to after treatment (P<0.001) (FIG. 3).
In the study, serum CAT, GSH, and SOD levels were found to be
signicantly lower in cats diagnosed with periodontal disease before
treatment compared to those without the condition (P<0.001) (FIG. 3).
Periodontal disease in cats; It is reported to be the disease that
most frequently causes health problems, with a prevalence rate of
2.8 to 24% from the age of 2 [4]. In the current study, periodontal
disease was diagnosed in 14 of 242 cats in terms of dental calculus
and Gingivitis. According to these data, the prevalence of periodontal
diseases in cats was determined as 5.78%.
It has been reported that the incidence of periodontal diseases is
directly proportional to the aging of the patient and is more common in
premolar and molar teeth [12, 13]. In this study, calculus on premolars
and molars and Gingivitis at the level of these teeth were found in
all of the cases, which supports that periodontal diseases are more
frequently in premolars and molars, and the fact that all of the cats
except one case (no: 12) were between 2–4 years old supports that
periodontal diseases will increase with age.
Among the cats showing periodontal disease according to races,
Tekir (domestic) race (57.4%), British race (35.71%) and nally Scottish
race (7.14%) were the most common. In the present study, the disease
was very common in Tekir (Domestic) races cats (57.4%). It is thought
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stress [17, 18, 19]. Tayman et al. [20] reported that IMA levels increased
in periodontal diseases and IMA levels decreased in healed cases.
In this study, IMA levels in cats with periodontal disease increased
statistically signicantly (P<0.001) compared to recovered cats. This
increase in IMA levels can be interpreted as due to inammation and
the production of reactive oxygen radicals (ROS) that cause cellular
damage in tissues.
Free radicals constantly produced in the cell are destroyed by
antioxidant defense systems produced during normal metabolism in
the body [21]. Antioxidants prevent or delay cell damage by scavenging
free radicals in the cell [21]. Enzyme systems in cells are effective
in the defense system against free radicals in living organisms. SOD
(Superoxide dismutase) and CAT (Catalase) are important enzymatic
antioxidants that prevent the accumulation of free radicals and the
onset of lipid peroxidation in the organism [22].
The rst defense process in the organism against free radicals
occurs with the SOD enzyme and protects the organism from the
harmful effects of oxidants [14]. Shang et al. [23] reported that the
activity of various enzymatic antioxidants such as SOD will decrease
in periodontal diseases. In this study, serum SOD levels were found
to be decreased in cats with periodontal disease.
In this study, serum SOD levels were signicantly (P<0.001) increased
in cats recovered after treatment compared to cats with periodontal
disease before treatment, and this increase in SOD levels can be
interpreted as an increase in SOD levels to compensate for the harmful
effects of excessive free radicals that cause cellular damage in tissues.
Catalase is an enzymatic antioxidant that plays an important role
in the oxidative defense of tissues by catalyzing the reduction of
hydrogen and lipid peroxides in living organisms [24]. Changes in CAT
enzyme activity are considered as an indicator of oxidative stress [25,
26]. Almerich–Silla et al. [27] reported that the activity of enzymatic
antioxidants such as CAT decreased in their study on periodontal
disease. In this study, serum CAT levels were found to be decreased
in cats with periodontal disease.
In this study, a statistically signicant (P<0.001) increase in serum
CAT levels was detected in cats that recovered after treatment
compared to cats with periodontal disease. This increase in serum
CAT levels is thought to be an excessive use of CAT activity as an
antioxidant to reduce the effects of free radicals that increase due
to inammation in periodontal disease.
Glutathione (GSH) is the most important non–enzymatic soluble
antioxidant. GSH is important in protecting the body against oxidative
stress by reducing the toxicity of free radicals in the organism [10, 14,
28] and GSH levels decrease during oxidative stress [28]. Fentoglu et
al. [29] found that GSH levels were lower in patients with Gingivitis and
Periodontitis compared to healthy control group. In this study, serum
GSH levels were signicantly (P<0.001) increased in cats recovered
after treatment compared to cats with periodontal disease before
treatment. This increase in GSH levels can be interpreted as increased
GSH consumption to protect against severe tissue destruction as a
result of increased production of oxidants.
CONCLUSIONS
The results show that oxidative stress and lipid peroxidation develop
in cats with periodontal disease due to increased free radicals. In
addition, it was thought that MDA, IMA, SOD, CAT and GSH activities
may be reliable parameters to determine oxidative stress in cats
with periodontal disease.
As a result, it was concluded that oxidative damage occurs in cats with
periodontal disease and as a result, additional antioxidant administration
to sick cats may contribute to the improvement of the disease.
Ethical statement
This study was approved by the Sivas Cumhuriyet University Animal
Experiments Local Ethics Board.
Conict of interest
The authors declare that they have no conict of interest. Statement
of Animal Rights all applicable international, national, and/or
institutional guidelines for the care and use of animals were followed.
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