Chapter 2 Cancer

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Chapter 2CancerIntroduction39Lung Cancer42Conclusions of Previous Surgeon General’s Reports 43Biologic Basis 43Epidemiologic Evidence 48Changes in Relative Risks Following Smoking CessationChanging Characteristics of Cigarettes 49Lung Cancer Histopathology 59Evidence Synthesis 61Conclusions 61Implications 61Laryngeal Cancer62Conclusions of Previous Surgeon General’s ReportsBiologic Basis 62Epidemiologic Evidence 62Evidence Synthesis 62Conclusions 62Implications 62Oral Cavity and Pharyngeal Cancers63116Conclusions of Previous Surgeon General’s ReportsBiologic Basis 117Epidemiologic Evidence 118Evidence Synthesis 119Conclusions 119Implications 119Pancreatic Cancer6263Conclusions of Previous Surgeon General’s ReportsBiologic Basis 64Epidemiologic Evidence 65Evidence Synthesis 67Conclusion 67Implications 67Esophageal Cancer48116136Conclusions of Previous Surgeon General’s ReportsBiologic Basis 136Epidemiologic Evidence 137136Cancer35

Surgeon General’s ReportEvidence SynthesisConclusion 137Implications 137137Bladder and Kidney Cancers166Conclusions of Previous Surgeon General’s ReportsBiologic Basis 166Epidemiologic Evidence 166Evidence Synthesis 167Conclusion 167Implication 167Cervical Cancer167Conclusions of Previous Surgeon General’s ReportsBiologic Basis 168Epidemiologic Evidence 168Evidence Synthesis 170Conclusion 170Implication 170Ovarian CancerConclusions of Previous Surgeon General’s ReportsBiologic Basis 173Epidemiologic Evidence 173Evidence Synthesis 173Conclusion 173Implication 173178208Conclusions of Previous Surgeon General’s ReportsBiologic Basis 210Animal Models 211Epidemiologic Evidence 211Chapter 2172178Conclusions of Previous Surgeon General’s ReportsBiologic Basis 180Epidemiologic Evidence 181Evidence Synthesis 182Conclusions 183Implications 18336171172Endometrial CancerColorectal Cancer168171Conclusions of Previous Surgeon General’s ReportsBiologic Basis 171Epidemiologic Evidence 171Evidence Synthesis 172Conclusion 172Implication 172Stomach Cancer166209

The Health Consequences of SmokingEvidence SynthesisConclusion 215Implications 215213250Prostate CancerConclusions of Previous Surgeon General’s ReportsBiologic Basis 250Epidemiologic Evidence 250Other Data 251Evidence Synthesis 252Conclusions 252Implications 252252Acute LeukemiaConclusions of Previous Surgeon General’s ReportsBiologic Basis 252Epidemiologic Evidence 253Evidence Synthesis 254Conclusions 254Implications 254Liver Cancer252296Conclusions of Previous Surgeon General’s ReportsBiologic Basis 296Epidemiologic Evidence 296Evidence Synthesis 297Conclusion 297Implications 297Adult Brain Cancer296302Conclusions of Previous Surgeon General’s ReportsBiologic Basis 302Epidemiologic Evidence 302Evidence Synthesis 303Conclusion 303Implications 303Breast Cancer250302303Conclusions of Previous Surgeon General’s Reports 303Biologic Basis 304Epidemiologic Evidence 305Cigarette Smoking and Breast Cancer Risk 305Genotype-Smoking Interactions 308Passive Smoking, Active Smoking, and Breast Cancer Risk 310Cigarette Smoking and Breast Cancer Hormone Receptor Status 311Cigarette Smoking and Breast Cancer Mortality 311Evidence Synthesis 312Conclusions 312Implications 312Cancer37

Surgeon General’s er 2

The Health Consequences of SmokingIntroductionSince the 1964 Surgeon General’s report, the evidence on active smoking and cancer has grown rapidly. In that first report, only cancers of the lung andlarynx in men were causally linked to cigarette smoking (U.S. Department of Health, Education, and Welfare [USDHEW] 1964). That list grew with subsequentreports to include more sites and to include cancers inwomen as well as in men.The topic of smoking and cancer was last addressed comprehensively in the 1990 SurgeonGeneral’s report on smoking cessation (U.S. Department of Health and Human Services [USDHHS] 1990)and in the 1982 report (USDHHS 1982), which focusedon cancer. The report on women and smoking(USDHHS 2001) also considered cancer, and this chapter builds from that report for several cancers. Thischapter reviews the evidence relating smoking to arange of cancers, some previously associated causallywith smoking and some for which substantial newevidence has become available since the 1990 reviewin the Surgeon General’s report on smoking cessation.For some less common cancers, little research has beenconducted and these cancer sites are not included inthis chapter. Lymphomas and multiple myeloma, skincancers, bone cancer, and testicular cancer were omitted because they have not been linked to smoking.Pediatric malignancies are also not discussed, since thisreport concerns active smoking rather than involuntary exposure to cigarette smoke in utero and afterbirth.The relationship between smoking and lung cancer in men was the first to be classified as causal, following a review by Surgeon General Luther L. Terry’scommittee in the landmark 1964 report (USDHEW1964). The many documented benefits from quittingsmoking include a large decline in the risk of lung cancer after cessation compared with the risk from continuing smoking (USDHEW 1979; USDHHS 1989,1990). There is now equally convincing evidence thatsmoking causes cancer at a number of other sites forwhich causal conclusions had not been previouslyreached.Previous Surgeon General’s reports have concluded that smoking causes cancer in several organsites. The list of cancers caused by smoking has included cancers of the urinary bladder, esophagus, kidney, larynx, lung, oral cavity, and pancreas. The pastconclusions are detailed in the text that follows andare summarized in Table 2.1. The International Agencyfor Research on Cancer (IARC) has also reviewed theevidence on tobacco and cancer on two occasions, in1986 and again in 2002 (IARC 1986, 2002). The systemused by IARC differs from that applied in the SurgeonGeneral’s reports, but conclusions have generally beensimilar.The powerful epidemiologic evidence on smoking and lung cancer reported during the 1950s was oneof the first warnings of the strength of smoking as acause of cancer and other diseases (Doll and Hill 1954,1956). That warning was soon followed by the rise oflung cancer in women and the epidemic of otherchronic diseases caused by smoking. The past decadehas seen a rapid expansion of the application of molecular markers to complement traditional epidemiologic approaches to the study of smoking and cancer.This evolving field allows a clearer demonstration ofthe etiologic pathways from exposure to tobacco smoketo malignant transformation of target cells, and is discussed in relation to lung cancer as a model of thegrowing insights into the causal pathways from smoking to cancer.The overall contribution of smoking to diseaseand death continues to demand attention as excessmortality attributable to smoking maintains its rise.Cancer represents a substantial proportion of thiscontribution. An analysis of the two American CancerSociety (ACS) prospective cohort studies (Cancer Prevention Study I [CPS-I] and II [CPS-II]) by Thun andcolleagues (1995), shows that the risk of prematuremortality from smoking (death before 70 years of age)doubled in women and continued to rise in men during the interval (the 1960s to the 1980s) that separatesthese two cohorts. The contribution of lung cancer andother cancers to this excess in premature mortality wassubstantial. Annual death rates from lung cancer forwomen who were current smokers increased from 26.1to 154.6 per 100,000, and for men the increase was from187.1 to 341.3 per 100,000. Patterns varied by age. Therelative risks (RRs) of lung cancer changed from 11.9in CPS-I to 23.2 in CPS-II for men, and from 2.7 to 12.8for women. The percentages of lung cancer deaths attributable to smoking changed from 86 percent in CPSI to 90 percent in CPS-II for men, and from 40 percentto 79 percent for women (Thun et al. 1997a). Amongcurrent cigarette smokers overall, deaths attributableto cigarette smoking increased between CPS-I andCancer39

Surgeon General’s ReportTable 2.1Conclusions from previous Surgeon General’s reports concerning smoking as a cause ofcancer*Disease and statementSurgeon General’sreportBladder cancer“Epidemiological studies have demonstrated a significant association betweencigarette smoking and cancer of the urinary bladder in both men and women.These studies demonstrate that the risk of developing bladder cancer increaseswith inhalation and the number of cigarettes smoked.” (p. 75)1972“Epidemiological studies have demonstrated a significant association betweencigarette smoking and bladder cancer in both men and women.” (p. 1-17) “Cigarettesmoking acts independently and synergistically with other factors, such as occupational exposures, to increase the risk of developing cancer of the urinary bladder.”(p. 1-17)1979“A dose-response relationship has been demonstrated between cigarette smokingand cancer of the lung, larynx, oral cavity, and urinary bladder in women.” (p. 127)1980“Smoking is a cause of bladder cancer; cessation reduces risk by about 50 percentafter only a few years, in comparison with continued smoking.” (p. 178)1990Esophageal cancer“Epidemiological studies have demonstrated that cigarette smoking is associated withthe development of cancer of the esophagus.” (p. 12)1971“Cigarette smoking is a causal factor in the development of cancer of the esophagus,and the risk increases with the amount smoked.” (p. 1-17)1979“Cigarette smoking is causally associated with cancer of the lung, larynx, oral cavity,and esophagus in women as well as in men. . . .” (p. 126)1980“Cigarette smoking is a major cause of esophageal cancer in the United States.” (p. 7)1982Kidney cancer“Cigarette smoking is a contributory factor in the development of kidney cancer in theUnited States. The term ‘contributory factor’ by no means excludes the possibility ofa causal role for smoking in cancers of this site.” (p. 7)1982Laryngeal cancer“Evaluation of the evidence leads to the judgment that cigarette smoking is a significant factor in the causation of laryngeal cancer in the male.” (p. 37)1964“Cigarette smoking is causally associated with cancer of the lung, larynx, oral cavity,and esophagus in women as well as in men. . . .” (p. 126)1980*Words in boldface are for emphasis only and do not indicate emphasis in the original reports.40Chapter 2

The Health Consequences of SmokingTable 2.1ContinuedDisease and statementSurgeon General’sreportLung cancer“Cigarette smoking is causally related to lung cancer in men; the magnitude of theeffect of cigarette smoking far outweighs all other factors. The data for women,though less extensive, point in the same direction.” (p. 196)1964“Additional epidemiological, pathological, and experimental data not only confirmthe conclusion of the Surgeon General’s 1964 Report regarding lung cancer in menbut strengthen the causal relationship of smoking to lung cancer in women.” (p. 36)1967“Cigarette smoking is causally related to lung cancer in women. . . .” (p. 4)1968“Cigarette smoking is causally associated with cancer of the lung. . .in women as wellas in men. . . .” (p. 126)1980Oral cancer“Smoking is a significant factor. . .in the development of cancer of the oral cavity.”(p. 4)1968“Recent epidemiologic data strongly indicate that cigarette smoking plays anindependent role in the development of oral cancer.” (p. 59)1974“Epidemiological studies indicate that smoking is a significant causal factor in thedevelopment of oral cancer.” (p. 1-17)1979“Cigarette smoking is causally associated with cancer of the. . .oral cavity. . .in womenas well as in men. . . .” (p. 126)1980“Cigarette smoking is a major cause of cancers of the oral cavity in the United States.”(p. 6)1982Pancreatic cancer“Epidemiological evidence demonstrates a significant association between cigarettesmoking and cancer of the pancreas.” (p. 75)1972“Recent epidemiologic data confirm the association between smoking and pancreaticcancer.” (p. 59)1974“Cigarette smoking is related to cancer of the pancreas, and several epidemiologicalstudies have demonstrated a dose-response relationship.” (p. 1-17)1979“Cigarette smoking is a contributory factor in the development of pancreatic cancer inthe United States. The term ‘contributory factor’ by no means excludes the possibilityof a causal role for smoking in cancers of this site.” (p. 7)1982Sources: U.S. Department of Health, Education, and Welfare 1964, 1967, 1968, 1971, 1972, 1974, 1979; U.S. Department ofHealth and Human Services 1980, 1982, 1990.Cancer41

Surgeon General’s ReportCPS-II from 41.2 to 56.5 percent in men and from 16.7to 47.4 percent in women. Lung cancer accounted fora larger proportion of all-cause mortality in CPS-II, inpart reflecting the decline in cardiovascular diseasemortality.In contrast to these changes from the 1960s to the1980s, an analysis of the Surveillance, Epidemiology,and End Results (SEER) database indicates that therates of cancer began to decline from 1991 to the present(Ries et al. 2000a, 2003). The decline was observed inlarge part for smoking-related cancers (stomach, oralcavity, larynx, lung and bronchus, pancreatic, and bladder) (McKean-Cowdin et al. 2000). For each of thesecancers, both the incidence and the mortality ratesdeclined. Mortality also declined for cancer of the kidney, while incidence declined for cancer of the esophagus and for leukemia. These changes likely reflect, atleast in part, the decline in smoking among men and,to a lesser extent, among women, paralleling the earlier national decline in smoking.In developing this chapter, the literature reviewapproach was necessarily selective. For cancers forwhich a causal conclusion had been previouslyreached, there was no attempt to cover all relevant literature, but rather to focus on key issues or particularly important new studies for the site. For sites forwhich a causal conclusion had not been previouslyreached, a comprehensive search strategy was used.Lung CancerLung cancer was one of the first diseases to becausally linked to tobacco smoking. Although thereare causes of lung cancer other than tobacco smoking,lung cancer occurrence rates have served as a sentinelfor the epidemic of tobacco-caused diseases that began during the twentieth century because of the predominant causal role of smoking in these diseases.Across the early decades of the last century, cliniciansnoted the increase in lung cancer among their patients,and Ochsner and DeBakey (1939) speculated that cigarette smoking might be the cause in a case seriesreported in 1939. Although the possibility of an artifactual increase reflecting diagnostic bias was considered, by midcentury there was no doubt as to thepresence of an epidemic (Macklin and Macklin 1940).Lung cancer was therefore the focus of many early epidemiologic studies on smoking (White 1990; Doll etal. 1994) and one of the principal topics of the 1964Surgeon General’s report (USDHEW 1964), whichreached the momentous conclusion that smoking wasa cause of lung cancer (in men). Lung cancer mortality, which closely parallels incidence because of theextremely high case-fatality rate, is tracked in countries throughout the world and has provided a usefulanchoring and index point for estimating the burdenof tobacco-caused diseases (Peto et al. 1994). A decreasein lung cancer incidence and mortality rates has become evident among younger men in the United Statesand in other countries in the last 20 years, reflectingthe impact of efforts over decades to reduce smoking(Gilliland and Samet 1994; Wingo et al. 1999).42Chapter 2However, 40 years after smoking was first identified as a cause of lung cancer, it remains a leadingcause of cancer and of death from cancer. Lung canceraccounts for 28 percent of all cancer deaths in theUnited States (ACS 2003). In 2003, an estimated 171,900new cases of lung cancer were expected to be diagnosed in the United States, accounting for 13 percentof all cancer diagnoses, and an estimated 157,200deaths attributable to lung cancer were expected tooccur. In spite of vigorous research on therapy, survival remains poor with five-year survival of only 15percent for all stages of lung cancer combined (ACS2003). The age-adjusted annual incidence rate is declining steadily in men, from a high of 102.1 per 100,000in 1984 to 80.8 per 100,000 in 2000 (ACS 2003; Ries etal. 2003). In the 1990s, the rate of increase began toslow for women, but by 2000 the incidence rate amongwomen was 49.6 per 100,000 (Thun et al. 1997b; Wingoet al. 1999; Ries et al. 2003). During the 1990s deathsattributable to lung cancer declined significantly inmen, while mortality rates in women continued to increase. These changing patterns of incidence and mortality reflect temporal changes in smoking behaviorsamong U.S. adults that occurred decades ago (NationalCancer Institute [NCI] 1997). Smoking declined moreprecipitously among men than among women beginning in the 1950s, and the recent patterns of change inlung cancer rates reflect these earlier prevalence rates.Lung cancer refers to a histologically and clinically diverse group of malignancies arising in the respiratory tract, primarily but not exclusively in cells

The Health Consequences of Smokinglining the airways of the lung. The four principal types,classified by light microscopy and special stains, aresquamous cell carcinoma, small cell undifferentiatedcarcinoma, adenocarcinoma, and large cell carcinoma.Beginning at the trachea, the airways branch 20 or moretimes. Until recently, most cancers were believed tooriginate in the larger airways of the lung, typically atthe fourth through the eighth branches. However, therehas been a rise in the frequency of adenocarcinomassince the 1960s, which tend to develop in the peripheral lung (Churg 1994). The specific cells of origin ofthe different types of lung cancer are still unknown;candidates include the secretory cells, pluripotentialbasal cells, and the neuroepithelial cells (National Research Council [NRC] 1991, 1999).The rising incidence of lung cancer through thefirst half of the twentieth century prompted intensiveepidemiologic investigations of the disease, resultingin the identification of a number of causal agents(Samet 1994; Blot and Fraumeni 1996). Cigarette smoking is by far the largest cause of lung cancer, and theworldwide epidemic of lung cancer is attributablelargely to smoking. However, occupational exposureshave placed a number of worker groups at high risk,and some of these occupational agents are synergisticwith smoking in increasing lung cancer risks (Saracciand Boffetta 1994; IARC 2002). There is some evidencethat both indoor and outdoor air pollution also increaselung cancer risks generally (Samet and Cohen 1999).Observational evidence showing a familial aggregation of lung cancer has suggested that genetic factorsalso may determine risks in smokers, but the specificgenes remain under active investigation.Prior reports have fully described the variationof lung cancer risk with aspects of smoking (USDHHS1982, 1989, 1990, 2001). In smokers, the risk of lungcancer depends largely on the duration of smoking andthe number of cigarettes smoked (Samet 1996). Theexcess risks for smokers, compared with persons whohave never smoked, are remarkably high. Many studies provide RR estimates for developing lung cancerof 20 or higher for smokers compared with lifetimenonsmokers (USDHHS 1990; Wu-Williams and Samet1994). A risk-free level of smoking has not been identified, and even involuntary exposure to tobacco smokeincreases lung cancer risks for nonsmokers (USDHHS1986). Lung cancer risk decreases with successful cessation and maintained abstinence, but not to the levelof risk for those who have never smoked, even after15 to 20 years of not smoking (USDHHS 1990; NCI1997). Other aspects of smoking—depth of inhalationand the type of cigarettes smoked—have relativelysmall effects on risk once dur

Chapter 2 Cancer Introduction 39 Lung Cancer 42 Conclusions of Previous Surgeon General’s Reports 43 . smoking causes cancer at a number of other sites for which causal conclusions had not been previously . evidence on tobacco and cancer on two occasions, in 1986 and again in 2002 (IARC 1986, 2002). The system

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