Systematic Review Dental Implants Int. J. Oral Maxillofac. Surg. 2018; 47: 1336–1342 https://doi.org/10.1016/j.ijom.2018.02.010, available online at https://www.sciencedirect.com Survival of dental implants placed in HIV-positive patients: a systematic review C. A. A. Lemos, F. R. Verri, R. S. Cruz, J. F. Santiago Júnior, L. P. Faverani, E. P. Pellizzer: Survival of dental implants placed in HIV-positive patients: a systematic review. Int. J. Oral Maxillofac. Surg. 2018; 47: 1336–1342. ã 2018 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. No consensus has been reached on the use of dental implants in human immunodeficiency virus (HIV)-positive patients. This systematic review evaluated dental implants in HIV-positive patients in terms of implant survival and success rates, marginal bone loss, and complications. The review was conducted according to the PRISMA checklist. Two independent reviewers performed a comprehensive search of the PubMed/MEDLINE, Scopus, and Cochrane Library databases for studies published until October 2017. Six studies were selected for review. In total, 821 implants were placed: 493 in 169 HIV-positive patients, and 328 in 135 HIV- negative patients. The mean duration of follow-up was 47.9 months. Weighted mean survival rate, success rate, and marginal bone loss values were calculated for the HIV-positive patients. Mean survival and success rates at the patient level (according to the number of patients) were 94.76% and 93.81%, respectively; when calculated at the implant level (according to the number of implants), these rates were 94.53% and 90.37%, respectively. Mean marginal bone loss was 0.83 mm at the patient level and 0.99 mm at the implant level. Thus, dental implants are suitable for the rehabilitation of HIV-positive patients with controlled risk factors and normal CD4+ cell counts. 0901-5027/01001336 + 07 ã 2018 International Association of Oral and Maxillofacial Surge C. A. A. Lemos1, F. R. Verri1, R. S. Cruz1, J. F. Santiago Júnior2, L. P. Faverani3, E. P. Pellizzer1 1Department of Dental Materials and Prosthodontics, São Paulo State University (UNESP), Araçatuba Dental School, Araçatuba, Brazil; 2Department of Health Sciences, University of Sacred Heart – USC, Bauru, Brazil; 3Department of Surgery and Integrated Clinic, São Paulo State University (UNESP), Araçatuba Dental School, Araçatuba, Brazil Key words: dental implant; human immunode- ficiency virus; complications; success; marginal bone loss; systematic review. Accepted for publication 23 February 2018 Available online 16 March 2018 Dental implants are considered a favour- able treatment option for the rehabilitation of patients who present partial or total edentulism, as survival and success rates are high1. However, treatment longevity can be reduced in patients with a compro- mised medical status or systemic condi- tions2. In addition, the effects of general health problems on implant failure rates are still poorly documented2, especially in human immunodeficiency virus (HIV)- positive patients3. Infection with HIV may lead to the development of acquired immunodefi- ciency syndrome (AIDS), which is associ- ated with increased morbidity and mortality rates4. The virus attacks the immune system, especially CD4+ T-cells, and causes a reduction in host resistance to different pathogens5,6. Furthermore, some studies have linked the presence of HIV/ AIDS to an increased risk of complica- tions from oral surgical procedures6,7. Such an increased risk of complications may compromise implant survival and contribute to failures8,9. However, as a result of the introduction of highly active ons. Published by Elsevier Ltd. All rights reserved. https://doi.org/10.1016/j.ijom.2018.02.010 https://doi.org/10.1016/j.ijom.2018.02.010 Survival of implants placed in HIV-positive patients 1337 antiretroviral therapy (HAART), HIV/ AIDS is becoming a chronic disease, and the life expectancy of patients with HIV/AIDS has increased due to an in- crease in their immunological resis- tance6,10. As a result, more HIV-positive patients are likely to seek dental treatment, including dental implants, for oral reha- bilitation. No consensus has been reached con- cerning the risks associated with dental implant placement in HIV-positive patients. This systematic review was per- formed to evaluate the clinical perfor- mance of implants placed in HIV- positive patients. The null hypotheses were as follows: (1) the survival rate of implants in HIV-positive patients is simi- lar to that in HIV-negative patients; (2) marginal bone loss and complications in HIV-positive patients are similar to those in HIV-negative patients. Materials and methods Registry protocol This systematic review was performed according to the Preferred Reporting Items for Systematic Reviews and Meta-Analy- ses (PRISMA) checklist11 and in accor- dance with models proposed in the literature12–14. Furthermore, the methods used in this systematic review have been registered in the International Prospective Register of Systematic Reviews (PROS- PERO; CRD42017059318). Eligibility criteria The focused question addressed was ‘‘Are dental implants placed in HIV-positive patients at increased risk of implant failure, marginal bone loss, and complications?’’ The primary outcome evaluated was the implant survival rate, and secondary out- comes were the implant success rate, mar- ginal bone loss, and complication rate. Study types eligible for inclusion were randomized controlled trials (RCTs), pro- spective studies, and retrospective studies (retrospective studies were included be- cause of the limited number of RCTs and prospective studies available). All studies reported the survival rates of implants in HIV-positive patients and were published in English. In vitro studies, animal studies, case series, case reports, and reviews were excluded. Information sources and search Two independent authors (C.A.A.L. and R.S.C.) conducted an electronic search of the PubMed/MEDLINE, Scopus, and Cochrane Library databases for articles published up until October 2017. The key words used were: (HIV [MeSH Terms] and Dental implants [MeSH Terms]) OR (Human Immunodeficiency Virus [All Fields] and Dental implants [MeSH Terms]) OR (AIDS [All Fields] and dental implants [MeSH Terms]) OR (Acquired Immunodeficiency Syndrome [MeSH Terms] and dental implant [MeSH Terms]). The same researchers performed a manual search of the following journals: Clinical Implant Dentistry and Related Research, Clinical Oral Implants Re- search, Implant Dentistry, International Journal of Oral and Maxillofacial Implants, International Journal of Oral and Maxillofacial Surgery, Journal of Clinical Periodontology, Journal of Den- tistry, Journal of Oral and Maxillofacial Surgery, Journal of Oral Implantology, Journal of Oral Rehabilitation, Journal of Periodontology, and Periodontology 2000. In addition, OpenGrey (http:// www.opengrey.eu) was used to search the grey literature. Data collection process One author (C.A.A.L.) collected relevant information from the articles and a second author (L.P.F) checked all of the informa- tion collected. A careful analysis was per- formed to check for disagreements among the authors. Any such disagreements were resolved through discussion with a third author (J.F.S.J) until a consensus was reached. Risk of bias Two investigators (C.A.A.L. and F.R.V.) assessed the methodological quality of the studies using the Newcastle–Ottawa scale (NOS) for cohort studies, which is based on three major components: selection, comparability, and outcome. According to the NOS, a maximum of nine stars can be given to a study, which represents the highest quality. A score of five or fewer stars indicates a high risk of bias, while a score of six or more stars indicates a low risk of bias15. Additional analyses The kappa statistic (k) was used to deter- mine inter-reader agreement during the article selection process in the database search. Weighted mean values for margin- al bone loss, survival rate, and success rate were calculated using Microsoft Excel (Microsoft Corp., Redmond, WA, USA). Results Study selection The database search retrieved 360 articles: 143 from PubMed/MEDLINE, 145 from Scopus, 57 from the Cochrane Library, and 15 from other sources (hand-search and grey literature). After reading the titles and abstracts against the eligibility crite- ria, eight articles remained. Two articles were excluded after full-text reading: one reported a duplicate sample of patients and data from another included article16, and one was an editorial article17. Ultimately, six articles reporting four observational studies3,8,9,18 and two retrospective stud- ies19,20 were included in this systematic review (Fig. 1). Three of the studies only evaluated HIV-positive patients8,9,20, and three compared HIV-positive and HIV- negative patients3,18,19. The inter-investigator agreement for articles selected from PubMed/MEDLINE (k = 1.0), Scopus (k = 0.81), and the Cochrane Library (k = 1.0) indicated a high level of agreement21. Study characteristics A total of 821 implants were placed in 304 patients: 493 implants in 169 HIV-positive patients, and 328 implants in 135 HIV- negative patients. The mean age of the patients was 51.6 years. The mean follow- up period was 47.9 months (range 6–120 months). Implants were most often placed in the mandible. There were several var- iations in the implant systems used, in- cluding length (range 8–16 mm) and diameter (range 3.3–5 mm). The quantita- tive and qualitative study data are summa- rized in Tables 1 and 2. The patients had a mean CD4+ T-cell count of <550 cells/mm3 in the majority of studies. However, in the study by Gher- lone et al.9, the mean count was 726.3 cells/mm3. Antiretroviral therapy was reported in four studies3,8,18,20, all of which used HAART. One of the select- ed studies compared two groups: group 1 patients had been treated with protease inhibitor (PI)-based HAART and group 2 patients had been treated with non-nu- cleoside reverse transcriptase inhibitor (NNRTI)-based HAART (without a PI)3. The study found that antiretroviral therapy did not influence the implant survival rate. Four studies reported the use of prophy- lactic drug therapy with antibiotics (amox- icillin with or without clavulanic acid)3,9,18,20. Two studies reported the use of anti-inflammatory drugs postopera- tive (sodium diclofenac, paracetamol, or piroxicam)3,20. One study did not use pro- http://www.opengrey.eu http://www.opengrey.eu 1338 Lemos et al. Fig. 1. Flowchart of the search strategy. phylactic or postoperative medication8. Rinsing with chlorhexidine was reported in three studies8,9,20. Risk of bias/quality analysis of the studies included Four studies were awarded seven stars and two studies were awarded eight stars on the NOS, indicating a low risk of bias for the included studies. Categories most frequent- ly missing stars were non-exposed cohort (absence of a non-exposed cohort), addi- tional comparison factors, and the duration of follow-up (insufficient) (Table 3). Survival and success rates of implants All of the studies assessed reported the survival rates of implants in HIV-positive patients. Specifically, 27 of 493 implants failed (5.5%). In the studies that reported HIV-negative patients3,18,19, 16 of 328 implants failed (4.9%). Two studies reported 100% survival of implants placed in HIV-positive patients3,18, while all of the other studies reported survival rates of >90%8,9,19,20. The implant failure rates for each study are illustrated in Fig. 2. Regarding the success rate of implants, three studies3,18,20 used the success crite- ria defined by Albrektsson et al.22. One article did not report success rate data9, while four studies reported success rates that were the same as the implant survival rates3,8,18,19. Only one study reported suc- cess and survival rates that were differ- ent20. In that study, there was one implant failure (98.3%); however, due to the large number of complications, the implant suc- cess rate was 68.4%. The weighted mean values of the im- plant survival and success rates were cal- culated at the patient level (according to the number of patients) and at the implant level (according to the number of implants). At the patient level, the mean survival rate was 94.76% and the mean success rate was 93.81%. At the implant level, the mean survival rate was 94.53% and the mean success rate was 90.37% (Table 1). Marginal bone loss Three studies evaluated marginal bone loss3,9,18. One study evaluated only HIV-positive patients, and these patients showed a mean marginal bone loss of 1.19 mm9. The two other studies observed no difference in marginal bone loss be- tween HIV-positive and HIV-negative patients, with a mean loss of <0.55 mm in both groups3,18. Weighted mean values of marginal bone loss were calculated: the mean loss at the patient level was 0.83 mm and at the implant level was 0.99 mm (Table 1). Complications Three studies reported complication rates3,9,20. One of these studies found no complications in the patients evaluated3. The other two studies reported peri- implantitis (n = 35), mucositis (n = 6), and prosthetic failure (n = 2) as the most prevalent complications in patients with HIV9,20. Discussion The oral rehabilitation of patients using dental implants is now a routine treatment in clinics. However, limited scientific evi- dence is available to guide clinicians re- garding the risks associated with dental implant placement in HIV-positive patients9. The first null hypothesis of this review was accepted, since the survival rate of implants in HIV-positive patients was similar to that in HIV-negative patients23. Of the six selected studies, three per- formed a direct comparison between HIV-positive and HIV-negative patients; none found any difference in implant sur- vival rate between the two groups3,18,19. Some factors may be related to these favourable results observed in HIV-posi- tive patients, such as antiretroviral therapy (HAART), which increases the number of CD4+ T-cells and consequently reduces immunosuppression in the patient24. Four studies reported the use of HAART in HIV-positive patients, which may have contributed to the increase in mean CD4 + cells3,8,18,20. However, the other two studies reported that the CD4+ cell count did not influence the implant survival rate3,9. A greater risk of complications has been related to the presence of substantial im- munosuppression (CD4+ cell count <200 cells/mm3) and to severe neutrope- nia (absolute neutrophil count <500 cells/ mm3)6,25. However, the selected studies in this systematic review reported mean CD4 + T-cell counts of >400 cells/mm3, except for one study that reported a mean CD4+ T-cell count of <200 cells/mm3 (mean 141.25 cells/mm3); this study showed the highest rate of implant failure among the included studies (9.1%)8. In addition, S u rviva l o f im p la n ts p la ced in H IV -p o sitive p a tien ts 1 3 3 9 Table 1. Summary of the quantitative analysis of included studies. Study Patients, n Implants, n Mean age, years Arch CD4+ count (cells/mm3), mean (SD) Complications, n MBL (mm), mean (SD) Survival rates of implants, n (%) Weighted mean values of the outcomes for HIV-positive patients MBL Survival Success May et al. 20168 16 33 36.2 28 Mx 6 Md 141.25 (35.5) NR NR 30 (90.9%) Based on number of patients Gherlone et al. 20169 66 190 55.3 Mx Md 726.3 (201.4) PI (10) PF (2) 1.19 (0.87) 175 (92.1%) 0.83 mm 94.76% 93.81% Gay-Escoda et al. 201620 9 57 42 4Mx 8 Md 436 (NR) Mucositis (6) PI (25) NR 56 (98.2%) Based on number of implants Rania et al. 201519 145 NR >300b (NR) NR NR HIV(+): 126 (94.0%) HIV(�): 274 (94.5%) 0.99 mm 94.53% 90.37% 34 HIV(+) 134 54 111 HIV(�) 290 52 Oliveira et al. 20113,a 39 46.2 59 Md HIV(+)1: 400 (NR) None HIV(+)1: 0.49 HIV(+)1: 20 (100%) 11 HIV(+)1 20 HIV(+)2: 543.5 (NR) HIV(+)2: 0.47 HIV(+)2: 19 (100%) 13 HIV(+)2 19 HIV(�): 0.55 HIV(�): 20 (100%) 15 HIV(�) 20 Stevenson et al. 200718 29 57.1 58 Md 467 (NR) NR HIV(+): 0.06 (0.09) HIV(+): 40 (100%) 20 HIV(+) 40 HIV(�): 0.18 (0.17) HIV(�): 18 (100%) 9 HIV(�) 18 MBL, marginal bone loss; Md, mandible; Mx, maxilla; NR, not reported; PF, prosthetic failure; PI, peri-implantitis; SD, standard deviation. a This study compared two groups: group 1 patients treated with protease inhibitor-based HAART and group 2 patients treated with non-nucleoside reverse transcriptase inhibitor-based HAART (without a protease inhibitor). b The authors mentioned only that ‘‘all patients received surgery after achieving a CD4+ count >300 cell/mm3’’. 1 3 4 0 L em o s et a l. Table 2. Summary of the qualitative analysis of included studies. Study Study design Follow-up, months Implant system Diameter (D) Length (L) Antiretroviral therapy Medication Prophylaxis Postoperative May et al. 20168 Observational 60 Bicon D: 4, 4.5, 5 mm L: 8, 11 mm HAART No medication Chlorhexidine gluconate 0.12% rinse Gherlone et al. 20169 Observational 12 WinSix D: 3.3, 3.8, 4, 5 mm L: 9, 11, 13 mm NR Amoxicillin–clavulanic acid (2 g 1 h before surgery) Amoxicillin–clavulanic acid (1 g twice per day for 7 days); chlorhexidine (0.2% rinse for 15 days) Gay-Escoda et al. 201620 Retrospective 77.4 Nobel, Defcon, Astra, Straumann D: NR L: NR HAART Amoxicillin (2 g 1 h before surgery) Amoxicillin (750 mg every 8 h for 7 days); sodium diclofenac (50 mg every 8 h for 5 days); paracetamol (1 g every 8 h for 4 days); chlorhexidine 0.12% (every 12 h for 15 days) Rania et al. 201519 Retrospective 120 NR NR NR NR Oliveira et al. 20113,a Observational 12 Serson Implus D: 3.5 L: 10–16 mm HIV(+)1: PI- based HAART HIV(+)2: NNRTI-based HAART (without PI) Amoxicillin (500 mg 1 h before surgery); piroxicam (20 mg 1 h before surgery) Amoxicillin (500 mg three times per day for 5 days); piroxicam (20 mg every 24 h for 3 days) Stevenson et al. 200718 Observational 6 BioHorizons D: NR L: NR HAART Amoxicillin (1 h before surgery) Amoxicillin (500 mg 3 per day for 7 days) HAART, highly active antiretroviral therapy; NR, not reported; NNRTI, non-nucleoside reverse transcriptase inhibitor; PI, protease inhibitor. Table 3. Quality assessment of the included studies based on the Newcastle–Ottawa scale. Study Selection Comparability Outcome Total Exposed cohort Non-exposed cohort Ascertainment of exposure Outcome of interest not present at start Main factor Additional factor Assessment of outcome Follow-up long enougha Adequacy of follow-up May et al. 20168 $ 0 $ $ $ 0 $ $ $ 7 Gherlone et al. 20169 $ 0 $ $ $ $ $ 0 $ 7 Gay-Escoda et al. 201620 $ 0 $ $ $ 0 $ $ $ 7 Rania et al. 201519 $ $ 0 $ $ 0 $ $ $ 7 Oliveira et al. 20113 $ $ $ $ $ $ $ 0 $ 8 Stevenson et al. 200718 $ $ $ $ $ $ $ 0 $ 8 a Five years was considered an adequate time period over which to observe the outcome ‘implant failure’. Survival of implants placed in HIV-positive patients 1341 Fig. 2. Number of implants that survived, number that failed, and the implant failure rate in HIV-positive patients for each of the six studies. the same study reported no usage of pro- phylactic or postoperative medications8. These factors may have been responsible for the failures, since patients with a CD4+ T-cell count <200 cells/mm3 would usu- ally be given broad-spectrum antibio- tics25. In a systematic review, Esposito et al.26 reported that prophylactic antibio- tics reduce the failure of dental implants placed in ordinary conditions, but that there are no apparent differences in the occurrence of postoperative infections. Thus, the use of antibiotics before surgery is recommended, especially because the inflammatory process at the site of surgery causes a temporary reduction in the CD4+ T-cell count after implant placement5. Marginal bone loss is considered an important parameter in implantology27. In this review, the mean marginal bone loss was below the 1.2 mm considered acceptable in the literature23. In studies that conducted a comparison between patients with and without HIV, there was no difference in marginal bone loss3,18. Therefore, the second null hy- pothesis was also accepted. Clinical analysis of bone resorption levels is especially important in HIV-pos- itive patients because HAART causes dif- ferent bone disorders and thus reduces bone mineral density3. Oliveira et al.3 compared NNRTI-based HAART and PI-based HAART, since reduced bone mineral density has been shown to corre- late significantly with PI-based HAART. Although these authors observed low bone mineral density in HIV-positive patients, there was no difference in marginal bone loss between patients with and without HIV infection, regardless of the antiretro- viral therapy used. However, it is impor- tant to note that the longest follow-up period in the three studies evaluating mar- ginal bone loss was 1 year. Thus, addition- al clinical studies with longer follow-up periods are necessary to verify the clinical stability of bone tissue in HIV-positive patients. The most frequently reported complica- tion in the selected studies was peri- implantitis9,20. Implant failures were most often related to postoperative complica- tions that led to infection and/or peri- implantitis and consequent implant loss8,9,20. However, the high risk of peri- implantitis in these patients may have been associated with factors other than immunosuppression. Gay-Escoda et al.20 reported the highest number of peri- implantitis cases (n = 25); most involved patients who had advanced periodontal disease and had failed to comply with periodontal/peri-implant maintenance vis- its. These results are in agreement with those of another systematic review, which reported that supportive implant treatment (maintenance visits) prevents the occur- rence of tissue disease around implants28. Gherlone et al.9 also presented a high number of patients with peri-implantitis (10 cases). Such a high risk of complica- tions was observed in patients who smoked (>10 cigarettes per day), which also contributed significantly to implant failure in HIV-positive patients. These results corroborate those of another study, which found that smoking affects implant survival rates and the incidence of post- operative infections29. The results of this review should be interpreted with caution, as there were a number of uncontrolled confounding fac- tors in the included studies, no RCT stud- ies were included, and three studies had short follow-up periods. Thus, in the fu- ture, more studies with longer follow-up periods should be conducted to compare HIV-positive and negative patients. In conclusion, within the limitations of this study, this systematic review indicates that dental implants are suitable for HIV- positive patients with controlled risk fac- tors and normal CD4+ cells counts, be- cause implant survival rates and levels of marginal bone loss were similar to those of HIV-negative patients. Funding None. Competing interests The authors declare that there was no conflict of interest in the elaboration of this study. Ethical approval Not applicable. 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Pellizzer Department of Dental Materials and Pros- thodontics São Paulo State University (UNESP) Araçatuba Dental School José Bonifácio St 1193 Araçatuba São Paulo 16015-050 Brazil Tel: +55 1836363297 Fax: +55 1836363245 E-mail: ed.pl@uol.com.br http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0045 http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0045 http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0045 http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0045 http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0045 http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0045 http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0050 http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0050 http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0050 http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0055 http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0055 http://refhub.elsevier.com/S0901-5027(18)30064-X/sbref0055 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characteristics Risk of bias/quality analysis of the studies included Survival and success rates of implants Marginal bone loss Complications Discussion Funding Competing interests Ethical approval Patient consent References