Effects of marijuana smoking on the lung

Annals of the American Thoracic Society

Volumn 10, Issue 3, 2013, Pages 239-247

  Tashkin, Donald P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chronic bronchitis; Chronic obstructive lung disease; Lung cancer; Lung function; Marijuana

Indexed keywords

CANNABINOID 1 RECEPTOR; CANNABIS; CARBON MONOXIDE; CARCINOGEN; COCARCINOGEN; INDUCIBLE NITRIC OXIDE SYNTHASE; ISOPRENALINE; METHACHOLINE; NITROSAMINE; PHENOL DERIVATIVE; POLYCYCLIC AROMATIC HYDROCARBON; REACTIVE OXYGEN METABOLITE; TOBACCO SMOKE; VINYL CHLORIDE;

ACETYLCHOLINE RELEASE; AIRWAY CONDUCTANCE; AIRWAY RESISTANCE; ARTICLE; ASPERGILLUS FUMIGATUS; ASTHMA; BACTERICIDAL ACTIVITY; BRONCHODILATATION; BRONCHOSPASM; BRONCHUS TONE; CANCER RISK; CANNABIS SMOKING; CARCINOGENIC ACTIVITY; CELL HYPERPLASIA; CHEST TIGHTNESS; CHRONIC BRONCHITIS; CHRONIC COUGH; CHRONIC GRANULOMATOUS DISEASE; CHRONIC OBSTRUCTIVE LUNG DISEASE; COMPUTER ASSISTED TOMOGRAPHY; DYSPNEA; FOLLOW UP; FUNCTIONAL RESIDUAL CAPACITY; FUNGICIDAL ACTIVITY; GOBLET CELL; HEALTH MAINTENANCE ORGANIZATION; HOST RESISTANCE; HUMAN; IMMUNOHISTOLOGY; INFECTION RISK; KIDNEY TRANSPLANTATION; LOWER RESPIRATORY TRACT INFECTION; LUNG ALVEOLUS MACROPHAGE; LUNG BAROTRAUMA; LUNG CANCER; LUNG COMPLICATION; LUNG FUNCTION; LUNG INFECTION; LUNG PARENCHYMA; LUNG STRUCTURE; LUNG TUBERCULOSIS; LUNG VOLUME; MUCOCILIARY CLEARANCE; NEBULIZER; NERVE ENDING; NITROGEN WASHOUT; NONHUMAN; PNEUMOMEDIASTINUM; PNEUMOTHORAX; RESPIRATORY FUNCTION; SMOKING; SPONTANEOUS PNEUMOTHORAX; SQUAMOUS CELL METAPLASIA; TOBACCO; TOTAL LUNG CAPACITY; TREATMENT DURATION; VALSALVA MANEUVER; WHEEZING;

EID: 84880854553     PISSN: 23256621     EISSN: None     Source Type: Journal    
DOI: 10.1513/AnnalsATS.201212-127FR     Document Type: Article

References (89)

1. Johnston LD, O'Malley PM, Bachman JG, Schulenberg JE. Monitoring the future: national results on adolescent drug use. Overview of key findings, 2011. Ann Arbor: Institute for Social Science Research, University of Michigan; 2012.
2. Hoffmann D, Brunneman DK,GoriGB, Wynder EL. On the carcinogenicity of marijuana smoke. Recent Adv Phytochem 1975;9:63-81.
3. Novotny M, Merli F, Weisler D, Fencl M, Saeed T. Fractionation and capillary gas chromatographic mass spectrometric characterization of the neutral components in marijuana and tobacco smoke concentrates. J Chromatogr A 1982;238:141-150.
4. Nadel JA, Comroe JH Jr. Acute effects of inhalation of cigarette smoke on airway conductance. J Appl Physiol 1961;16:713-716.
5. Tashkin DP, Shapiro BJ, Frank IM. Acute pulmonary physiologic effects of smoked marijuana and oral Δ9-tetrahydrocannabinol in healthy young men. N Engl J Med 1973;289:336-341.
6. Vachon L, Fitzgerald, Solliday NH, Gould IA, Gaensler EA. Single-dose effect of marijuana smoke: bronchial dynamics and respiratory-center sensitivity in normal subjects. N Engl J Med 1973;288: 985-989.
7. Tashkin DP, Shapiro BJ, Frank IM. Acute effects of smoked marijuana and oral Δ9-tetrahydrocannabinol on specific airway conductance in asthmatic subjects. Am Rev Respir Dis 1974;109:420-428.
8. Tashkin DP, Shapiro BJ, Frank IM. Acute effects of marihuana on airway dynamics in spontaneous and experimentally induced bronchial asthma. In: Braude M, Szara S, editors. Pharmacology of marihuana. New York: Raven Press; 1976, pp. 785-801.
9. Calignano A, Katona I, Desarnaud F, Giuffrida A, La Rana G, Mackie K, Freund TF, Piomelli D. Bidirectional control of airway responsiveness by endogenous cannabinoids. Nature 2000;408:96-101.
10. Grinspoon L. Marijuana. Sci Am 1969;221:17-25.
11. Roy PE, Magnan-Lapointe F, Huy ND, Boulet M. Chronic inhalation of marijuana and tobacco smoke in dogs: pulmonary pathology. Res Commun Chem Pathol Pharmacol 1976;14:305-317.
12. Fleischman RW, Baker JR, Rosenkrantz H. Pulmonary pathologic changes in rats exposed to marihuana smoke for 1 year. Toxicol Appl Pharmacol 1979;47:557-566.
13. Fleischman RW, Hayden DW, Braude MC, Rosenkrantz H. Chronic marihuana inhalation toxicity in rats. Toxicol Appl Pharmacol 1975; 34:467-478.
14. Fliegiel SEG, Beals TF, Tashkin DP, Paule MG, Scallet AC, Ali SF, Bailey JR, Slikker W Jr. Marijuana exposure and pulmonary alterations in primates. Pharmacol Biochem Behav 1991;40: 637-642.
15. Huber GL, Mahajan VK. The comparative response of the lung to marihuana or tobacco smoke inhalation. In Chesher G, Consroe P, Musty R, editors. Marijuana: an international research report. Proceedings of the Melbourne Symposium on Cannabis, September 2-4, 1987. National Campaign against Drug Abuse Monograph Series No. 7, pp. 19-24. Canberra: Australian Government Publishing Service; 1987.
16. Wu T-C, Tashkin DP, Djahed B, Rose JE. Pulmonary hazards of smoking marijuana as compared with tobacco. N Engl J Med 1988; 318:347-351.
17. Tashkin DP, Coulson AH, Clark VA, Simmons M, Bourque LB, Duann S, Spivey GH, Gong H. Respiratory symptoms and lung function in habitual heavy smokers of marijuana alone, smokers of marijuana and tobacco, smokers of tobacco alone, and nonsmokers. Am Rev Respir Dis 1987;135:209-216.
18. Bloom JW, Kaltenborn WT, Paoletti P, Camilli A, Lebowitz MD. Respiratory effects of non-tobacco cigarettes. Br Med J (Clin Res Ed) 1987;295:1516-1518.
19. Polen MR, Sidney S, Tekawa IS, Sadler M, Friedman GD. Health care use by frequent marijuana smokers who do not smoke tobacco. West J Med 1993;158:596-601.
20. Taylor DR, Poulton R, Moffitt TE, Ramankutty P, Sears MR. The respiratory effects of cannabis dependence in young adults. Addiction 2000;95:1669-1677.
21. Aldington S, WilliamsM, NowitzM, Weatherall M, Pritchard A,McNaughton A, Robinson G, Beasley R. Effects of cannabis on pulmonary structure, function and symptoms. Thorax 2007;62:1058-1063.
22. Moore BA, Augustson EM, Moser RP, Budney AJ. Respiratory effects of marijuana and tobacco use in a US sample. J Gen Intern Med 2004;20:33-37.
23. Tan WC, Lo C, Jong A, Xing L, Fitzgerald MJ, Vollmer WM, Buist SA, Sin DD; Vancouver Burden of Obstructive Lung Disease (BOLD) Research Group. Marijuana and chronic obstructive lung disease-a population-based study. CMAJ 2009;180:814-820.
24. Tashkin DP, Simmons M, Tseng C-H. Impact of changes in regular use of marijuana and/or tobacco on chronic bronchitis. COPD 2012;9: 367-374.
25. Tashkin DP, Calvarese BM, Simmons MS, Shapiro BJ. Respiratory status of seventy-four habitual marijuana smokers. Chest 1980;78: 699-706.
26. Tashkin DP, Simmons MS, Sherrill D, Coulson AH. Heavy habitual marijuana smoking does not cause an accelerated decline in FEV1 with age. Am J Respir Crit Care Med 1997;155:141-148.
27. Hancox RJ, Poulton R, Ely M, Welch D, Taylor DR, McLachlan CR, Greene JM, Moffitt TE, Caspi A, Sears MR. Effects of cannabis on lung function: a population-based cohort study. Eur Respir J 2010; 35:42-47.
28. Stuart DG, Collings WD. Comparison of vital capacity and maximum breathing capacity of athletes and nonathletes. J Appl Physiol 1959;14:507-509.
29. Pletcher MJ, Vittinghoff E, Kalhan R, Richman J, Safford M, Sidney S, Lin F, Kertesz S. Association between marijuana exposure and pulmonary function over 20 years. JAMA 2012;307:173-181.
30. Roth MD, Arora A, Barsky SH, Kleerup EC, Simmons M, Tashkin DP. Airway inflammation in young marijuana and tobacco smokers. Am J Respir Crit Care Med 1998;157:928-937.
31. Thompson AB, Huerta G, Robbins RA, Sisson JH, Spurzem JR, Von Essen S, Rickard KA, Romberger DJ, Rubinstein I, Ghafouri M, et al. The bronchitis index: a semiquantitative visual scale for the assessment of airways inflammation. Chest 1993;103: 1482-1488.
32. Fligiel SEG, Roth MD, Kleerup EC, Barsky SH, Simmons MS, Tashkin DP. Tracheobronchial histopathology in habitual smokers of cocaine, marijuana, and/or tobacco. Chest 1997;112:319-326.
33. Barbers RG, Gong H Jr, Tashkin DP, Oishi J, Wallace JM. Differential examination of bronchoalveolar lavage cells in tobacco cigarette and marijuana smokers. Am Rev Respir Dis 1987;135:1271-1275.
34. Sherman MP, Campbell LA, Gong H Jr, Roth MD, Tashkin DP. Antimicrobial and respiratory burst characteristics of pulmonary alveolar macrophages recovered from smokers of marijuana alone, smokers of tobacco alone, smokers of marijuana and tobacco and nonsmokers. Am Rev Respir Dis 1991;144:1351-1356.
35. Baldwin GC, Tashkin DP, Buckley DM, Park AN, Dubinett SM, Roth MD. Marijuana and cocaine impair alveolar macrophage function and cytokine production. Am J Respir Crit Care Med 1997;156: 1606-1613.
36. Shay AH, Choi R, Whittaker K, Salehi K, Kitchen CMR, Tashkin DP, Roth MD, Baldwin GC. Impairment of antimicrobial activity and nitric oxide production in alveolar macrophages from smokers of marijuana and cocaine. J Infect Dis 2003;187:700-704.
37. Auerbach O, Stout AP, Hammond ED, Garfinkel L. Changes in bronchial epithelium in relation to cigarette smoking and its relation to lung cancer. N Engl J Med 1961;265:253-267.
38. Barsky SH, Roth MD, Kleerup EC, Simmons M, Tashkin DP. Histopathologic and molecular alterations in bronchial epithelium in habitual smokers of marijuana, cocaine and/or tobacco. J Natl Cancer Inst 1998;90:1198-1205.
39. Taylor FM. Marijuana as a potential respiratory tract carcinogen: a retrospective analysis of a community hospital population. South Med J 1988;81:1213-1216.
40. Donald PJ. Advanced malignancy in the young marijuana smoker. Adv Exp Med Biol 1991;288:33-56.
41. Sridhar KS, Raub WA, Weatherby NL, Metsch LR, Surratt HL, Inciardi JA, Duncan RC, Anwyl RS, McCoy CB. Possible role of marijuana smoking as a carcinogen in the development of lung cancer at a young age. J Psychoactive Drugs 1994;26:285-288.
42. Endicott JN, Skipper P, Hernandez L. Marijuana and head and neck cancer. In: Friedman H, Klein TW, Spector S., editors. Drugs of abuse, immunity and AIDS. New York: Plenum Press; 1993, pp. 107-113.
43. Fung M, Gallagher C, Machtay M. Lung and aero-digestive cancers in young marijuana smokers. Tumori 1999;85:140-142.
44. Zhang Z-F, Morgenstern H, Spitz MR, Tashkin DP, Marshall JR, Hsu TC, Schantz SP. Marijuana use and increased risk of squamous cell carcinoma of the head and neck. Cancer Epidemiol Biomarkers Prev 1999;8:1071-1079.
45. Hsairi M, Achour N, Zouari B, Ben Romdhane H, Achour A, Maalej M, Nacef T. [Etiologic factors in primary bronchial carcinoma in Tunisia.] Tunis Med 1993;71:265-268.
46. Sasco AJ, Merill RM, Dari I, Benhaïm-Luzon V, Carriot F, Cann CI, Bartal M. A case-control study of lung cancer in Casablanca, Morocco. Cancer Causes Control 2002;13:609-616.
47. Sanchez C, de Ceballos ML, Gomez del Pulgar T, Rueda D, Corbacho C, Velasco G, Galve-Roperh I, Huffman JW, Ramón y Cajal S, Guzmán M. Inhibition of glioma growth in vivo by selective activation of the CB2 cannabinoid receptor. Cancer Res 2001;61:5784-5789.
48. De Petrocellis L, Melck D, Palmisano A, Bisogno T, Laezza C, Bifulco M, Di Marzo V. The endogenous cannabinoid anadamide inhibits human breast cancer cell proliferation. Proc Natl Acad Sci USA 1998;95:8375-8380.
49. Ruiz L, Miguel A, Diaz-Laviada I. Δ9-Tetrahydrocannabinol induces apoptosis in human prostate PC-3 cells via a receptorindependent mechanism. FEBS Lett 1999;458:400-404.
50. Portella G, Laezza C, Laccetti P, De Petrocellils L, Di Marzo V, Bifulco M. Inhibitory effects of cannabinoid DB1 receptor stimulation on tumor growth and metastatic spreading: actions on signals involved in angiogenesis and metastasis. FASEB J 2003;17:1771-1773.
51. Lisgresti A, Bisogno T, Matias I, De Petrocellis L, Cascio MG, Cosenza V, D'Argenio G, Scaglione G, Bifulco M, Sorrentini I, et al. Possible endocannabinoid control of colorectal cancer growth. Gastroenterology 2003;125:677-687.
52. Ligresti A, Moriello AS, Starowicz K, Matias I, Pisanti S, De Petrocellis L, Laezza C, Portella G, Bifulco M, Di Marzo V. Antitumor activity of plant cannabinoids with emphasis on the effect of cannabidiol on human breast cancer. J Pharmacol Exp Ther 2006;318:1375-1387.
53. Velasco G, Carracedo A, Blázquez C, Lorente M, Aguado T, Haro A, Sánchez C, Galve-Roperh I, Guzmán M. Cannabinoids and gliomas. Mol Neurobiol 2007;36:60-67.
54. Sarafaraz S, Afaq F, Adhami VM, Mukhtar H. Cannabinoid receptor as a novel target for the treatment of prostate cancer. Cancer Res 2005;65:1635-1641.
55. Olea-Herrero N, Vara D, Malagarie-Cazenave S, Diaz-Laviada I. Inhibition of human tumour prostate PC-3 cell growth by cannabinoids R(+)-methanandamide and JWH-015: involvement of CB2. Br J Cancer 2009;101:940-950.
56. Vara D, Salazar M, Olea-Herrero N, Guzman M, Velasco G, Diaz-Laviada I. Anti-tumoral action of cannabinoids on hepatocellular carcinoma: role of AMPK-dependent activation of autophagy. Cell Death Differ 2011;18:1099-1111.
57. Sidney S, Beck JE, Tekawa IS, Quesenberry CP, Friedman GD. Marijuana use and cancer incidence. Am J Public Health 1997;87: 585-590.
58. Rosenblatt KA, Daling JR, Chen C, Sherman KJ, Schwartz SM. Marijuana use and risk of oral squamous cell carcinoma. Cancer Res 2004;64:4049-4054.
59. Llewellyn CD, Linklater K, Bell J, Johnson NW, Warnakulasuriya S. An analysis of risk factors for oral cancer in young people: a case-control study. Oral Oncol 2004;40:304-313.
60. Llewellyn CD, Johnson NW, Warnakulasuriya AAS. Risk factors for oral cancer in newly diagnosed patients aged 45 years and younger: a case-control study in southern England. J Oral Pathol Med 2004; 33:525-532.
61. Hashibe M, Morgenstern H, Cui Y, Tashkin DP, Zhang Z-F, Cozen W, Mack TM, Greenland S. Marijuana use and the risk of lower and upper aerodigestive tract cancers: results of a population-based case-control study. Cancer Epidemiol Biomarkers Prev 2006;15: 1829-1834.
62. Aldington S, Harwood M, Cox B, Weatherall M, Beckert L, Hansell A, Pritchard A, Robinson G, Beasley R; Cannabis and Respiratory Disease Research Group. Cannabis use and risk of lung cancer: a case-control study. Eur Respir J 2008;31:280-286.
63. Sewell RA, Cohn AJ, Chawarski MC. Doubts about the role of cannabis in causing lung cancer [letter to the editor]. Eur Respir J 2008;32:815-816.
64. Klein TW, Cabral GA. Cannabinoid-induced immune suppression and modulation of antigen-presenting cells. J Neuroimmune Pharmacol 2006;1:50-64.
65. Ungerleider JT, Andrysiak T, Tashkin DP, Gale RP. Contamination of marihuana cigarettes with pathogenic bacteria-possible source of infection in cancer patients. Cancer Treat Rep 1982;66:589-591.
66. Kagen SL, Kurup VP, Sohnle PC, Fink JN. Marijuana smoking and fungal sensitization. J Allergy Clin Immunol 1983;71:389-393.
67. Denning DW, Follansbee SE, Scolaro M, Norris S, Edelstein H, Stevens DA. Pulmonary aspergillosis in the acquired immunodeficiency syndrome. N Engl J Med 1991;324:654-662.
68. Chusid MJ, Gelfland JA, Nutter C, Fauci AS. Pulmonary aspergillosis, inhalation of contaminated marijuana smoke, chronic granulomatous disease [letter]. Ann Intern Med 1975;82:682-683.
69. Hamadeh R, Ardehali A, Locksley RM, York MK. Fatal aspergillosis associated with smoking contaminated marijuana in a marrow transplant recipient. Chest 1988;94:432-433.
70. Sutton S, Lum BL, Torti FM. Possible risk of invasive pulmonary aspergillosis with marijuana use during chemotherapy for small cell lung cancer. Drug Intell Clin Pharm 1986;20:289-291.
71. Marks WH, Florence L, Lieberman J, Chapman P, Howard D, Roberts P, Perkinson D. Successfully treated invasive pulmonary aspergillosis associated with smoking marijuana in a renal transplant recipient. Transplantation 1996;61:1771-1783.
72. Munckhof WJ, Konstantinos A, Wamsley M, Mortlock M, Gilpin C. A cluster of tuberculosis associated with use of a marijuana water pipe. Int J Tuberc Lung Dis 2003;7:860-865.
73. Newell GR, Mansell PW, Wilson MB, Lynch HK, Spitz MR, Hersh EM. Risk factor analysis among men referred for possible acquired immune deficiency syndrome. Prev Med 1985;14:81-91.
74. Tindall B, Philpot CR, Cooper DA, Gold J, Donovan B, Penny R, Barnes T. The Sydney AIDS Project: development of acquired immunodeficiency syndrome in a group of HIV seropositive homosexual men. Aust N Z J Med 1988;18:8-15.
75. Caiaffa WT, Vlahov D, Graham NM, Astemborski J, Solomon L, Nelson KE, Muñoz A. Drug smoking, Pneumocystis carinii pneumonia, and immunosuppression increase risk of bacterial pneumonia in human immunodeficiency virus-seropositive infection drug users. Am Rev Respir Dis 1994;150:1493-1498.
76. Kaslow RA, Blackwelder WC, Ostrow DG, Yerg D, Palenicek J, Coulson AH, Valdiserri RO. No evidence for a role of alcohol or other psychoactive drugs in accelerating immunodeficiency in HIV-1- positive individuals: a report from the Multicenter AIDS Cohort Study. JAMA 1989;261:3424-3429.
77. Feldman AL, Sullivan JT, Passero MA, Lewis DC. Pneumothorax in polysubstance abusing marijuana and tobacco smokers: 3 cases. J Subst Abuse 1993;5:183-186.
78. Mattox KL. Pneumomediastinum in heroin and marijuana users. JACEP 1976;5:26-28.
79. Miller WE, Spiekerman RE, Hepper NG. Pneumomediastinum resulting from performing Valsalva maneuvers during marijuana smoking. Chest 1972;62:233-234.
80. Goodyear K, Laws D, Turner J. Bilateral spontaneous pneumothorax in a cannabis smoker. J R Soc Med 2004;97:435-436.
81. Herrejon SA, Blanquer OJ, Simo Mompo M, Ruiz Montalt F, Núñez Śanchez C, Chiner Vives E. [Pneumothorax due to drug inhalation.] Med Interna 1992;9:137-139.
82. Luque MA III, Cavallaro DL, Torres M, Emmanual P, Hillman JV. Pneumomediastinum, pneumothorax, and subcutaneous emphysema after alternate cocaine inhalation and marijuana smoking. Pediatr Emerg Care 1987;3:107-109.
83. Birrer RB, Calderon J. Pneumothorax, pneumomediastinum, and pneumopericardium following Valsalva's maneuver during marijuana smoking. N Y State J Med 1984;84:619-620.
84. Hazouard E, Koninck JC, Attucci S, Fauchier-Rolland F, Brunereau L, Diot P. Pneumorachis and pneumomediastinum caused by repeated Muller's maneuvers: complications of marijuana smoking. Ann Emerg Med 2001;38:694-697.
85. Johnson MK, Smith RP, Morrison D, Laszlo G, White RJ. Large lung bullae in marijuana smokers. Thorax 2000;55:340-342.
86. Phan TD, Lau KK, Li X. Lung bullae and pulmonary fibrosis associated with marijuana smoking. Australas Radiol 2005;49:411-414.
87. Thompson CS,White RJ. Lung bullae and marijuana. Thorax 2002;57:563.
88. Hii WS, Tam JDC, Thompson BR, Naughton MT. Bullous lung disease due to marijuana. Respirology 2008;13:122-127.
89. Tan C, Hatam N, Treasure T. Bullous disease of the lung and cannabis smoking: insufficient evidence for a causative link. J R Soc Med 2006;99:77-80.