Received: 16 October 2018 Revised: 24 October 2018 Accepted: 29 October 2018 DOI: 10.1111/cid.12700 ORIGINAL ARTICLE Clinical indices and local levels of inflammatory biomarkers in per-implant health of obese and nonobese individuals Mohammed N. Alasqah MSc, DABP1 | Nouf Al-Shibani MSD,PhD2 | Khulud Abdulrahman Al-Aali CAGS, DScD3 | Osama A. Qutub DScD4 | Tariq Abduljabbar DMSc5 1 Department of Preventive Dental Sciences, College of Dentistry, Prince Sattam Bin Abdulaziz University, Alkharj, Kingdom of Saudi Arabia | Zohaib Akram MDSc6 Abstract Background: Obesity seem to regulate peri-implant health. It is proposed that peri-implant crevicular fluid (PICF) levels of interleukin (IL)-1β and IL-6 are higher in obese as compared to non- 2 Department of Periodontics and Community Dentistry, King Saud University, Riyadh, Saudi Arabia 3 Department of Prosthodontics, College of Dentistry, Princess Nourah Bint Abdulrahman University, Riyadh, Saudi Arabia 4 Oral and Maxillofacial Prosthodontics, Faculty of Dentistry, King Abdulaziz University, Jeddah, Saudi Arabia 5 Department of Prosthetic Dental Science, College of Dentistry, King Saud University, Riyadh, Saudi Arabia 6 Department of Periodontology, Faculty of Dentistry, Ziauddin University, Karachi, Pakistan Correspondence Tariq Abduljabbar, Department of Prosthetic Dental Science, College of Dentistry, King Saud University, Riyadh 11545, Saudi Arabia. Email: tajabbar@ksu.edu.sa Funding information Deanship of Scientific Research, King Saud University, Grant/Award Number: RG1438-075 obese individuals. Objective: The purpose of the present clinico-laboratory study is to estimate and compare the clinical and radiographic indices and PICF levels of IL-1β and IL-6 among obese and nonobese patients. Materials and Methods: Fifty patients were divided into two groups (25 obese with ≥27.5 kg/m2 and 25 nonobese with <27.5 kg/m2 individuals). Clinical indices for both periodontal and periimplant evaluating plaque index (PI), bleeding on probing (BOP), probing depth (PD), clinical attachment level (CAL), and crestal bone loss (CBL) were recorded around teeth and implants. PICF was collected and assessed for the levels of IL-1β and IL-6 using enzyme-linked immunosorbent assay. Results: A significant difference was observed in PI and BOP around natural teeth and implants in obese patients, respectively (P < .05). CBL was found to be significantly higher among obese as compared to nonobese patients (P = .022). Peri-implant and periodontal PD was higher in obese as compared to nonobese but did not reach statistical significance. Levels of IL-1β and IL-6 were statistically significantly higher among obese patients as compared to nonobese (P = .001). Pearson correlation analysis showed IL-1β was positively correlated with CBL (P = .0079), whereas IL-6 showed positive correlation with both BOP (P = .0019) and CBL (P = .015) among obese patients. Conclusions: Clinical peri-implant parameters were worse and proinflammatory biomarkers were significantly higher in obese patients compared with nonobese subjects. The findings of the present study suggests that increased proinflammatory biomarkers in PICF of obese patients may modulate peri-implant inflammation around dental implants. KEYWORDS biomarkers, crestal bone loss, dental implants, obesity 1 | I N T RO D U C T I O N is higher than consumption that subsequently leads to adipose tissue accumulation.4 Obesity is rising globally and has become a serious public health Peri-implantitis is a chronic inflammatory disease which is described dilemma. Epidemiologists have reported that obesity is particularly by the presence of bleeding on probing (BOP) and/or suppuration, deep- escalating in the developing world.1 The explosion of overweight and ened peri-implant sulcus (>4 mm) and crestal bone loss (CBL; ≥2 mm).5,6 obesity in developing world has increased the risk of heart diseases, It is assumed that the risk indicators involved in the pathogenesis of peri- stroke, diabetes mellitus, and certain types of cancers.2,3 This metabolic odontal disease also contribute to peri-implant infections.7 The primary condition occurs because of the altered energy imbalance when intake etiology is the colonization of the oral bacteria to form pathogenic Clin Implant Dent Relat Res. 2018;1–5. wileyonlinelibrary.com/journal/cid © 2018 Wiley Periodicals, Inc. 1 ALASQAH ET AL. 2 biofilm at the implant-abutment interface.8 However, various sys- formulate.18 The HOMA-IR score that exceeded 2.7 projected insulin temic conditions may negatively affect the predictability of dental resistance. implant outcomes leading to peri-implant inflammation, peri-implant bone destruction and, eventually, implant failure and loss.9 Although the association between obesity and periodontal disease has been well understood,10–12 however, recent data have also suggested a possible association between obesity and peri-implant disease. Recent cross-sectional studies that evaluated the levels of proinflammatory biomarkers in saliva and peri-implant crevicular fluid (PICF) reported that patients with obesity are at risk of increased periimplant soft and hard tissue inflammation.13,14 Another study demonstrated that altered inflammatory state in obesity because of high levels of C-reactive proteins in serum is associated with increased bleeding tendency in obese patients with dental implants. 2.3 | Clinical periodontal and peri-implant assessments An expert periodontal examiner (MNA) recorded the values for total periodontal and peri-implant measurements. The kappa scores for the reliability was 0.90 which was deemed an acceptable agreement within the examiner. Periodontal and peri-implant scoring for plaque index (PI) and BOP was based upon dichotomous recording as present = 1 and absent = 0. Probing depth (PD) was assessed with references using the Consensus report of the Eleventh European Workshop on Periodontology-2015.19 Both clinical and peri-implant 15 Several cross-sectional studies have evaluated the severity of peri-implant inflammation and obesity, and to date, no clinical investigation has assessed the levels of proinflammatory cytokines in the PICF in individuals with and without obesity. In order to evaluate the measurements were recorded at six sites (distolingual, mid-lingual, mesiolingual, mesiobuccal, mid-buccal, and distobuccal) around tooth and implant and documented as mean percentages per individual. PD was assessed to the nearest millimeter using a graded periodontal probe (UNC-15 Hu-Friedy, Chicago, IL). pathological mechanism of peri-implant inflammation in patients with increased body weight, there is a need to broaden the knowledge of the possible impact of obesity on the prevalence of peri-implant dis- 2.4 | Standardized digital x-rays eases. Therefore, the purpose of this study is to quantify the local Radiographic data was recorded by an expert and calibrated asses- levels of proinflammatory biomarkers (interleukin-[IL]-6, IL-1β) in sor. Radiographs were taken as described in our previous studies.20 obese and nonobese patients with peri-implantitis, compared to sub- Digital periapical radiographs were studied incorporating in a special- jects without peri-implantitis. ized software (Romexis; images stored at 1:1 ratio) and examined on a calibrated computer display screen with the help of an image ana- 2 | MATERIALS AND METHODS lyzer (Scion Image Analyzer, Scion, Frederick, MD). For data calibration, Scion Image calculated the minimum and maximum pixel values of 16-bit images and was automatically set up on a linear density cal- 2.1 | Participants and ethical procedure ibration function that provided an approximation of the original The current clinico-laboratory study adheres to the principles 16-bit pixel values. CBL was computed from the distance of the described by the Declaration of Helsinki that were revised in 2013 supracrestal part of the implant to the alveolar bone. for research involving human subjects. All participants filled the information sheet that described the details of the research purpose and techniques of the current study. Recruited patients were: >35 years of age; obese patients assessed by measuring BMI and categorized according to World Health Organization classification of Asian obesity16; fasting blood glucose (FBG) that ranged between 75 and 125 mg/dL. Risk factors that may modify periimplant status such as use of smokeless and smoking tobacco,17 alcohol, and patients with chronic systemic diseases such as uncontrolled diabetes mellitus and acquired immune deficiency syndrome were excluded. 2.2 | Serum investigations 2.5 | Collection of PICF and measurement of biomarkers Peri-implant sites were carefully cleaned from supragingival deposits and isolated with sterile gauze and dried using air syringe. PICF samples were collected using standard paper strips (Periopaper, Interstate Drug Exchange, Amityville, NY) inserted 1-2 mm into the peri-implant sulcus space for 30 seconds. Contaminated samples by saliva or blood were not used. Once collected, PICF volume was then measured using a calibrated electronic gingival fluid measuring device (Periotron 8000, Oraflow. Inc, NY). PISF was stored at −80 C until further analysis. A trained laboratory technician blinded to the study groups quantified the levels of IL- Serum lipid analysis that included the evaluation of triglycerides, 1β and IL-6. PICF samples were allowed to centrifuged at 5000 × g total cholesterol, high density lipoprotein, low density lipoprotein, for 15 minutes. Levels of biomarkers were quantified using enzy- and glucose parameters, including fasting blood glucose levels matic immunosorbent assay (ELISA) according to the manufac- (FBGL), insulin, and homeostasis model assessment of insulin resis- turer's recommendations (Quantikine, R&D Systems, Minneapolis, tance (HOMA-IR) were measured from the serum samples of both the MN) and calculated as picograms per milliliters (pg/mL), respec- groups. HOMA-IR was estimated using the following mathematical tively. Final results were plotted using standard curves created equation: [FBGL (mg/dL)] × [fasting serum insulin (mu/mL)]/405 prior from each assay. ALASQAH ET AL. 3 Baseline clinical periodontal and peri-implant parameters among obese and nonobese patients 2.6 | Statistical proposal and analysis TABLE 2 Normal distribution of the dependent variables was computed using Shapiro-Wilk tests. Significance of comparisons between groups of means was tested using two-sample t-test. Bonferroni post hoc adjustment was tested for multiple comparisons. Pearson correlation analysis was carried out for correlation between biomarker levels and clinical peri-implant indices by evaluating the correlation coefficient. P value less than .05 was regarded as significant. Clinical parameters Obese Nonobese P value Periodontal parameters Plaque index (%) 57.2  9.2 41.4  7.9 .032 Bleeding on probing (%) 56.4  9.1 37.6  8.4 .041 Probing depth (mm) 3.7  1.4 3.2  1.2 NS Clinical attachment level (mm) 3.3  1.0 3.0  1.0 NS Peri-implant parameters 3 | RESULTS Twenty-five number of obese (13 males and 12 females) and nonob- Plaque index (%) 34.7  10.8 17.1  5.2 .013 Bleeding on probing (%) 29.3  11.5 13.7  3.6 .017 Probing depth (mm) 2.6  0.18 2.3  0.21 NS Crestal bone loss (mm) 1.9  0.1 0.7  0.3 .022 ese (14 males and 11 females) patients were included and divided in two groups, respectively. The mean age of obese individuals was 61 years whereas the mean age of nonobese individuals was showed statistical significance among both groups in which mean PI 59 years. Forty-three dentals implants were evaluated in obese and BOP was recorded as 57.2% and 56.4% in obese patients, patients, whereas a total of 39 dental implants were examined in whereas 41.4% and 37.6% was measured in nonobese group, respec- nonobese patients. Implants in service averaged 5.7 years in obese tively. Periodontal PD was calculated as 3.7 mm in obese, whereas and 6.1 years in nonobese patients. FBGL estimated for obese and healthy patients showed 3.2 mm. Evaluation of clinical attachment nonobese patients were 122.4 mg/dL and 98.2 mg/dL, respectively. level (CAL) in obese and nonobese was recorded as 3.3 mm and 2 Body mass index for obese was recorded 36.8 kg/m and for nonob- 3.0 mm, respectively. ese 23.6 kg/m . Serum metabolic parameters of obese individuals For peri-implant indices, obese group showed statistically signifi- including total cholesterol, low density lipoprotein, triglycerides, and cantly higher values of PI, BOP, and CBL than nonobese individuals. PI HOMA-IR were significantly high from nonobese subjects. Mean and BOP was recorded as 34.7% (P = .013) and 29.3% (P = .017) in duration of obesity reported by obese cohort was 11.3 years. Almost obese patients, whereas 17.1% and 13.7% was measured in nonobese 26% and 59% of test and control patients reported twice brushing, group, respectively. CBL also showed higher values for obese patients respectively (Table 1). as compared to nonobese patients (P = .022; Table 2). 2 Clinical indices including periodontal and peri-implant recordings PICF volume and levels of IL-1β ad IL-6 were found to be higher are presented in Table 2. Only PI (P = .032) and BOP (P = .041) in obese patients than nonobese (Table 3). Pearson correlation analysis revealed IL-1β was positively correlated with CBL (P = .0079), TABLE 1 whereas IL-6 showed positive correlation with both BOP (P = .0019) Baseline parameters of the study groups Parameters Number of study participants (n) Obese Nonobese and CBL (P = .015) among obese patients (Table 4). P value 25 25 NS Sex (M/F) 13/12 14/11 NS Mean age in years 61  9.9 59  9.2 NS Although recent data has investigated about peri-implant health 39 NS among patients with obesity,14,21 little is known about proinflamma- NS tory biomarker levels that may help researchers to extrapolate the Number of implants 4 | DI SCU SSION 43 Implants in service (y) 5.7  1.1 6.1  2.5 Fasting blood glucose (mg/dL) 122.4  8.5 98.2  9.4 .001 BMI in kg/m2 (range) 36.8 (31.9-41.7) 23.6 (20.9-22.7) .001 Total cholesterol (mg/dL) 196  34 173  30 .015 the biomolecular level. The findings of the current study revealed that LDL (mg/dL) 108  22 92  21 .043 peri-implant indices including PI, BOP, CBL, and proinflammatory bio- HDL (mg/dL) 44  7 41  5 NS markers were significantly higher in obese patients compared with 167  25 133  17 .012 nonobese subjects. HOMA-IR 3.8 (0.9-7.4) 1.3 (0.48-4.8) .001 Obesity duration (y) 11.3  6.8 NA NA .048 Triglyceride (mg/dL) 74 41 Twice daily 26 59 inflammation. This study aimed to quantify the levels of biomarkers and elucidate the association of obesity and peri-implant health on Brushing frequency (%) Once daily pathological role of overweight, such as obesity, in peri-implant Abbreviation: BMI, body mass index; HDL, high-density lipoprotein; HOMA-IR, homeostasis model assessment of the insulin resistance; LDL, low-density lipoprotein; NA, not applicable; NS, not significant. Peri-implant crevicular fluid volume and biomarker levels among obese and nonobese patients TABLE 3 Parameters Obese Nonobese P value Volume of PICF (μl) 3.1  0.8 2.0  0.5 .01 IL-1β (pg/mL) 284.82  27.8 158.73  23.9 .001 IL-6 (pg/mL) 2697.5  101.6 1359.7  88.4 .001 ALASQAH ET AL. 4 Pearson correlation analysis among biomarkers and peri-implant parameters fat percentage were positively associated with clinical parameters TABLE 4 Parameters Obese such as BOP and plaque scores. This is also explained by the increased Nonobese ence and these pockets cannot be considered pathological as the PI Correlation coefficient 0.0837 P value −0.6212 .0196a .7524 scores were < 4 mm. It is suggested that overweight patients with higher and deep PD harbor enhanced percentage levels of bacteria causing periodontal diseases.28 Although the direct cause-effect of BOP Correlation coefficient −0.3977 −0.1285 this link needs validation, it is contemplated that obesity-associated .1532 .5581 immune changes in peri-implant structures may alter the pocket envi- 0.1931 −0.1682 niche around dental implants. Future studies should be undertaken in .4721 .6912 order to prove the microbiological/immune-inflammatory process of 0.4554 −0.1292 In chronic hyperglycemia, numerous proteins undergo a nonenzy- .9549 matic glycosylation, resulting in accumulated glycation end products P value ronment and/or host defenses, affecting the subgingival bacterial PD Correlation coefficient P value CBL peri-implant probing sites in obese patients. Correlation coefficient .0079a P value IL-6 (AGEs). There is ample data that indicates chronic hyperglycemic state PI is associated with excess formation of AGEs which are responsible for Correlation coefficient 0.3349 0.0526 periodontal and peri-implant tissue destruction.29,30 These proteins .7845 .8599 surmount impaired fibroblastic growth and causes considerable 0.3941 0.1181 tory cytokines including IL-6 and IL-1β.31 Moreover, it is suggested .6192 that chronic hyperglycemia impairs the chemotactic and phagocytic P value BOP increase in the formation and expression of destructive proinflamma- Correlation coefficient P value .0019 a PD function of neutrophils (which prevent destruction of bacteria in peri- Correlation coefficient 0.0157 −0.0933 odontal pockets), thereby increasing tissue destruction.32 It is noted .8485 .7823 that in the current study, mean FBGL among obese patients was 0.3342 0.1438 that the increased levels of proinflammatory cytokines and increased .5991 amount of peri-implant destruction may be partly explained by the P value CBL 122.4 mg/dL which indicates prediabetes. Therefore, it is supposed Correlation coefficient .0155a P value a PD in obese patients. Although PD in obese group was higher as compared to nonobese, these differences did not show statistical differ- IL-1β AGEs and partly by the oxidative stress (induced as a result of Significant at P < .05. hyperglycemia).33,34 The probable pathological mechanism that modulates peri- The robust element of the current study lies in its evaluation of implant health around dental implants in overweight individuals can the two biomarker levels which are considered proinflammatory and be clarified by the increased systemic inflammatory burden in obe- destructive in nature and are implicated in causing hard and soft tissue 17,18 Obesity is associated with increased amount of body fat. The inflammation around the dental implants. In this way, the current adipocyte cells are responsible for the amplified levels of proinflam- study pushes the association of obesity and how it modulates peri- matory cytokines that are released from the cells itself and macro- implant tissue inflammation into a new direction. This allows us to sity. 22 phages that are relatively increased in obesity. It is note-worthy that CBL was found to be significantly higher among obese patients as extrapolate the assessment of an important risk factor such as obesity and overweight that may cause dental implant failure. compared to nonobese. It is proved by the recent experimental study by Fujita and Maki that obese mice fed with high amounts of fat can lead to increase alveolar bone loss.23 Interestingly, PICF levels of IL-1β were found raised in obese patients. Research suggests that IL-1β is a 5 | CONC LU SION Clinical peri-implant parameters were worse and proinflammatory well-known biomarker for alveolar bone destruction.24,25 These biomarkers were significantly higher in obese patients compared hypotheses could explain the plausible associations of increased bone with nonobese subjects. The finding of the present study suggests loss around dental implants in obesity. that increased proinflammatory biomarkers in PICF of obese Worthy-of-note, scores of clinical peri-implant and periodontal indices including PI and BOP were higher in obese patients than non- patients may modulate peri-implant inflammation around dental implants. obese. This is indicated by the neglected attitudes of oral hygiene measures by obese individuals. Our data indicates that only 26% of obese subjects brush twice daily. A study by Franchini et al.26 pro- ACKNOWLEDGMENT posed that obese adults showed irregular patterns of toothbrushing The authors extend their appreciation to the Deanship of Scientific behavior. Moreover, a recent meta-analysis by Khan et al. 27 revealed that obesity indicators including BMI, waist circumference and body Research at King Saud University, Riyadh, Saudi Arabia for funding this work through Research Group # RG-1438-075. ALASQAH ET AL. 5 CONF LICT OF IN TE RE ST The authors declare that they have no conflict of interests. ORCID Tariq Abduljabbar Zohaib Akram https://orcid.org/0000-0001-7266-5886 https://orcid.org/0000-0001-9618-8818 RE FE R ENC E S 1. WHO. WHO overweight and obesity fact sheet No311. 2006; Available at: http://www.who.int/mediacentre/factsheets/fs311/en/index.html#. 2. GBD 2015 Obesity Collaborators. Health effects of overweight and obesity in 195 countries over 25 years. N Engl J Med. 2017;377:13-27. 3. Dankel SJ, Loenneke JP, Loprinzi PD. Health outcomes in relation to physical activity status, overweight/obesity, and history of overweight/obesity: a review of the WATCH paradigm. Sports Med. 2017; 47:1029-1034. 4. Bray G. The Metabolic Syndrome and Obesity. Totowa, NJ: Humana Press Inc; 2007. 5. Lang NP, Berglundh T. Peri-implant diseases: where are we now? Consensus of the seventh European workshop on periodontology. J Clin Periodontol. 2011;38:178-181. 6. Sanz M, Chapple IL. Clinical research on peri-implant diseases: consensus report of Working Group 4. J Clin Periodontol. 2012;39:202-220. 7. Heitz-Mayfield LJ. Peri-implant diseases: diagnosis and risk indicators. J Clin Periodontol. 2008;35:292-304. 8. Grischke J, Eberhard J, Stiesch M. Antimicrobial dental implant functionalization strategies—a systematic review. Dent Mater J. 2016;35: 545-558. 9. Turri A, Orlato Rossetti PH, Canullo L, Grusovin MG, Dahlin C. Prevalence of peri-implantitis in medically compromised patients and smokers: a systematic review. Int J Oral Maxillofac Implants. 2016;31:111-118. 10. Akram Z, Abduljabbar T, Abu Hassan MI, Javed F, Vohra F. Cytokine profile in chronic periodontitis patients with and without obesity: a systematic review and meta-analysis. Dis Markers. 2016;2016:1-12. https://doi.org/10.1155/2016/4801418. 11. Vohra F, Akram Z, Bukhari IA, Sheikh SA, Riny A, Javed F. Comparison of periodontal inflammatory parameters and whole salivary cytokine profile among Saudi patients with different obesity levels. Int J Periodontics Restorative Dent. 2018;38:e119-e126. 12. Akram Z, Safii SH, Vaithilingam RD, Baharuddin NA, Javed F, Vohra F. Efficacy of non-surgical periodontal therapy in the management of chronic periodontitis among obese and non-obese patients: a systematic review and meta-analysis. Clin Oral Investig. 2016;20:903-914. 13. Abduljabbar T, Al-Sahaly F, Kellesarian SV, et al. Comparison of periimplant clinical and radiographic inflammatory parameters and whole salivary destructive inflammatory cytokine profile among obese and non-obese men. Cytokine. 2016;88:51-56. 14. Elangovan S, Brogden KA, Dawson DV, et al. Body fat indices and biomarkers of inflammation: a cross-sectional study with implications for obesity and peri-implant oral health. Int J Oral Maxillofac Implants. 2014;29:1429-1434. 15. 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. 2018;20:130-136. 16. Barba C, Cavalli-Sforza T, Cutter J, Darnton-Hill I. Appropriate bodymass index for Asian populations and its implications for policy and intervention strategies. Lancet. 2004;363:157-163. 17. Akram Z, Vohra F, Bukhari IA, Sheikh SA, Javed F. Clinical and radiographic peri-implant parameters and proinflammatory cytokine levels among cigarette smokers, smokeless tobacco users, and nontobacco users. Clin Implant Dent Relat Res. 2018;20:76-81. 18. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412-419. 19. Tonetti MS, Chapple IL, Jepsen S, Sanz M. Primary and secondary prevention of periodontal and peri-implant diseases: introduction to, and objectives of the 11th European workshop on periodontology consensus conference. J Clin Periodontol. 2015;42:S1-S4. 20. AlQahtani MA, Alayad AS, Alshihri A, Correa FO, Akram Z. Clinical peri-implant parameters and inflammatory cytokine profile among smokers of cigarette, e-cigarette, and waterpipe. Clin Implant Dent Relat Res. 2018. https://doi.org/10.1111/cid.12664. 21. Alkhudhairy F, Vohra F, Al-Kheraif AA, Akram Z. Comparison of clinical and radiographic peri-implant parameters among obese and non-obese patients: a 5-year study. Clin Implant Dent Relat Res. 2018;20:756-762. 22. Trayhurn P, Wood IS. Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr. 2004;92:347-355. 23. Fujita Y, Maki K. High-fat diet-induced obesity triggers alveolar bone loss and spontaneous periodontal disease in growing mice. BMC Obes. 2015;3(1):1. 24. Graves D. Cytokines that promote periodontal tissue destruction. J Periodontol. 2008;79:1585-1591. 25. Graves DT, Cochran D. The contribution of interleukin-1 and tumor necrosis factor to periodontal tissue destruction. J Periodontol. 2003; 74:391-401. 26. Franchini R, Petri A, Migliario M, Rimondini L. Poor oral hygiene and gingivitis are associated with obesity and overweight status in paediatric subjects. J Clin Periodontol. 2011;38:1021-1028. 27. Khan S, Barrington G, Bettiol S, Barnett T, Crocombe L. Is overweight/obesity a risk factor for periodontitis in young adults and adolescents?: a systematic review. Obes Rev. 2018;19:852-883. 28. Maciel SS, Feres M, Gonçalves TE, et al. Does obesity influence the subgingival microbiota composition in periodontal health and disease? J Clin Periodontol. 2016;43:1003-1012. 29. Schmidt AM, Weidman E, Lalla E, et al. Advanced glycation endproducts (AGEs) induce oxidant stress in the gingiva: a potential mechanism underlying accelerated periodontal disease associated with diabetes. J Periodontal Res. 1996;31:508-515. 30. Al-Sowygh ZH, Ghani SM, Sergis K, Vohra F, Akram Z. Peri-implant conditions and levels of advanced glycation end products among patients with different glycemic control. Clin Implant Dent Relat Res. 2018;20:345-351. 31. McManus LM, Bloodworth RC, Prihoda TJ, Blodgett JL, Pinckard RN. Agonist-dependent failure of neutrophil function in diabetes correlates with extent of hyperglycemia. J Leukoc Biol. 2001;70:395-404. 32. Manouchehr-Pour M, Spagnuolo PJ, Rodman HM, Bissada NF. Comparison of neutrophil chemotactic response in diabetic patients with mild and severe periodontal disease. J Periodontol. 1981;52:410-415. 33. Alasqah M, Mokeem S, Alrahlah A, et al. Periodontal parameters in prediabetes, type 2 diabetes mellitus, and non-diabetic patients. Braz Oral Res. 2018;32:e81. 34. Abduljabbar T, Al-sahaly F, Al-kathami M, Afzal S, Vohra F. Comparison of periodontal and peri-implant inflammatory parameters among patients with prediabetes, type 2 diabetes mellitus and non-diabetic controls. Acta Odontol Scand. 2017;75:319-324. How to cite this article: Alasqah MN, Al-Shibani N, Al-Aali KA, Qutub OA, Abduljabbar T, Akram Z. Clinical indices and local levels of inflammatory biomarkers in per-implant health of obese and nonobese individuals. Clin Implant Dent Relat Res. 2018;1–5. https://doi.org/10.1111/cid.12700