REVIEW ARTICLE
The effects of cannabis use on oral health
Chunyan Liu,
Xia Qi,
Dongru Yang,
Anthony Neely,
Zheng Zhou,
Chunyan Liu
School of Dentistry, University of Detroit Mercy, Detroit, MI, USA
School and Hospital of Stomatology, Hebei Medical University & Hebei Key Laboratory of Stomatology, Shijiazhuang, Hebei, China
Search for more papers by this authorXia Qi
School of Dentistry, University of Detroit Mercy, Detroit, MI, USA
School and Hospital of Stomatology, Hebei Medical University & Hebei Key Laboratory of Stomatology, Shijiazhuang, Hebei, China
Search for more papers by this authorCorresponding Author
Dongru Yang
School and Hospital of Stomatology, Hebei Medical University & Hebei Key Laboratory of Stomatology, Shijiazhuang, Hebei, China
Correspondence
Zheng Zhou, School of Dentistry, University of Detroit Mercy, 2700 Martin Luther King Jr. Blvd., Detroit, MI 48208, USA.
Email: [email protected]
Dongru Yang, School and Hospital of Stomatology, Hebei Medical University & Hebei Key Laboratory of Stomatology, Shijiazhuang, Hebei, China.
Email: [email protected]
Search for more papers by this authorAnthony Neely
School of Dentistry, University of Detroit Mercy, Detroit, MI, USA
Search for more papers by this authorCorresponding Author
Zheng Zhou
School of Dentistry, University of Detroit Mercy, Detroit, MI, USA
Correspondence
Zheng Zhou, School of Dentistry, University of Detroit Mercy, 2700 Martin Luther King Jr. Blvd., Detroit, MI 48208, USA.
Email: [email protected]
Dongru Yang, School and Hospital of Stomatology, Hebei Medical University & Hebei Key Laboratory of Stomatology, Shijiazhuang, Hebei, China.
Email: [email protected]
Search for more papers by this authorChunyan Liu,
Xia Qi,
Dongru Yang,
Anthony Neely,
Zheng Zhou,
Chunyan Liu
School of Dentistry, University of Detroit Mercy, Detroit, MI, USA
School and Hospital of Stomatology, Hebei Medical University & Hebei Key Laboratory of Stomatology, Shijiazhuang, Hebei, China
Search for more papers by this authorXia Qi
School of Dentistry, University of Detroit Mercy, Detroit, MI, USA
School and Hospital of Stomatology, Hebei Medical University & Hebei Key Laboratory of Stomatology, Shijiazhuang, Hebei, China
Search for more papers by this authorCorresponding Author
Dongru Yang
School and Hospital of Stomatology, Hebei Medical University & Hebei Key Laboratory of Stomatology, Shijiazhuang, Hebei, China
Correspondence
Zheng Zhou, School of Dentistry, University of Detroit Mercy, 2700 Martin Luther King Jr. Blvd., Detroit, MI 48208, USA.
Email: [email protected]
Dongru Yang, School and Hospital of Stomatology, Hebei Medical University & Hebei Key Laboratory of Stomatology, Shijiazhuang, Hebei, China.
Email: [email protected]
Search for more papers by this authorAnthony Neely
School of Dentistry, University of Detroit Mercy, Detroit, MI, USA
Search for more papers by this authorCorresponding Author
Zheng Zhou
School of Dentistry, University of Detroit Mercy, Detroit, MI, USA
Correspondence
Zheng Zhou, School of Dentistry, University of Detroit Mercy, 2700 Martin Luther King Jr. Blvd., Detroit, MI 48208, USA.
Email: [email protected]
Dongru Yang, School and Hospital of Stomatology, Hebei Medical University & Hebei Key Laboratory of Stomatology, Shijiazhuang, Hebei, China.
Email: [email protected]
Search for more papers by this authorAbstract
Cannabis, also known as marijuana, is one of the most commonly used substances for medical and recreational purposes globally. With the trend of global legalization of medical use of cannabis and even the recreational use, the prevalence of recreational use of cannabis has increased markedly over the past few years. Correspondingly, the potential health concerns related to cannabis consumption have also increased. Therefore, it is necessary for oral healthcare providers to understand the effects of cannabis use on oral health. This review briefly summarizes the components of cannabis, biologic activities on tissues, and mechanisms of action in human cells and tissues. Oral tissue expression of cannabinoid receptors and the potential association of cannabis to oral diseases are also examined. The goals of this review are to (1) elaborate the basic biology and physiology of cannabis in human oral tissues, and (2) provide a better understanding the effects of its use and abuse on oral health. Due to insufficient information, more well-designed studies should be conducted. It is urgent to include cannabis usage into dental patient health records.
REFERENCES
- Abidi, A. H., Presley, C. S., Dabbous, M., Tipton, D. A., Mustafa, S. M., & Moore, B. M. 2nd (2018). Anti-inflammatory activity of cannabinoid receptor 2 ligands in primary hPDL fibroblasts. International Journal of Molecular Sciences, 87, 79–85.
- Aghazadeh Tabrizi, M., Baraldi, P. G., Borea, P. A., & Varani, K. (2016). Medicinal chemistry, pharmacology, and potential therapeutic benefits of cannabinoid CB2 receptor agonists. Chemical Reviews, 116, 519–560.
- Atakan, Z. (2012). Cannabis, a complex plant: Different compounds and different effects on individuals. Therapeutic Advances in Psychopharmacology, 2, 241–254.
- Beneng, K., Renton, T., Yilmaz, Z., Yiangou, Y., & Anand, P. (2010). Cannabinoid receptor CB1-immunoreactive nerve fibres in painful and non-painful human tooth pulp. Journal of Clinical Neuroscience, 17, 1476–1479.
- Biro, T., Toth, B. I., Hasko, G., Paus, R., & Pacher, P. (2009). The endocannabinoid system of the skin in health and disease: Novel perspectives and therapeutic opportunities. Trends in Pharmacological Sciences, 30, 411–420.
- Borsani, E., Majorana, A., Cocchi, M. A., Conti, G., Bonadeo, S., Padovani, A., … Rodella, L. F. (2014). Epithelial expression of vanilloid and cannabinoid receptors: A potential role in burning mouth syndrome pathogenesis. Journal of Clinical Pharmacy and Therapeutics, 29, 523–533.
- Busch, L., Sterin-Borda, L., & Borda, E. (2004). Expression and biological effects of CB1 cannabinoid receptor in rat parotid gland. Biochemical Pharmacology, 68, 1767–1774.
- Busch, L., Sterin-Borda, L., & Borda, E. (2006). Effects of castration on cannabinoid cb receptor expression and on the biological actions of cannabinoid in the parotid gland. Clinical and Experimental Pharmacology and Physiology, 33, 258–263.
- Chu, Z.-L., Jones, R. M., He, H., Carroll, C., Gutierrez, V., Lucman, A., … Leonard, J. (2007). A role for β-cell-expressed G protein-coupled receptor 119 in glycemic control by enhancing glucose-dependent insulin release. Endocrinol, 148, 2601–2609.
- Cuba, L. F., Salum, F. G., Cherubini, K., & Figueiredo, M. A. Z. (2017). Cannabidiol: An alternative therapeutic agent for oral mucositis? Journal of Clinical Pharmacy and Therapeutics, 42, 245–250.
- Dall’Aglio, C., Mercati, F., Pascucci, L., Boiti, C., Pedini, V. and Ceccarelli, P.,(2010). Immunohistochemical localization of CB1 receptor in canine salivary glands. Veterinary Research Communications, 34, 9–12.
- Darling, M. R., & Arendorf, T. M. (1992). Review of the effects of cannabis smoking on oral health. International Dental Journal, 42, 19–22.
- Darling, M. R., & Arendorf, T. M. (1993). Effects of cannabis smoking on oral soft-tissues. Community Dent Oral, 21, 78–81.
- Deadwyler, S. A., Hampson, R. E., Mu, J., Whyte, A., & Childers, S. (1995). Cannabinoids modulate voltage sensitive potassium A-current in hippocampal neurons via a cAMP-dependent process. Journal of Pharmacology and Experimental Therapeutics, 273, 734–743.
- Demuth, D. G., & Molleman, A. (2006). Cannabinoid signalling. Life Sciences, 78, 549–563.
- Derkinderen, P., Valjent, E., Toutant, M., Corvol, J. C., Enslen, H., Ledent, C., … Girault, J. A. (2003). Regulation of extracellular signal-regulated kinase by cannabinoids in hippocampus. Journal of Neuroscience, 23, 2371–2382.
- Ditmyer, M., Demopoulos, C., McClain, M., Dounis, G., & Mobley, C. (2013). The effect of tobacco and marijuana use on dental health status in Nevada adolescents: A trend analysis. Journal of Adolescent Health, 52, 641–648.
- Donald, P. J. (1986). Marijuana smoking–possible cause of head and neck carcinoma in young patients. Otolaryngology - Head and Neck Surgery, 94, 517–521.
- Felder, C. C., Joyce, K. E., Briley, E. M., Mansouri, J., Mackie, K., Blond, O., … Mitchell, R. L. (1995). Comparison of the pharmacology and signal transduction of the human cannabinoid CB1 and CB2 receptors. Molecular Pharmacology, 48, 443–450.
- Fernandez-Solari, J., Prestifilippo, J. P., Ossola, C. A., Rettori, V., & Elverdin, J. C. (2010). Participation of the endocannabinoid system in lipopolysaccharide-induced inhibition of salivary secretion. Archives of Oral Biology, 55, 583–590.
- Fernandez-Solari, J., Prestifilippo, J. P., Vissio, P., Ehrhart-Bornstein, M., Bornstein, S. R., Rettori, V., & Elverdin, J. C. (2009). Anandamide injected into the lateral ventricle of the brain inhibits submandibular salivary secretion by attenuating parasympathetic neurotransmission. Brazilian Journal of Medical and Biological Research, 42, 537–544.
- Firth, N. A. (1997). Marijuana use and oral cancer: A review. Oral Oncology, 33, 398–401.
- Gaoni, Y., & Mechoulam, R. (1964). Isolation, structure, and partial synthesis of an active constituent of hashish. Journal of the American Chemical Society, 86, 1646–1647.
- Garrett, E. R., & Hunt, C. A. (1974). Physicochemical Properties, Solubility, and Protein Binding of Δ9 - Tetrahydrocannabinol. Journal of Pharmaceutical Sciences, 63, 1056–1064.
- Godlewski, G., Offertaler, L., Wagner, J. A., & Kunos, G. (2009). Receptors for acylethanolamides-GPR55 and GPR119. Prostaglandins & Other Lipid Mediators, 89, 105–111.
- Grafton, S. E., Huang, P. N., & Vieira, A. R. (2016). Dental treatment planning considerations for patients using cannabis A case report. Journal of the American Dental Association, 147, 354–361.
- Grimaldi, C., Pisanti, S., Laezza, C., Malfitano, A. M., Santoro, A., Vitale, M., … Bifulco, M. (2006). Anandamide inhibits adhesion and migration of breast cancer cells. Experimental Cell Research, 312, 363–373.
- Guzmán, M. (2003). Cannabinoids: Potential anticancer agents. Nature Reviews Cancer, 3, 745–755.
- Hall, W., & Degenhardt, L. (2009). Adverse health effects of non-medical cannabis use. Lancet, 374, 1383–1391.
- Hashibe, M., Ford, D. E., & Zhang, Z. F. (2002). Marijuana smoking and head and neck cancer. Journal of Clinical Pharmacology, 42, 103s–107s.
- Howlett, A. C., Barth, F., Bonner, T. I., Cabral, G., Casellas, P., Devane, W. A., … Pertwee, R. G. (2002). International Union of Pharmacology. XXVII. Classification of Cannabinoid Receptors. Pharmacol Rev, 54, 161–202.
- Joshi, S., & Ashley, M. (2016). Cannabis: A joint problem for patients and the dental profession. British Dental Journal, 220, 597–601.
- Konermann, A., Jager, A., Held, S. A. E., Brossart, P., & Schmole, A. (2017). In vivo and in vitro identification of endocannabinoid signaling in periodontal tissues and their potential role in local pathophysiology. Cellular and Molecular Neurobiology, 37, 1511–1520.
- Kozono, S., Matsuyama, T., Biwasa, K. K., Kawahara, K., Nakajima, Y., Yoshimoto, T., … Maruyama, I. (2010). Involvement of the endocannabinoid system in periodontal healing. Biochemical and Biophysical Research Communications, 394, 928–933.
- Lanza Cariccio, V., Scionti, D., Raffa, A., Iori, R., Pollastro, F., Diomede, F., … Mazzon, E. (2018). Treatment of periodontal ligament stem cells with MOR and CBD promotes cell survival and neuronal differentiation via the PI3K/Akt/mTOR pathway. International Journal of Molecular Sciences, 19(8), 2341. https://doi.org/10.3390/ijms19082341
- Liu, C., Qi, X., Alhabeil, J., Lu, H., & Zhou, Z. (2019). Activation of cannabinoid receptors promote periodontal cell adhesion and migration. Journal of Clinical Periodontology, 46, 1264–1272. https://doi.org/10.1111/jcpe.13190
- Llewellyn, C. D., Linklater, K., Bell, J., Johnson, N. W., & Warnakulasuriya, K. A. A. S. (2003). Squamous cell carcinoma of the oral cavity in patients aged 45 years and under: A descriptive analysis of 116 cases diagnosed in the South East of England from 1990 to 1997. Oral Oncology, 39, 106–114.
- Llewellyn, C. D., Linklater, K., Bell, J., Johnson, N. W., & Warnakulasuriya, S. (2004). An analysis of risk factors for oral cancer in young people: A case-control study. Oral Oncology, 40, 304–313.
- Lopez, R., & Baelum, V. (2009). Cannabis use and destructive periodontal diseases among adolescents. Journal of Clinical Periodontology, 36, 185–189.
- Maccarrone, M., Bab, I., Biro, T., Cabral, G. A., Dey, S. K., Di Marzo, V., … Zimmer, A. (2015). Endocannabinoid signaling at the periphery: 50 years after THC. Trends in Pharmacological Sciences, 36, 277–296.
- Maccarrone, M., Di Rienzo, M., Battista, N., Gasperi, V., Guerrieri, P., Rossi, A., & Finazzi-Agro, A. (2003). The endocannabinoid system in human keratinocytes. Evidence that anandamide inhibits epidermal differentiation through CB1 receptor-dependent inhibition of protein kinase C, activation protein-1, and transglutaminase. Journal of Biological Chemistry, 278, 33896–33903.
- Marincsak, R., Toth, B. I., Czifra, G., Marton, I., Redl, P., Tar, I., … Biro, T. (2009). Increased expression of TRPV1 in squamous cell carcinoma of the human tongue. Oral Diseases, 15, 328–335.
- Marino, S., & Idris, A. I. (2017). Emerging therapeutic targets in cancer induced bone disease: A focus on the peripheral type 2 cannabinoid receptor. Pharmacological Research, 119, 391–403.
- Marks, M. A., Chaturvedi, A. K., Kelsey, K. et al (2014). Association of marijuana smoking with oropharyngeal and oral tongue cancers: Pooled analysis from the INHANCE consortium. Cancer Epidemiology, Biomarkers & Prevention, 23, 160–171.
- Matsuda, L. A., Lolait, S. J., Brownstein, M. J., Young, A. C., & Bonner, T. I. (1990). Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature, 346, 561–564.
- McConnell, W. R., Dewey, W. L., Harris, L. S., & Borzelleca, J. F. (1978). A study of the effect of delta 9-tetrahydrocannabinol (delta 9-THC) on mammalian salivary flow. Journal of Pharmacology and Experimental Therapeutics, 206, 567–573.
- Mechoulam, R. (1982). Chemistry of Cannabis. In F. Hoffmeister, & G. Stille (Eds.), Psychotropic Agents: Part III: Alcohol and Psychotomimetics, Psychotropic Effects of Central Acting Drugs (pp. 119–134). Berlin, Heidelberg: Springer, Berlin Heidelberg.
10.1007/978-3-642-67770-0_7 Google Scholar
- Mechoulam, R., Hanus, L. O., Pertwee, R., & Howlett, A. C. (2014). Early phytocannabinoid chemistry to endocannabinoids and beyond. Nature Reviews. Neuroscience, 15, 757–764.
- Miyashita, K., Oyama, T., Sakuta, T., Tokuda, M., & Torii, M. (2012). Anandamide induces matrix metalloproteinase-2 production through cannabinoid-1 receptor and transient receptor potential vanilloid-1 in human dental pulp cells in culture. Journal of Endodontics, 38, 786–790.
- Moriconi, A., Cerbara, I., Maccarrone, M., & Topai, A. (2010). GPR55: Current knowledge and future perspectives of a purported "Type-3" cannabinoid receptor. Current Medicinal Chemistry, 17, 1411–1429.
- Munro, S., Thomas, K. L., & Abu-Shaar, M. (1993). Molecular characterization of a peripheral receptor for cannabinoids. Nature, 365, 61–65.
- Nabissi, M., Morelli, M. B., Offidani, M., Amantini, C., Gentili, S., Soriani, A., … Santoni, G. (2016). Cannabinoids synergize with carfilzomib, reducing multiple myeloma cells viability and migration. Oncotarget, 7, 77543–77557.
- Nakajima, Y., Furuichi, Y., Biswas, K. K., Hashiguchi, T., Kawahara, K., Yamaji, K., … Maruyama, I. (2006). Endocannabinoid, anandamide in gingival tissue regulates the periodontal inflammation through NF-kappaB pathway inhibition. FEBS Letters, 580, 613–619.
- Napimoga, M. H., Benatti, B. B., Lima, F. O., Alves, P. M., Campos, A. C., Pena-Dos-Santos, D. R., … Guimaraes, F. S. (2009). Cannabidiol decreases bone resorption by inhibiting RANK/RANKL expression and pro-inflammatory cytokines during experimental periodontitis in rats. International Immunopharmacology, 9, 216–222.
- Nogueira-Filho, G. R., Todescan, S., Shah, A., Rosa, B. T., Tunes Uda, R., & Cesar Neto, J. B. (2011). Impact of cannabis sativa (marijuana) smoke on alveolar bone loss: A histometric study in rats. Journal of Periodontology, 82, 1602–1607.
- Onaivi, E. S. (2009). Cannabinoid receptors in brain: Pharmacogenetics, neuropharmacology, neurotoxicology, and potential therapeutic applications. International Review of Neurobiology, 88, 335–369.
- Osazuwa-Peters, N., Adjei-Boakye, E., Loux, T. M., Varvares, M. A., & Schootman, M. (2016). Insufficient evidence to support or refute the association between head and neck cancer and marijuana use. Journal of Evidence-Based Dental Practice, 16, 127–129.
- Ossola, C. A., Surkin, P. N., Mohn, C. E., Elverdin, J. C., & Fernandez-Solari, J. (2016). Anti-inflammatory and osteoprotective effects of cannabinoid-2 receptor agonist HU-308 in a rat model of lipopolysaccharide-induced periodontitis. Journal of Periodontology, 87, 725–734.
- Paradisi, A., Pasquariello, N., Barcaroli, D., & Maccarrone, M. (2008). Anandamide regulates keratinocyte differentiation by inducing DNA methylation in a CB1 receptor-dependent manner. Journal of Biological Chemistry, 283, 6005–6012.
- Pertwee, R. G., Howlett, A. C., Abood, M. E., Alexander, S. P., Di Marzo, V., Elphick, M. R., … Ross, R. A. (2010). International Union of Basic and Clinical Pharmacology. LXXIX. Cannabinoid receptors and their ligands: Beyond CB(1) and CB(2). Pharmacological Reviews, 62, 588–631.
- Pirino, C., & Cappai, M. G. (2018). The presence and distribution of cannabinoid type 1 and 2 receptors in the mandibular gland: The influence of different physical forms of diets on their expression in piglets. Journal of Animal Physiology and Animal Nutrition, 102, e870–e876.
- Pisanti, S., Malfitano, A. M., Ciaglia, E., Lamberti, A., Ranieri, R., Cuomo, G., … Bifulco, M. (2017). Cannabidiol: State of the art and new challenges for therapeutic applications. Pharmacology & Therapeutics, 175, 133–150.
- Preet, A., Ganju, R. K., & Groopman, J. E. (2007). Δ9-Tetrahydrocannabinol inhibits epithelial growth factor-induced lung cancer cell migration in vitro as well as its growth and metastasis in vivo. Oncogene, 27, 339–346.
- Prestifilippo, J. P., Fernandez-Solari, J., de la Cal, C., Iribarne, M., Suburo, A. M., Rettori, V., … Elverdin, J. C. (2006). Inhibition of salivary secretion by activation of cannabinoid receptors. Experimental Biology and Medicine, 231, 1421–1429.
- Prestifilippo, J. P., Fernandez-Solari, J., Medina, V., Rettori, V., & Elverdin, J. C. (2009). Role of the endocannabinoid system in ethanol-induced inhibition of salivary secretion. Alcohol and Alcoholism, 44, 443–448.
- Prestifilippo, J. P., Medina, V. A., Mohn, C. E., Rodriguez, P. A., Elverdin, J. C., & Fernandez-Solari, J. (2013). Endocannabinoids mediate hyposalivation induced by inflammogens in the submandibular glands and hypothalamus. Archives of Oral Biology, 58, 1251–1259.
- Que, K., He, D., Jin, Y., Wu, L., Wang, F., Zhao, Z., … Deng, J. (2017). Expression of cannabinoid type 1 receptors in human odontoblast cells. Journal of Endodontics, 43, 283–288.
- Rees, T. D. (1992). Oral effects of drug-abuse. Critical Reviews in Oral Biology & Medicine, 3, 163–184.
- Rosenblatt, K. A., Daling, J. R., Chen, C., Sherman, K. J., & Schwartz, S. M. (2004). Marijuana use and risk of oral squamous cell carcinoma. Cancer Research, 64, 4049–4054.
- Ryberg, E., Larsson, N., Sjogren, S., Hjorth, S., Hermansson, N. O., Leonova, J., … Greasley, P. J. (2007). The orphan receptor GPR55 is a novel cannabinoid receptor. British Journal of Pharmacology, 152, 1092–1101.
- Shariff, J. A., Ahluwalia, K. P., & Papapanou, P. N. (2017). Relationship between frequent recreational cannabis (Marijuana and Hashish) use and periodontitis in adults in the United States: National health and nutrition examination survey 2011 to 2012. Journal of Periodontology, 88, 273–280.
- Szabo, B., & Schlicker, E. (2005). Effects of cannabinoids on neurotransmission. Handbook of Experimental Pharmacology, (168), 327–365.
- Theocharis, S., Giaginis, C., Alexandrou, P., Rodriguez, J., Tasoulas, J., Danas, E., … Klijanienko, J. (2016). Evaluation of cannabinoid CB1 and CB2 receptors expression in mobile tongue squamous cell carcinoma: Associations with clinicopathological parameters and patients' survival. Phytotherapy Research, 37, 3647–3656.
- Thomson, W. M. (2008). Cannabis smoking and periodontal disease among young adults. JAMA, 299, 525.
- Thoungseabyoun, W., Tachow, A., Pakkarato, S., Rawangwong, A., Krongyut, S., Sakaew, W., … Hipkaeo, W. (2017). Immunohistochemical localization of cannabinoid receptor 1 (CB1) in the submandibular gland of mice under normal conditions and when stimulated by isoproterenol or carbachol. Journal of Animal Physiology and Animal Nutrition, 81, 160–166.
- Tsumura, M., Sobhan, U., Muramatsu, T., Sato, M., Ichikawa, H., Sahara, Y., … Shibukawa, Y. (2012). TRPV1-mediated calcium signal couples with cannabinoid receptors and sodium-calcium exchangers in rat odontoblasts. Cell Calcium, 52, 124–136.
- Versteeg, P. A., Slot, D. E., van der Velden, U., & van der Weijden, G. A. (2008). Effect of cannabis usage on the oral environment: A review. International Journal of Dental Hygiene, 6, 315–320.
- Whyte, L. S., Ryberg, E., Sims, N. A., Ridge, S. A., Mackie, K., Greasley, P. J., … Rogers, M. J. (2009). The putative cannabinoid receptor GPR55 affects osteoclast function in vitro and bone mass in vivo. Proceedings of the National Academy of Sciences of the United States of America, 106, 16511–16516.
- Yoshida, R., Niki, M., Jyotaki, M., Sanematsu, K., Shigemura, N., & Ninomiya, Y. (2013). Modulation of sweet responses of taste receptor cells. Seminars in Cell & Developmental Biology, 24, 226–231.
- Yoshida, R., Ohkuri, T., Jyotaki, M., Yasuo, T., Horio, N., Yasumatsu, K., … Ninomiya, Y. (2010). Endocannabinoids selectively enhance sweet taste. Proceedings of the National Academy of Sciences of the United States of America, 107, 935–939.
