Received: 3 October 2017 | Revised: 20 October 2017 | Accepted: 23 October 2017

DOI: 10.1111/cid.12556

ORIGINAL ARTICLE

Peri-implant parameters and C-reactive protein levels among

patients with different obesity levels

Fahim Vohra BDS, MClinDent, MRDRCS1 | Fahad Alkhudhairy BDS, MS, ABOD2 |
Abdulaziz A. Al-Kheraif PhD3 | Zohaib Akram BDS, MDSc4 | Fawad Javed PhD5

1
Department of Prosthetic Dental Science,
College of Dentistry, King Saud University,
Abstract
Riyadh 11545, Saudi Arabia
Background: It is hypothesized that peri-implant conditions are worse with increasing severity of
2
Department of Restorative Dental Sciences,
obesity, because systemic low-grade inflammatory marker (C-reactive protein [CRP]) is higher in
College of Dentistry, King Saud University,
Riyadh 11545, Saudi Arabia severe form of obese individuals.
3
Dental Health Department, College of Purpose: The aim of the cross-sectional retrospective study was to compare clinical and radio-
Applied Medical Sciences, King Saud
graphic peri-implant inflammatory parameters in patients with different levels of obesity and
University, Riyadh 11545, Saudi Arabia
4
correlate these parameters with CRP levels.
Department of Periodontology, Faculty of
Dentistry, Ziauddin University, Karachi Materials and methods: Eighty-four patients who participated in this study were divided into 4
756000, Pakistan
groups: class I obese (group 1), class II obese (group 2), class III obese (group 3), and nonobese indi-
5
Department of General Dentistry, Eastman
viduals (group 4) were included. Clinical (plaque index [PI], bleeding on probing [BOP], probing
Institute for Oral Health, University of
Rochester, Rochester, New York depth [PD]) and radiographic (marginal bone loss [MBL]) peri-implant parameters were recorded.
Serum CRP were quantified using enzyme-linked immunosorbent assay (ELISA). Clinical peri-
Correspondence implant parameters and serum CRP concentrations were analyzed using 1-way analysis of variance.
Fahim Vohra, Department of Prosthetic
The Pearson correlation coefficient was used to analyze correlations of CRP levels with any of the
Dental Science, College of Dentistry, King
Saud University, Riyadh 11545, Saudi clinical and radiographic parameters assessed.
Arabia.
Results: Peri-implant PI, BOP, PD, and MBL were significantly higher in group-1, -2, and -3
Email: fvohra@ksu.edu.sa
patients as compared to nonobese individuals (P < .05). Peri-implant PI, BOP, PD, and MBL were
Funding information significantly higher in obese patients of group-2 and group-3 as compared to obese patients in
Deanship of Scientific Research, King Saud
group-1 (P < .01). Mean PI, BOP, PD, and MBL were comparable between group-2 and group-3
University, Grant/Award Number:
RGP–1438–028
patients (P > .05). A significant positive correlations were found between CRP levels and BOP
(P 5 .0148) and PD (P 5 .0425); and significant negative correlation was found for MBL in group 3,
respectively (P 5 .0212).

Conclusion: Clinical and radiographic peri-implant inflammatory parameters and serum CRP were
significantly high in patients with severe form of obesity. Serum CRP levels correlated with peri-
implant bleeding in obese patients. These findings are preliminary and long-term controlled trials
are recommended to support these outcomes.

KEYWORDS
alveolar bone loss, bleeding on probing, C-reactive protein, dental implants, obesity

1 | INTRODUCTION 27.5–34.9 kg/m2, 35–39.9 kg/m2, and 40 kg/m2 are categorized as
class I, II, and III obese, respectively.4 It is one of the main causes of
Obesity is defined as increased adipose tissue to a degree in morbidity and mortality in current society and has become a major
which health is impaired and is mainly characterized by systemic public health problem. Recent data reveals that an estimate of 150
1–3
low-grade inflammation. Individuals with a body mass index (BMI) of million individuals suffer from some form of obesity and it is estimated

Clin Implant Dent Relat Res. 2017;1–7. wileyonlinelibrary.com/journal/cid V

C 2017 Wiley Periodicals, Inc. | 1
2 |
that the unexpected plateauing of adult obesity rates may increase up
5
to 300 million by 2025. Concern is growing about the rising preva-
lence of overweight and obesity in adults in Saudi Arabia. An estimated
prevalence of 36% of adults suffer from obesity and it is projected
that 41% in men and escalating rise of 78% in women by 2022,
respectively.6
Evidence suggests that obesity is associated with the build-up
of constant systemic inflammation.7,8 A systemic proinflammatory
state in obesity is suggested for increased alveolar bone loss with
altered immune response because of compromised functional
state of immune cells.9 C-reactive protein (CRP) in particular, is a
marker of systemic inflammation and is associated with obesity
and periodontitis.10 Elevated levels of CRP is characterized by
dysregulated and increased production of several proinflammatory
cytokines that are implicated in the pathogenesis of periodontal
destruction.9,11,12
In the past decade, obesity has been thoroughly investigated as
one of the risk factors for periodontal tissue destruction and associa-
tion between increased adiposity and poor periodontal outcomes is
well elucidated;13–16 In a recent cross-sectional study by Abduljabbar
and colleagues,17 it was concluded that obese individuals showed
increased peri-implant probing depth (PD) and higher amount of mar-
ginal bone loss (MBL) as compared to nonobese individuals. However,
the correlation of peri-implant tissue destruction with the severity of
obesity remains uninvestigated. We hypothesize that peri-implant
inflammatory parameters are compromised with increasing severity of
obesity, because systemic low-grade inflammatory marker (CRP) is
higher in severe form of obese individuals.7–9 Therefore, the aim of the
present cross-sectional retrospective study was to compare clinical and
radiographic peri-implant inflammatory parameters in patients with dif-
ferent levels of obesity and correlate serum CRP levels with clinical and
radiographic peri-implant parameters.
2 | MATERIALS AND METHODS
2.1 | Ethical guidelines
The study was performed following guidelines recognized by the
Declaration of Helsinki as revised in 2013 for experimentation
involving human patients. An information sheet was provided to the
patients that explained the objectives and methods of the present
study and individuals had the right to retire from the study at any stage
without penalty.
2.2 | Study groups
The study analyzed a total of 84 obese and nonobese individuals
recruited from private dental referral clinic (Dr F Alkhudhairy, Saudi
Arabia). These patients were further divided into 4 groups on the basis
of BMI as follows; Group-1: class-I obese individuals with BMI 27.5–
34.9 kg/m2; Group-2: class-II obese individuals with BMI 35–39.9 kg/
m2; Group-3: class-III obese individuals with BMI 40 kg/m2; Group-4:
nonobese individuals with BMI 18.5–22.9 kg/m . 24
VOHRA ET AL.
2.3 | Eligibility criteria
As inclusion criteria, all patients were (1) >30 years of age and; (2)
obese individuals classified according to World Health Organization
(WHO) classification of obesity for Asian cohort which defines BMI
27.5 kg/m2 4; (3) nonobese individuals with a BMI ranging between
18.5 and 22.9 kg/m2 4; and (4) dental implants which has been in
service for 36 months.
Self-reported tobacco smokers, individuals using smokeless
tobacco products,18 habitual alcohol users and patients with systemic
diseases such as acquired immune deficiency syndrome/HIV, renal
disorders, and cardiovascular disorders were excluded.
2.4 | Serum sampling for high-sensitivity CRP and lipid
parameters
Blood samples were collected from the antecubic fossa of the left fore-
arm of each patient in the morning and processed, divided into aliquots
and stored locally at 2808C until final analysis. High-sensitivity CRP
was assessed using an automated immunoanalyzer (IMMULITE; Diag-
nostics Products Corporation, Los Angeles, California). Lipid parameters
were measured in the serum samples including triglycerides, total cho-
lesterol, high-density lipoprotein (HDL), low-density lipoprotein (LDL),
and glucose parameters, including fasting blood glucose levels (FBGL),
insulin, and homeostasis model assessment of insulin resistance
(HOMA-IR). HOMA-IR was calculated as follows: [FBGL (mg/dL)] 3
[fasting serum insulin (mu/mL)]/405 formulate.19 The HOMA-IR
score >2.7 estimates insulin resistance.
2.5 | Clinical peri-implant examination
A trained and calibrated examiner (FA), who was blinded to the
study groups performed the clinical examinations. The overall kappa
value for intra-examiner reliability was 0.91 which was considered a
good agreement. Peri-implant status was based upon recording peri-
implant plaque index (PI), bleeding on probing (BOP), and PD with
references to the Consensus report of the Seventh European Work-
shop on Periodontology-2011.20 All recordings were measured at 6
sites per implant (mesiobuccal, mid-buccal, distobuccal, distolingual/
palatal, mid-lingual/palatal, and mesiolingual/palatal) and presented
as mean percentages per individual. PD was measured to the nearest
millimeter using a manual graded probe (UNC-15 Hu-Friedy,
Chicago, Illinois).
2.6 | Marginal bone loss
All radiographic examinations were performed by a trained and
calibrated investigator (FK) who was blinded to the study groups
(kappa 5 0.83). Digital periapical radiographs were taken and viewed on
a calibrated computer screen (Samsung SyncMaster digital TV monitor,
Korea) using a software program (Image Tool 3.0 Program, Department
of Dental Diagnostic Science, University of Texas Health Science
Center, San Antonio, Texas). MBL was defined as the distance from the
widest supracrestal part of the implant to the alveolar crest.21
VOHRA ET AL.
2.7 | Statistical analyses
Statistical analyses were carried out using a statistical software (SPSS v.
20, IBM, Chicago, Illinois). Data were expressed as means and standard
deviations with percentages and ranges. Normality of distribution of
the variables was tested with Shapiro-Wilk tests and confirmed with
Q–Q plots. Between-group comparison of means was verified with
Kruskal–Wallis test. The Pearson correlation coefficient was used to
analyze for correlations of CRP levels with any of the clinical and
radiographic peri-implant parameters assessed. Stepwise logistic
regression analysis was employed to identify explanatory variables for
peri-implant outcomes, controlling for the effect of possible covariate
such as FBGL, TC, LDL, triglyceride levels, HOMA-IR, and oral hygiene
care. The direction and strength of association between peri-implant
outcomes and covariates were assessed by generating odds ratios, the
precision of which could be measured by 95% confidence intervals.
Differences were considered significant with P < .05.
3 | RESULTS
3.1 | Characteristics of the study groups
In total, 84 individuals were included. Among all the 4 groups, there
were 25 class I obese patients (group 1), 22 class II obese patients
(group 2), 12 class III obese patients (group 3), and 25 nonobese
patients (group 4) as controls (Figure 1). A total of 39 implants in group
1, 35 in group 2, 26 in group 3, and 43 in group 4 were assessed. The
mean duration of implants in the study groups ranged from 42.1 to
78.3 months. The mean age of obese (class I, II, III) and nonobese indi-
viduals was 49.3 years (42–56 years), 51.8 years (40–54 years), 50.4
years (45–59 years), and 52.1 years (39–58 years), respectively. Mean
CRP levels among obese class I, II, and III patients was 3.18 mg/L,
3.34 mg/L, and 3.97 mg/L, respectively. FBGL in obese class I, II, and III
individuals were 104.8 mg/dL, 126.3 mg/dL, and 132.7 mg/dL, respec-
tively, whereas, FGBL in nonobese individuals was 86.1 mg/dL. The
mean BMI of obese and nonobese individuals was 32.2 kg/m2,
2 2 2
38.8 kg/m , 44.3 kg/m , and 21.1 kg/m , respectively. Among patients
FIGURE 1 Flow diagram showing recruitment of study participant
| 3
in groups 1, 2, and 3, the duration of obesity was 6.1 years, 8.7 years,
and 9.3 years, respectively. Metabolic parameters including TC, LDL,
TG, and HOMA-IR showed statistical difference between group 3 and
group 4 subjects (Table 1).
3.2 | Clinical and radiographic peri-implant parameters
The mean scores of peri-implant PI (P < .05), BOP (P < .05), and PD
(P < .05) were significantly higher in group-1, 22, and 23 patients as
compared to nonobese individuals. Peri-implant PI (P < .01), BOP
(P < .01), and PD (P < .01) were significantly higher in obese patients of
group-2 and group-3 as compared to obese patients in group-1. Peri-
implant PI was significantly higher in group-3 and group-4 patients as
compared to group-1 patients (P < .05). Peri-implant BOP and PD were
comparable in obese individuals of group-2 and group-3 (Table 2).
MBL was significantly higher in group-1, group-2, and group-3
patients as compared to nonobese individuals (P < .05). MBL was
significantly higher in group-2 and group-3 patients as compared to
group-1 patients (P < .01). Similarly, there was no significant difference
in MBL between group-2 and group-3 patients (P > .05) (Table 2).
3.3 | Correlation of CRP with clinical and radiographic
peri-implant parameters
Pearson correlation coefficient was calculated to analyze for any corre-
lations among CRP levels and the clinical and radiographic parameters
assessed in all 4 groups (Table 3). When the individual groups were
analyzed, a significant positive correlations were found between CRP
levels and BOP (P 5 .0148) and PD (P 5 .0425); and significant negative
correlation was found for MBL in group 3, respectively (P 5 .0212).
3.4 | Regression analysis to control metabolic
parameters
The logistic regression analysis revealed that peri-implant outcomes
showed statistically significant difference even after adjusting for
FBGL, TC, LDL, HDL, and TRG (P < .05) (Table 4).
4 | VOHRA ET AL.

TA BL E 1 General characteristics of the study groups

Group-1 Group-2 Group-3 Group-4

Characteristics Obese I Obese II Obese III Nonobese

Number of study participants (n) 25 22 12 25

Mean age in years (range) 49.3 (42–56) 51.8 (40–54) 50.4 (45–59) 52.1 (39–58)

Total number of implants 39 35 26 43

Implant position (maxilla/mandible) 22/17 21/14 16/10 21/22

Duration of implants in months (mean 6 SD) 73.4 6 12.6 51.2 6 14.9 42.1 6 21.8 78.3 6 16.5

Brushing frequency (%)

Once daily 85 81 93 77
Twice daily 15 19 7 23

Mean CRP in mg/L (range) 3.18 (2.65–3.34) 3.34 (2.97–3.89) 3.97abc (3.85–4.16) 2.56 (1.77–2.83)

Fasting blood glucose in mg/dL (mean 6 SD) 104.8 6 7.6 c

126.3 6 8.8 ac
132.7 6 8.4 ac
86.1 6 7.2
2
Mean BMI in Kg/m (range) 32.2 (30.9–33.8) 38.8 (36.6–38.9) 44.3 (40.4–47.5) 21.1 (20.9–22.7)

Duration of obesity in years (range) 5.1 (5–7) 8.7a (6–10.7) 9.3a (7–11.4) –

Total cholesterol (mg/dL) 195 6 37 199 6 32 209 6 44c 178 6 28

LDL (mg/dL) 105 6 21 108 6 24 116 6 24c 101 6 22

HDL (mg/dL) 41 6 7 43 6 6 45 6 6 41 6 6

Triglyceride (mg/dL) 156 6 22 165 6 22 178 6 28c 140 6 17

c c c
HOMA-IR 3.8 (0.8–7.3) 5.3 (1.1–9.7) 7.0 (2.2–12.1) 1.1 (0.62–4.9)

Abbreviations: BMI, Body mass index; CRP, C-reactive protein; LDL, low-density lipoprotein; HDL, high-density lipoprotein; HOMA-IR, homeostasis
model assessment of the insulin resistance.
a
Significantly different from group-1 (P < .05).
b
Significantly different from group-2 (P < .05).
c
Significantly different from group-4 (P < .05).

4 | DISCUSSION
To our knowledge from indexed literature, this is the first study to
assess the clinical and radiographic peri-implant parameters among
different levels of obesity and correlate these parameters with the
levels of CRP. The present study was based on the hypotheses that
peri-implant inflammatory parameters (PI, BOP, PD) and radiographic
bone loss (MBL) is compromised in severe obesity forms as compared
to individuals with mild or no obesity. The present result showed that
peri-implant parameters were compromised in obese patients than
nonobese patients, however, class II and class III obese patients
showed similar peri-implant tissue damage. Moreover, there was a sig-
nificant positive correlation between CRP levels and BOP and PD in
class III obese patients.
Obesity has been associated with metabolic disturbances and its
effects on other chronic diseases such as osteoarthritis, cardiovascular
complications, type 2 diabetes mellitus, and cancers are well-docu-
mented.22 It is speculated that obesity increases the risk of periodontal
attachment loss.14,15,23 The pathological mechanisms involved in peri-
implant tissue damage in obesity may be well-explained by similar
mechanisms involved in periodontitis. It is proposed that expansion of
white adipose tissue leads to generalized chronic inflammation by 2

TA BL E 2 Peri-implant clinical and radiographic parameters among patients in group 1, 2, 3, and 4

Group-1 Group-2 Group-3 Group-4

Obese I Obese II Obese III Nonobese
Peri-implant characteristics (n 5 25) (n 5 22) (n 5 12) (n 5 25)

Mean plaque index in % (range) 20.5a (13.1–21.7) 27.8b (18.5–30.9) 28.1b (26.6–34.4) 13.6 (5.2–16.4)

Mean bleeding on probing in % (range) 19.1c (13.4–22.4) 25.4b (16.7–32.5) 27.8b (24.3–32.8) 11.7 (5.1–14.6)

Mean probing depth in mm (range) 2.4c (1.9–2.8) 3.1b (2.7–3.8) 3.6b (2.3–4.1) 1.2 (0.6–2.0)
c b b
Mean marginal bone loss in mm (range) 1.8 (1.9–3.3) 2.6 (2.4–4.5) 2.7 (3.3–5.1) 0.9 (0–2.5)
a
Compared to groups 3 and 4.
b
Compared to groups 1 and 4.
c
Compared to groups 2, 3, and 4.
VOHRA ET AL. | 5

TA BL E 3 Pearson correlation analysis among CRP and PI, BOP, PD, unknown, it is speculated that obesity-associated immune changes in
and MBL periodontal tissues alter the pocket environment and/or host defenses,
Peri-implant inflammatory affecting the subgingival microbial colonization.28 Further studies
parameters Group-1 Group-2 Group-3 Group-4 assessing the microbiological and immune-inflammatory aspect of peri-
PI implant sites in obese patients are recommended to confirm this
hypothesis.
Correlation coefficient .8001 .6713 2.1976 2.5167
Numerous studies have reported a strong association between
P value .9126 .7128 .2462 .0381*
systemic CRP levels and poor periodontal and peri-implant health.29,30
BOP Furthermore, higher levels of CRP are documented in obese patients as
Correlation coefficient .5127 2.3572 .1634 2.3145 compared to nonobese individuals.31 It needs to be stressed that sites
with peri-implantitis are histologically characterized by elevated levels
P value .1728 .5793 .0148* .4810
of proinflammatory cells and cytokines which may further increase the
PD
degree of BOP.32 Our study demonstrated a significant positive associ-
Correlation coefficient .1341 .4559 .1916 2.7669 ation of CRP levels with BOP and PD. This possible association
P value .8725 .3958 .0425* .0412* between CRP levels and BOP may reflect the potential significance of
the local peri-implant inflammatory burden in systemic inflammation
MBL
(obesity).
Correlation coefficient .4201 2.1570 2.5883 2.4492
It has been reported that chronic hyperglycemia is associated with
P value .0177 .3650 .0212* .8264 excessive formation of advanced glycation end products (AGEs) in the
*Significant at P < .05. tissues.33 AGEs are coupled with impaired fibroblastic growth and
increased production of proinflammatory cytokines (including IL-1b
and IL-6).34 Moreover, it is indicated that chronic hyperglycemia
different mechanisms that is over expression of proinflammatory cyto-
weakens the chemotactic and phagocytic function of neutrophils
kines (interleukin [IL]-1b, IL-6, tumor necrosis factor-alpha) into the
(that prevent destruction of bacteria in deep pockets)35; which may be
bloodstream and stimulating macrophages.24,25 Hence, this chronic
a possible justification for enhanced peri-implant tissue damage. It is
inflammation increases the susceptibility of obese patients to infectious
2 noteworthy that in the present study that some obese patients in
challenges by down regulating the immune response. In addition, the
group 2 (class II) and group 3 (class III) were hyperglycemic, therefore it
increased prevalence of periodontal tissue damage in obese individuals
is speculated that the oxidative stress (induced as a result of hypergly-
becomes strong with unhealthy diet.26 It is proposed that diet rich in
cemia) worsened peri-implant inflammation in these patients thereby
high cholesterol and fatty acids may modulate alveolar bone loss
26,27 further compromising clinical (PI, BOP, PD), and radiographic (MBL)
regardless of increased BMI. These immunological and metabolic
parameters of peri-implant inflammation. However, the effect of FBGL
findings may explain the increased susceptibility of patients with
levels on peri-implant inflammation in obese patients were controlled
obesity to peri-implant breakdown.
(through stepwise logistic regression analysis); nevertheless, the effects
The finding of the present study states that the PD levels were
of hyperglycemia cannot be overruled.
higher in group 2 and group 3 patients. In a recent study by Maciel and
Severity of peri-implant inflammation in patients with obesity may
colleagues,28 it was concluded that obese patients with deep PDs
be associated with the attitude toward oral hygiene and duration of
harbored higher levels of periodontopathogenic bacteria as compared
the obesity. The higher percentage of PI among obese patients may be
to nonobese individuals. Although the cause of this association is still
attributed to the neglected attitude toward oral hygiene care.36,37
Furthermore, in the present study, duration of obesity among patients
TA BL E 4 Logistic regression model for covariates influencing peri- in class II (8.7 years) and class III (9.3 years) obese individuals was
implant outcomes with odds ratios, 95% confidence intervals (CI), almost similar and higher than class I (5.1 years) obese individuals. It is
and P values speculated that duration of obesity among patients could have
Covariate Odds ratio 95% CI P value influenced the previously existing peri-implant inflammatory state in
these patients. Moreover, the extrapolation of the changes in the
FBG 2.14 0.78, 5.13 .039
anthropometric values among the test groups was not possible, and
Total cholesterol 2.59 1.18, 4.72 .032
therefore, this may have disfigured the peri-implant outcomes between
LDL 3.72 1.01, 6.11 .075 various studied groups. In addition it is suggested that patients with
Triglyceride 2.29 1.52, 6.88 .017 peri-implant inflammation with a longer history of obesity may be more
susceptible to tissue destruction. Further studies are warranted to test
HOMA-IR 1.74 1.21, 4.1 .002
these hypotheses.
Abbreviations: FBG, fasting blood glucose; LDL, low-density lipoprotein;
There are certain limitations in the present study that should not
HDL, high-density lipoprotein.
Bold denotes statistically significant result at P < .05 in direction of be disregarded. The present study only assessed clinical and radio-
increased risk. graphic peri-implant parameters. Perhaps the sampling of peri-implant
6 |
crevicular fluid for the detection of proinflammatory cytokines may
have resulted in the analysis of site specific destruction around
implants among different levels of obesity. In addition, the cross-
sectional nature of the present study assessed clinical and radiographic
findings at only 1 time point and that longitudinal study may have
helped to analyze the evolution of destruction of soft and hard peri-
implant tissue. Moreover, the unmatched number of study individuals
in group-3 (class III obese) with other study groups may have skewed
the results. With these limitations, patients with severe form of obesity
should be considered as having increased susceptibility toward peri-
implant inflammation. It is recommended that clinicians should educate
and warn obese patients about the biological response around dental
implants and provide frequent oral hygiene screening and maintenance
procedures in patients with increasing severity of obesity (high risk).
5 | CONCLUSION
Within the limits of this cross-sectional retrospective study, it is
concluded that clinical and radiographic peri-implant inflammatory
parameters were significantly high in patients with severe form of
obesity. Serum CRP levels correlated with peri-implant bleeding in
obese patients. These findings are preliminary and long-term controlled
trials are recommended to support these outcomes.
AC KNOW LEDG MENT S
The authors extend their appreciation to the Deanship of Scientific
Research at King Saud University for funding this work through
research group number (RGP–1438–028).
CONFLIC T OF I NTE R ES T
The authors declare that they have no conflict of interests and all
authors have read and approved the final draft.
ORCI D
Zohaib Akram BDS, MDSc http://orcid.org/0000-0001-9618-8818
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How to cite this article: Vohra F, Alkhudhairy F, Al-Kheraif AA,
Akram Z, Javed F. Peri-implant parameters and C-reactive
protein levels among patients with different obesity levels. Clin
Implant Dent Relat Res. 2017;00:1–7. https://doi.org/10.1111/
cid.12556