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Management of cannabis-induced periodontitis via resective surgical therapy A clinical report

Fatemeh Momen-Heravi, DDS, MPH; ABSTRACT Philip Kang, DDS Background and Overview. There is a lack of clinical research on the potential effect of cannabis use on the as well as eriodontal inflammation and bone loss its effect on treatment outcomes. The aim of this case report is to are manifestations of periodontal dis- illustrate the clinical presentation of in a young ease, which is attributed to different woman who was a chronic cannabis user, as well as successful 1 P environmental and genetic factors. treatment involving motivating the patient to quit cannabis use and Environmental factors, such as smoking, are undergo nonsurgical and surgical therapy. 2 well-studied. Smoking is identified as a signifi- Case Description. A 23-year-old woman sought care at the dental cant risk factor for both severity and extent of clinic for periodontal treatment. During a review of her medical periodontal disease through impairing the im- history, the patient reported using cannabis frequently during a mune response, and compromising the tissue’s 3-year period, which coincided with the occurrence of gingival 3 healing ability. Some epidemiologic studies and inflammation. She used cannabis in the form of cigarettes that were clinical reports suggest a relationship between placed at the mandibular anterior region of her mouth for prolonged 4 6 cannabis smoking and periodontal disease. - periods. Localized prominent papillary and marginal gingival In a cohort study that evaluated periodontal enlargement of the anterior mandible were present. The mandibular attachment loss (AL) at different ages (26, 32, anterior teeth showed localized severe . The and 38 years old), smokers had 3.5%, 12.8%, and clinicians informed the patient about the potentially detrimental 23.2% AL compared with nonsmokers, respec- consequences of continued cannabis use; she was encouraged to quit, tively. Frequent cannabis use was reported to be which she did. The clinicians performed nonsurgical therapy (scaling associated with greater AL after age 32 years, but and root planing) and osseous surgery. The treatment outcome 4 not at age 26 years. Those who had smoked was evaluated over 6 months; improved radiographic and clinical tobacco at young ages (from 15 through 38 years) results were observed throughout the follow-up period. were at a higher risk of being in the moderately Conclusions and Practical Implications. Substantial avail- or markedly increasing trajectory groups of ability and usage of cannabis, specifically among young adults, re- periodontal disease. There was a similar risk quires dentists to be vigilant about clinical indications of cannabis use gradient for those who were in the highest 20% and to provide appropriate treatments. Behavioral modification, 5 of cannabis usage. nonsurgical therapy, and surgical therapy offer the potential for 6 Thomson and colleagues reported the inci- successful management of cannabis-related periodontitis. dence of AL between the ages of 26 and 32 years Key Words. Cannabis; ; marijuana; in the none, occasional, and high cannabis nonsurgical therapy; oral health; periodontal disease; periodontal surgery; periodontitis. JADA 2016:-(-):--- Copyright ª 2016 American Dental Association. All rights http://dx.doi.org/10.1016/j.adaj.2016.10.009 reserved.

JADA -(-) http://jada.ada.org - 2016 1 ORIGINAL CONTRIBUTIONS exposure groups as 6.5%, 11.2%, and 23.6%, respectively. occurrence of gingival inflammation. She used cannabis After controlling for sex, tobacco smoking (measured in in the form of hand-constructed cigarettes that were pack-years), compliance, and , the relative placed at the lower anterior region of her teeth and lips risks for the highest cannabis exposure group were 1 for prolonged periods. The patient reported that gingival (95% confidence interval [CI], 1.2-2.2) for exhibiting 1 or enlargement occurred shortly after she started smoking more sites with 4 millimeters or more AL, 3.1 (95%CI, cannabis; she reported xerostomia as well. 1.5-6.4) for exhibiting 1 or more sites with 5 mm or more During the clinical examination we observed gener- AL, and 2.2 (95% CI, 1.2-3.9) for exhibiting incident AL in alized decalcification of the teeth near the buccal 6 comparison with people who never smoked cannabis. gingival margins. The papillary and marginal gingivae Tobacco smoking was strongly associated with peri- showed localized enlargement. We noted a nodular odontal disease occurrence; however, no relationship was appearance of the facial gingiva with 6-mm AL at the found between cannabis use and tobacco smoking in mesiofacial aspect of tooth no. 24 and mesiofacal aspect 6 predicting the occurrence of periodontal disease. of tooth no. 25 (Figure 1A, B). While examining the Cannabis is one of the most commonly used recrea- periodontium, we found the lingual gingiva had normal 7 tional drugs in the United States and across the world. probing depths in conjunction with mild gingival Based on the 2013 National Survey on Drug Use and inflammation (Figure 1C). The probing depth, attach- Health, cannabis is the most frequently used recreational ment level, and are shown in the 8 substance, with 19.8 million past-month users. In 2014, table. Radiographic interproximal bone loss was also 2.5 million people 12 years or older reported use of evident (Figure 1D). marijuana for the first time during the past 12 months, Only 2 sites in the maxilla (mesiobuccal aspect of which indicates an average of nearly 7,000 new users tooth no. 2, mesiobuccal aspect of tooth no. 14) had 8 each day. It has been estimated that approximately 147 probing depths greater than 3 mm without concomitant 9 million people (2.5%) around the world use cannabis. In radiographic and clinical AL. We found no evidence of the United States, policy changes including legalization AL clinically in areas other than the mandibular anterior and legislation in many states have increased usage teeth. We did not identify interproximal bone loss on drastically, and have lowered the perception of risk by posterior bitewing and periapical radiographs. The pa- 8 the public, especially in the population of young adults. tient stated that she was aware of the enlarged gingiva in A dental health screening of 13-to18-year-olds across the anterior region and reported sensitivity, bleeding, 8 years in public and private middle schools and high and discomfort in that region. schools in Nevada showed significantly higher rates We made a periodontal diagnosis of drug-associated of cannabis use (12%) compared with the national gingival enlargement, mucogingival deformities, and 10 15 average. As a dental health care professional, it can be conditions around teeth in the form of gingival excess challenging to uncover a patient’s drug abuse and treat and localized severe, chronic periodontitis. the various manifestations of cannabis use in the oral We planned the following sequence of therapy: cavity. - prophylaxis with localized Although some reports have addressed the effect of (SRP) around the mandibular anterior teeth; cannabis smoking on the oral cavity, including xero- - periodontal re-evaluation; stomia, leukoplakia, oral candida, and specific peri- - surgical therapy as needed. odontal complications such as , periodontal The overall prognosis at that time was determined as 16 bone loss, and gingival enlargement, documented clinical questionable based on Kwok and Caton’s classification, periodontal manifestations of frequent cannabis use as the periodontal status of the involved teeth was 11 14 are limited. - Moreover, we are not aware of any study influenced by local and systemic factors that might not reporting clinical management of cannabis-induced AL. have been possible to control. We performed localized In the following case report, we discuss a patient with SRP involving the mandibular anterior incisors, whereas chronic, cannabis-induced localized periodontitis and other areas received an adult prophylaxis. We re- gingival enlargement. enforced instructions to the patient. In addition, the patient was started on a CASE REPORT gluconate (0.12%) oral rinse, twice a day, for 2 weeks. We A 23-year-old woman sought care at the postgraduate informed the patient about the potential health conse- periodontics clinic at the College of Dental Medicine at quences of cannabis, and the patient reported quitting Columbia University. The patient’s medical history was cannabis use after SRP. noncontributory, and the patient denied the use of any medications and tobacco smoking. Her oral hygiene was fair with some plaque accumulation on the mandibular incisors. The patient reported smoking cannabis ABBREVIATION KEY. AL: Attachment loss. D: Distal. frequently over a 3-year period, which coincided with the F: Facial. L: Lingual. M: Mesial. SRP: Scaling and root planing.

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Figure 1. Clinical and radiographic presentations during initial visit and nonsurgical therapy. A. Initial visit, frontal view. B. Initial visit, facial view of mandibular anterior teeth showing papillary gingival enlargement and edematous tissue with increased probing depth (7 millimeters) at the mesiofacial aspect of teeth nos. 24 and 25. C. Initial visit, lingual view of anterior teeth showing nodular appearance. D. Radiographic bone loss seen at the mandibular anterior teeth (nos. 23-26) with more prominent bone loss at interproximal site of teeth nos. 24 and 25. E. Frontal view at re-evaluation visit 4 weeks after scaling and root planing.

We performed TABLE a periodontal re- Periodontal indexes at initial visit, re-evaluation visit, and evaluation 4 weeks after initial therapy 6 months after surgical treatment. (Figure 1E). The TOOTH INITIAL VISIT RE-EVALUATION VISIT 6 MONTHS AFTER mandibular incisors NO. (PROBING DEPTH, AL*) (PROBING DEPTH, AL) SURGICAL TREATMENT (PROBING DEPTH, AL) exhibited probing † ‡ § ¶ depths of 5-6 mm, M F FDFML LDLMFFDFMLLDLMFFDFMLLDL with persistent 21 3, 0 2, 0 3, 0 3, 0 2, 0 3, 0 3, 0 2, 0 3, 0 3, 0 2, 0 2, 0 3, 0 2, 0 3, 0 3, 0 2, 0 3, 0 bleeding on probing 22 3, 0 2, 0 3, 0 3, 0 2, 0 3, 0 3, 0 2, 0 3, 0 3, 0 2, 0 2, 0 2, 0 2, 0 2, 0 3, 0 2, 0 3, 0 (Table). Other teeth 23 5, 0# 4, 0 4, 0 3, 0 2, 0 3, 0 5, 0 4, 0 4, 0 3, 0 2, 0 3, 0 2, 0 2, 0 2, 0 3, 0 2, 0 3, 0 showed shallow prob- 24 7, -1 4, 0 4, 0 3, 0 2, 0 2, 0 5, 0 4, 0 4, 0 3, 0 2, 0 2, 0 2, 0 2, 0 2, 0 3, 0 2, 0 2, 0 ing depth without 25 7, -1 4, 0 5, 0 2, 0 2, 0 2, 0 6, 0 4, 0 5, 0 2, 0 2, 0 2, 0 2, 0 2, 1 2, 0 2, 0 2, 0 2, 0 clinical AL and radio- 26 5, -1 4, 0 5, 0 2, 0 2, 0 2, 0 5, 0 4, 0 4, 0 2, 0 2, 0 2, 0 3, 0 2, 0 3, 0 2, 0 2, 0 2, 0 graphic bone loss. We 27 5, 0 3, 0 3, 0 3, 0 2, 0 3, 0 4, 0 3, 0 3, 0 3, 0 2, 0 3, 0 3, 0 2, 0 2, 0 3, 0 2, 0 3, 0 made a decision to * AL: Attachment level (negative numbers indicate above cementoenamel junction). † M: Mesial. proceed with surgical ‡ F: Facial. intervention in an § D: Distal. attempt to re-establish ¶ L: Lingual. the marginal bone # A bold number denotes bleeding on probing. integrity and healthy gingiva. frenectomy, and the flap was apically positioned to bone Surgical procedure. During our evaluation, the level and secured with a continuous sling suture of 4-0 results of bone sounding suggested a normal lingual black silk (Figure 2). We placed a periodontal dressing marginal bone level. Thus, we made the decision to avoid over the surgical wound. We instructed the patient to a lingual mucoperiosteal flap reflection. We reflected rinse with chlorhexidine 0.12% twice a day. Two weeks a facial, full-thickness mucoperiosteal flap from the after the surgery, the facial tissue appeared uniformly mesiofacial aspect of tooth no. 22 to the distofacial aspect pale and pink, with the exception of a slight gingival of tooth no. 27. We noted 1-wall infrabony defects at the granulation tissue rebound between teeth nos. 24 and 25, interproximal aspect of teeth nos. 24 and 25 and teeth which we eventually removed by 1 month nos. 25 and 26. We performed degranulation of the after surgery. osseous defects, SRP and osteoplasty on all teeth, and an Clinical outcomes. Healing was uneventful, and the ostectomy to re-establish marginal bone morphology to original goals of pocket reduction and restoration of a recreate a healthy bony architecture. We performed a healthy marginal bony architecture were achieved,

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hygiene, and demographics are required to assess and construct fully adjusted models and establish perti- nent risk. Our case report demon- strates suc- cessful man- agement of a localized peri- odontal AL and gingival papillary enlargement associated with frequent chronic Figure 2. Clinical presentations during surgical therapy. A. Incision. B. Flap elevation, osteoplasty, and ostectomy. C. Facial cannabis use view of suturing and frenotomy. D. Lingual view of suturing. in a young woman. 24 thereby creating conditions that allowed the patient to Layman was the first to report an association between maintain a plaque-free environment (Figure 3). chronic cannabis use and gingival enlargement, which At 1 month after surgery, all treated teeth had probing in that report was described as “fiery-red gingiva,” and depths of 2 to 3 mm; and at 6 months, probing depths similar in form to that seen in a phenytoin sodium 14 remained stable with no increase (Table). We obtained drug–induced enlargement. Rawal and colleagues re- periapical radiographs at baseline and at 2 and 6 months ported a nodular (pebbly) appearance of the gingiva, after surgery. We measured the bony defects at baseline without AL, in 2 men who were frequent cannabis and 6 months after surgery using ImageJ, a Java-based users. We found only 1 documented case of a frequent 12 image processing program developed at the National cannabis user (Baddour and colleagues ) with alveolar Institutes of Health. At baseline, the defect depth was bone loss in addition to the gingival enlargement. In 6.2 mm, as measured from the cementoenamel junction both of the latter cases and including our case report, to the defect base. At 6 months after surgery, there was the duration of marijuana use was more than 2 years. radiographic evidence of a 2.1-mm decrease in depth, Although the incidence and prevalence of cannabis use indicating a near-complete osseous fill of the defect. is reported to be higher in men, the demographics for cannabis use are changing and are different based on 25 DISCUSSION race and ethnicity. A study by Nogueira-Filho and 26 Cannabis is the most widely used illicit substance in colleagues, in which marijuana was inhaled in the 17 the United States. Besides psychological and general presence of dental plaque for 8 minutes per day, 18 19 health effects of cannabis use, described elsewhere, , resulted in significantly more bone loss as compared cannabis also has various effects on the oral cavity. with controls. Cannabis use has been associated with poor oral health, In this respect, investigators have reported that a 7 13 higher caries rates, and higher plaque scores. , Xero- G-protein–coupled receptor, GPR55, is activated by stomia and cannabis stomatitis are reported in frequent cannabinoids and upregulates the number and matura- 19 20 27 cannabis users. , Cannabis smoking is reported to be tion of osteoclasts. Although such reports support the associated with a higher incidence of premalignant le- biological plausibility of a link between cannabis use and sions and malignant lesions, including head and neck periodontal disease, including bone loss, the patho- 7 21 23 cancer. , - Knowledge of the effect of cannabis use on genic mechanisms remain to be investigated. Delta- oral health and periodontal health is inadequate. 9-tetrahydrocannabinol, known as THC, is the most Perspective cohort studies that include covariates such potent cannabinoid in cannabis. It has been shown to as frequency, amount of product usage, age of starting have immunosuppressive effect via the cannabinoid usage, duration of usage, mode of administration, oral receptor type 2 receptors found in immune cells, which

4 JADA -(-) http://jada.ada.org - 2016 ORIGINAL CONTRIBUTIONS can potentially propagate change of oral microbiota due to altered immune 28 29 response. , It has been well recog- nized that it is difficult to ac- count for the frequency, duration, amount, and route of administration in all people and correlate in vitro and in vivo studies Figure 3. Clinical and radiographic presentations after surgery. A. Clinical presentation 2 months after surgical therapy. B. with the bio- Reduction of probing depth to 2 millimeters at 1 month after surgery. C. Clinical presentation 6 months after surgical therapy. logically rele- D. Radiographic findings 1.5 months after surgical therapy. E. Radiographic findings 6 months after surgery. vant dose. Personal risk factors, including amount of plaque, oral after phase 1 therapy. Despite determination of the initial hygiene, systemic health, and socioeconomic status make prognosis as questionable, we observed an excellent it difficult to assess the specific effect of cannabis use postoperative healing response in our patient. The pos- on periodontal health. itive outcome was attributed to the patient’s cessation of A study conducted by Schulz-Katterback and col- cannabis use, and her healing was possibly aided by her 30 32 leagues evaluated the effect of cannabis use and risk of young age. developing dental caries. The result of this study showed that frequent cannabis users visit dentists less regularly CONCLUSION and have higher plaque index. Cannabis users reported 30 In conclusion, frequent chronic cannabis use may result dry mouth from 1 to 6 hours after the use of cannabis. 20 in periodontal bone loss and gingival enlargement as A study conducted by Darling and Arendorf reported it did in our patient. By informing our patient about high prevalence of dry mouth after cannabis smoking the health consequences of cannabis use, we were able 69 6 18 6 ( . %) compared with cigarette smoking ( . %). to help the patient quit cannabis smoking. A combi- Moreover, the buffering capacity of saliva was reported 31 nation of nonsurgical and surgical therapy resulted in to be reduced in cannabis smokers. As mentioned, the decreased probing pocket depths, gingival inflamma- direct effect of cannabis can induce periodontal bone tion, and sulcus bleeding index and decreased attach- loss, xerostomic effects, and subsequent accumulation of ment level, when comparing the initial and 6-month plaque and as a result of poor plaque control; follow-up data. In the 6-month follow-up examination, these effects could be contributing to the initiation of radiographs after surgical periodontal therapy showed periodontal disease, in addition to the ingredients of significant resolution of bony defects. The combination cannabis. of nonsurgical and surgical therapy may be an effective In our patient, we found moderate to severe AL approach to manage cannabis-induced periodontitis. and marginal gingival enlargement, which were more Beyond the limits of this case report, the significance of pronounced in the anterior mandible. The gingival surgical intervention in the evidence-based treatment of enlargement and swelling that we observed from cannabis-induced periodontal bone loss remains to be canine to canine in the mandible might be due to more evaluated. n gingival absorption of cannabis because of the habitual placement of the cannabis cigarette and additional 14 24 Dr. Momen-Heravi is a resident, Division of Periodontics, Section of mechanical irritation in the area. , Oral and Diagnostic Sciences, College of Dental Medicine, Columbia Initially, we identified an unclear prognosis and un- University, New York, NY. Dr. Kang is an assistant professor, Dental Medicine, and the director, predictable outcome after our planned treatment of Postgraduate Periodontics, Division of Periodontics, Section of Oral and pocket reduction surgery and osseous surgery, performed Diagnostic Sciences, College of Dental Medicine, Columbia University,

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