1. PÁGINA DE TÍTULO
1.
Título do artigo: INTER-RELAÇÃO DE OBESIDADE VISCERAL,
OBESIDADE GLÚTEO-FEMORAL E DOENÇA PERIODONTAL EM
MULHERES
2.
Autor / Co-autores: Prof. Dra. Dóris Hissako Sumida (Prof. Titular da
Faculdade de Odontologia de Araçatuba-SP – FOA-UNESP); Prof. Dr.
Fernando Shiba (Prof. Colaborador do Programa de Pós Graduação
Multicêntrico em Ciências Fisiológicas – FOA-UNESP).
3.
Angelo César |Fernandes Jacomossi – Médico Endocrinologista – Pósgraduando (mestrado) do
Programa de Pós Graduação Multicêntrico em
Ciências Fisiológicas – FOA-UNESP) – Endereço para correspondência: Rua
Antônio Afonso de Toledo, 874 CEP: 16015-270 Araçatuba-SP –
jacomed@hotmail.com - (18)997112702 / Fone/Fax(18)36223504.
4.
Título abreviado: Inter-relação de Obesidade e Periodontite
5.
Palavras-chave: visceral obesity; gluteofemoral obesity; intra-abdominal fat;
periodontal diseases; periodontitis
6.
Número de palavras: 2911
7. Tipo de Manuscrito: artigo original
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ABSTRACT
Objectives: To evaluate the severity of Periodontal Disease (PD) in obese women
from the same community considering the distribution of body fat. Materials and
Methods: 39 women were evaluated, 15 with visceral obesity (VOb), 10 with
gluteofemoral obesity (GFOb) and 14 with normal weight (C). All were submitted
to periodontal evaluation and scored according to the Community Periodontal
Index (CPI). Anthropometric measurements and bioimpedanciometry were
performed in order to discriminate the regionalization of body fat. A collect of
blood sample was made for fasting dosage of glycemia and insulinemia for
calculation of HOMA-IR determination and laboratory quantification of insulin
resistance. The three groups were compared in relation to the severity of PD.
Correlation analyzes were performed between CPI and the following parameters:
Body Mass Index (BMI), waist circumference (WC), waist / hip circumference
ratio (C / Q), percentage of visceral fat in relation to body weight (% GV) and
HOMA-IR. Results: The mean CPI score was significantly higher (p = 0.0045) in
the ObV group than in the C group. There was no difference in the GFOb group
when compared to the VOb group and the C group. There was a significant
positive correlation between the CPI score (p = 0.0173), C / Q (p = 0.0004), and
WC (p = 0.0082). Conclusion: the present study confirms previous literature data
associating Obesity with PD, suggesting that such association may not occur in all
obese individuals, but especially in those with accumulation of intra-abdominal fat.
INTRODUTION
There are some evidences associating Obesity and Periodontal Disease (PD) (1,2).
The Obesity is characterized by fat body accumulation. The main parameter used
to diagnose in adulthood is Body Mass Index (BMI), calculated by ratio between
the squared height and the weight. Values equal or greater than 30kg/m² is
considered condition diagnoses (3). DP consist in a conditions group affecting the
dental support tissues: the gingiva, periodontal ligament, cementum and alveolar
bone. It represents the result of persistent infection and inflammation in response to
local pathogens (4). Both of them are considered chronic diseases, highly prevalent
that course with systemic, persistent and low-grade inflammation (5,6). Obese
individuals, as well as those affected by PD, show augmented circulating levels of
inflammatory markers. Although the pathophysiological mechanisms responsible
by the Obesity/PD association are not yet clear, it has been postulated a possible
double way characterizing this interrelation. The abnormal fat tissue expanding is
accompanied by increased pro-inflammatory cytokines secretion, notably the
Tumoral Necrosis Factor (TNF-∝) and the Interleukin-6 (IL-6), by adipose cells
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and infiltrates macrophages in the vascular-stroma. These cytokines can also
stimulate the osteoclast cells differentiate through Receptor Activator of Nuclear
Factor kappa-Β ligand (RANKL) expression, increasing the bone reabsorption.
Furthermore TNF-∝ acts recruiting neutrophil polymorphonuclear cells (PMN) and
intensifying the host immune response. Such phenomena contributing to the PD
chronicity and progressivity (7,8). By the other hand the PD also represents an
inflammatory mediators producer source, which can spread systemically and
decrease the cellular response to insulin receptor stimulation, accentuating the
insulin resistance, the cornerstone of the Metabolic Syndrome (MS) diagnosis
(9,10). Although the Obesity, in general, represents an increased risk to
Cardiovascular Diseases (CVD) and others comorbidities, exist a group of fat
people which must not be included in this scenario. Differently of the most of
obese individuals, which show fat accumulation mainly in the intra-abdominal
compartment, these individuals response to weight gain through subcutaneous fat
tissue expansing, specially in the gluteofemoral area. They are individuals that,
although they may have increased BMI, they do not develop CVD or metabolic
complications frequently (11). The most of studies has sought to demonstrate the
relationship between obesity, in general terms, and PD, without consider the
regionalization of the fat deposit (12). In the present study we analyze both obese
women with fat predominance in the intra-abdominal compartment and those with
fat predominance in the gluteofemoral (subcutaneous) compartment regarding the
risk of having PD or the PD severity.
MATERIALS AND METHODS:
A cross-sectional analysis was performed comparing 39 women between the ages
of 20 and 40 years. Twenty-five were obese [Body Mass Index (BMI) ≥ 30 and <40
kg / m²] and fourteen had normal weight (BMI ≥ 18.5 and <25 kg / m²) which
served as control group (C). All were users of the Unified Health System (SUS) of
the municipality of Santo Antônio do Aracanguá-SP, Brazil, being regularly
attended by the family health team and invited to participate in the study. Among
the obese women, 15 had visceral obesity (VOb), according to the resulting value
obtained by the ratio between waist circumference (WC) and hip circumference
(cm) (W/H > 0,85), and 10 carriers of gluteofemoral obesity (GFOb) (W/H ≤ 0.85).
The following exclusion criteria were obeyed: Diabetes mellitus (DM), smoking,
alcoholism, illicit drug use, climacteric or postmenopausal status, plastic surgery in
the hip, abdomen or chest region, oral contraceptive use and chronic inflammatory
diseases. Blood sample for laboratory evaluation was collected within the first
week of the menstrual cycle. All participants signed a free and informed consent
form agreeing to participate in the research. The study was approved by the Ethics
Committee of the Universidade Estadual Paulista - FOA/UNESP (CAAE:
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72005317.5.0000.5420), in accordance with the criteria of Resolution 466 of the
National Health Council on human research. The anthropometric evaluation was
performed with the participants wearing light and barefoot clothing. Obesity was
defined by a BMI (Weight in kilograms divided by the square of the height in
meters) equal to or greater than 30 kg/m² (13). The weight was measured on an
electronic scale (Filizola®), and the height was measured by a portable
stadiometer. The body fat distribution was characterized by W/H ratio, measured
by a tape measure. The WC
measurement was made with the tape positioned
comfortably in the midline, located between the last palpable rib and the apex of
the iliac crest, in the orthostatic position, with the reading being recorded at the end
of the expiration. The hip measurement was performed on the side of the person,
who was standing with arms at the side of the body and feet together, placing the
tape around the buttocks in a horizontal plane, at the level where the glutes reach
their maximum amplitude. Measurements were taken after overnight fasting of at
least eight hours in order to minimize the influence of gastric contents on WC
measurement. Each calibration was repeated twice; when the difference between
them was less than 1 cm, the mean was calculated. If the difference exceeded 1cm,
the measurements were repeated (14). A blood sample was collected after a fasting
period of 8 and 12 hours, and the glucose concentration was determined using
automated technique. Insulinemia was measured by radioimmunoassay - RIA
(Coat-a-Count insulin, Siemens Healthcare Diagnostics, Los Angeles, CA USA).
HOMA-IR (Homeostatic Model Assessment) was calculated by the following
formula: [Fasting Glucose (mmol / L) x Insulin fasting (µU / mL)] / [22.5], with a
normal value lower than 2.71, and served to quantify resistance to insulin (15). The
status of the periodontium was evaluated by the Community Periodontal Index
(CPI) (16). A single examiner conducted the evaluations. The mouth was divided
into sextants and six sites of each of the following teeth were evaluated: 17, 16, 11,
26, 27, 47, 46, 31, 36, 37. The highest code will be registered according to the
following criteria: 0 (healthy), 1 (gingival bleeding after probing), 2 (presence of
sub or supragingival calculus), 3 (periodontal pocket with 4-5 mm) and 4
(periodontal pocket with at least 6 mm). The study participants were classified as:
healthy periodontium (PCI = 0), gingivitis (PCI = 1 or 2) or periodontitis (PCI = 3
or 4). Complementarily, all participants underwent a direct analysis of bioelectrical
impedance (Z), with eight electrodes (tetrapolar) and two different frequencies
(20kHz, 100kHz, InBody®120) in order to obtain a parameter representative of the
amount of intra-abdominal fat (Visceral Fat percentage - VF%) and Total Body Fat
percentage (TF%) (17,18). The normality of the data was verified using the
Shapiro-Wilk test. The PCI, the periodontal condition of the sextants, the HOMAIR index, the age and the BMI were analyzed using the Kruskal-Wallis test,
followed by the Dunn test for multiple comparisons. TF%, VF%, VF% / TF% ratio,
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W/H ratio and WC were analyzed using the Variance Analysis, followed by the
Tukey test for multiple comparisons. The Spearman correlation test was used to
analyze the correlation between the CPI score and the following parameters: BMI,
TF%, VF%, VF% / TF% ratio, HOMA-IR and W/H ratio. The level of significance
was 5%.
RESULTS
No difference was observed in age. The BMI, WC, TF%, VF% and WC were
significantly higher (p <0.05) in the groups GFOb and VOb compared to the
control group (Table 1). There was also no difference in the VF% / TF% ratio
among the groups. The VOb group had a significantly higher WC in relation to the
GFOb group (p<0.05). The W/H ratio was significantly lower (p <0.05) in the
control and GFOb groups when compared to the VOb group, but there was no
difference between control and GFOb group in this parameter. There was no
difference between BMI, TF% and VF% between the GFOb and VOb groups
(Table 1).
Table 1. Age, BMI, TF%, VF%, VF% / TF% ratio, W/H ratio and WC.
Variáveis
Controle
GFOb
VOb
Age (years)
26.43 + 2.66
26.10 + 2.13
28.18 + 2.41
BMI (Kg/m²)
22.04 + 0.47
33.95 + 1.33 *
34.56 + 1.24 *
TF%
33.44 + 1.53
47.57 + 1.29 *
44.81 + 1.40 *
VF%
16.66 + 0.74
22.24 + 0.58 *
22.03 + 0.58 *
VF% / TF%
0.49 + 0.01
0.46 + 0.01
0.49 + 0.01
W/H
0.73 + 0.03
0.79 + 0.01
0.95 + 0.01 *#
WC (cm)
68.64 + 2.20
93.00 + 3.40 *
110.10 + 2.68*#
* p <0.05 compared to the control group; #p <0.05 compared to the GFOb group
The VOb group had a significantly higher HOMA-IR index (p = 0.0002) than the
CG group. No difference was observed in the HOMA-IR index of the GFOb group
in relation to the other groups (Figure 1).
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Figure 1. Evaluation of the HOMA-IR index. Values are presented as average ±
mean standard error. * p <0.05 compared to the control group.
Patients in the VOb group had a significantly lower number (p = 0.0174) of healthy
sextants compared to CG. A significantly higher number (p = 0.0162) of sextants
with gingival bleeding in the ObV group was also observed in relation to the CG.
The GFOb group showed no difference in these variables in relation to the other
groups. There was no difference in the number of sextants with presence of dental
calculus or periodontal pocket between groups (Table 2).
Table 2. Mean number of sextants per patient according to the periodontal status
assessed by the Community Periodontal Index.
Periodontal Condition
Control
GFOb
VOb
Health Gingive
5.00 + 0.36
4.07 + 0.46
3.43 + 0.39 *
Probing Bleeding
0.57 + 0.29
0.79 + 0.28
1.57 + 0.29 *
Dental Calculus
0.43 + 0.20
1.14 + 0.33
0.79 + 0.24
Periodontal Pocket (4-5mm)
0.07 + 0.07
0.07 + 0.07
0.43 + 0.20
*p<0.05 compared to control group; values are shown as average ± mean standard
error
The mean PCI score was significantly higher (p = 0.0045) in the VOb group than
in the control group. There was no difference in the GFOb group when compared
to the other groups (Figure 2).
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Figure 2. Evaluation of the periodontal condition by IPC. Values are presented as
average ± mean standard error. * p <0.05 compared to the control group.
There was a significant positive correlation between the PCI score and the VF% (p
= 0.0300), HOMA-IR (p = 0.0173), W/H (p = 0.0004) and WC (p = 0.0082)
(Table 3).
Table 3. Analysis of the correlation between the CPI score and the BMI,TF%,
vVF%, VF%/TF%, HOMA-IR, W/H and WC.
Spearman
Correlation
Test (r)
p-value
BMI
0.26
0.15
% de total fat
0.22
0.23
% visceral fat
0.39
0.03*
% de total fat / % de visceral fat
0.28
0.13
HOMA-IR
0.43
0.02*
W/H
0.59
0.0004*
WC
0.54
0.01*
Variables
*p<0,05
DISCUSSION
The study showed that obese women, with predominance of intra-abdominal fat,
have a higher PCI score compared to women of normal weight (C). Otherwise, the
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obese women with gluteofemoral fat region did not present a significantly different
score of PCI when compared to VOb women or to the control group.These results
suggest that women afflicted with visceral obesity may have a worse oral health
compared to lean women, belonging to the same age group and with similar living
habits and socioeconomic conditions, since they come from the same community.
Obese women, as a whole (GFOb and VOb), had the anthropometric
measurements, BMI, WC and W/H, and two parameters extracted from
bioimpedance (%TF and %VF), significantly different from those generated from
the group of women with normal weight, demonstrating the greater corporal
adiposity of these women in relation to the lean ones. There was no difference
between the groups when analyzed by the biometric impedance parameter %VF /
%TF ratio, representative of the proportion of visceral fat in relation to the amount
of total body fat. It will be expected that these visceral obese individuals, presented
this parameter increased when compared to individuals with normal weight or their
peers with predominance of subcutaneous fat. However the real bioelectrical
impedance acuracy to determine the amount of the visceral adipose tissue (VAT)
has not yet been well established among different populations and ethnics groups.
Browning and collaborators founded that the bioelectrical impedance analysis
estimates were more highly correlated with total abdominal fat than VAT. (19).
Some studies showed that it analyses better, or equivalently estimates, VAT amount
compared to tape-measured waist circumference (20,21), but other studies found
the opposite (22). Anyway WC is an index of central obesity recommended by the
National Institutes of Health, World Healthy Organization, the American Heart
Association, and the International Diabetes Foundation for screening for risk of
metabolic and cardiovascular disease, due its value as a criterion for visceral obese
definition (23). Large-population, multiethnic studies are needed to demonstrate
whether abdominal bioelectrical impedance analysis is consistently superior to
waist circumference to estimate VAT across populations. The VOb patients showed
a higher HOMA-IR value than lean women, pointing to the presence of insulin
resistance (IR) in women with visceral obesity. HOMA-IR has been used as an
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important laboratory method to identify and quantify IR in several studies because
of its positive and highly significant correlation with the clamp (24), the gold
standard method for IR diagnosis (25). Although no statistically significant
difference was observed between the two subgroups of obese women (VOb versus
GFOb), the mean HOMA-IR value of the GFOb group did not differ from that of
the control group, suggesting that there is a lower magnitude of IR in these women
with subcutaneous obesity. Regarding the periodontal evaluation, we observed that
the VOb patients presented a lower number of sextants with healthy gingiva and a
greater number of sextants with bleeding at the probe. This finding suggests the
existence of a negative influence of the degree of adiposity on periodontal health.
There was also a significant difference between the VOb group and the control
group regarding PCI, corroborating to the greater severity of PD in women with
greater accumulation of fat than in women with normal weight. Likewise, no
statistically significant difference was found between the two subgroups of obese
women regarding this parameter, but the GFOb patients did not show a worse
periodontal condition in relation to the control group and there was a tendency for
PD condition to be less severe in women with GFOb compared to VOb women,
reinforcing the hypothesis that the visceral fat accumulation may be more
negatively associated to PD than the subcutaneous fat accumulation. Excessive
production of inflammatory cytokines by visceral adipocytes, and by immune cells
infiltrated into fatty tissue, may accentuate periodontitis (7,8). On the other hand it
is known that the subcutaneous fat does not constitute a source producing proinflammatory cytokines. In fact, one of its secretory products is adiponectin, a
hormone with anti-inflammatory actions and beneficial metabolic effects (26). The
design of the present study does not allow to establish a causal relationship
between the two diseases, much less if PD could aggravate the obesity and the IR.
However, theoretically, because the inflamed periodontium is also a source of
cytokines, the PD may accentuate the typical alterations of the Metabolic
Syndrome (27), considering that these proinflammatory products reach all organs
through the systemic circulation. TNF-α seems to play a central role in this
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scenario. In addition to reducing the cellular response to insulin, directly limiting
the metabolic effects of this hormone, this cytokine interferes with adipogenesis,
decreasing expression of the transcription factor PPARγ (Peroxisome ProliferatorActivated Receptor Gamma) and protein C/EBPα (CCAAT/enhancer- binding
protein alpha), essential elements for the recruitment of immature adipocytes and
their differentiation into cells capable of storing lipids. The limitation of the storage
capacity of adipose tissue favors the ectopic deposition of fat mainly in the liver,
heart and pancreas, accentuating the metabolic alterations in Visceral Obesity
(28,29,30). Vivekananda and collaborators conducted a study evaluating 60 obese
subjects with a W/H ratio > 0.90 who underwent a weight reduction program, were
able to observe a decrease in serum levels of TNF-α and an increase in adiponectin
levels associated with a concomitant improvement in the clinical PD parameters
(31). Prospectives interventions studies are needed to better clarify the
pathophysiological aspects involved in the two diseases. When all the patients were
analyzed together, the PCI was positively correlated with the percentage of visceral
fat, HOMA-IR, W/H and waist circumference, strengthening the association of PD
with anthropometric and laboratory parameters indicative of accumulation of
visceral fat. There was no significant correlation of PD with BMI. Indeed, this
parameter does not reflect the appropriate size of metabolic burden of fat in our
body. In contrast, WC would mirror the metabolic burden of fat better than BMI
(32), because it is a clinical marker of visceral fat accumulation. Few longitudinal
studies have examined the interrelation of visceral obesity and PD. Three
prospective observational studies found a temporal association between obesity and
the subsequent development of PD. One of these studies considered body fat
distribution rather than BMI as exposure, demonstrating that the 1% increase in W/
H ratio was associated with a 3% increase in the risk of developing periodontal
ligament loss, alveolar bone loss, and probing pocket depth progression throughout
the follow-up (33). Two intervention studies found that the response to noninvasive periodontal treatment was better among lean than obese, whereas three
other studies did not find significant differences (34,35). Nevertheless, such studies
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are heterogeneous, since different definitions and parameters are used by the
authors, as well as periodontal evaluations, as those used to define the distribution
of body fat. These issues are clinically extremely relevant since they deal with two
diseases of high prevalence and socioeconomic impact. Health professionals
should be attentive to this association and approach them concomitantly,
reinforcing the necessity of the multiprofessional work in the evaluation and
treatment of these individuals. In conclusion, the present study reforce previous
data from the literature associating Obesity with PD, suggesting that such
association may not occur in all obese, but mainly in those with accumulation of
intra-abdominal fat.
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