Epidemiology
Determinants of the Excessive Rates
of Lung Cancer in Northeast Florida

By Kevin W. Wolfe, MD, FCCP

By the 1970s, Duval County (Jacksonville), Florida had the highest age-adjusted rate of lung cancer among white men of any metropolitan county in the country, exceeding the national level by nearly 50%.⁴ During the 1980s and 1990s, lung cancer became the leading cause of cancer death among women as well as men nationwide, with especially high rates arising among white women in Duval County. Rates among blacks, however, were near U.S. levels for black men and women.

It has long been recognized that cigarette smoking is the major preventable cause of lung cancer in the United States.^5,6 In 1999, the Heart and Lung Institute at St. Vincent's Medical Center (Jacksonville, FL) in association with the University of North Florida (Jacksonville, FL), the American Cancer Society (Atlanta, GA), and the International Epidemiology Institute (Rockville, MD) published results of a case-control study assessing whether smoking habits and/or other factors contributed to the exceptionally high rates of lung cancer in Duval County.¹²

Previous research⁴ had suggested some role for occupational exposures, but the emergence of parallel excesses of lung cancer in women as well as men suggested that exposures to hazardous occupational agents may not be the key factors. Air pollution in Jacksonville had not been considered excessive,^7-9 but the possibility of an effect on the area's respiratory cancer rates remained. Although it is often difficult to quantify exposure levels, some epidemiologic surveys have linked air pollution, especially from burning of fossil fuels, with increased risk of lung cancer.¹⁰ Research over the past two decades has also shown that diets low in fresh vegetables, fruits, and carotenoids are fairly consistently linked to increased risks of lung cancer,¹¹ but whether the dietary patterns of Jacksonville residents influenced the area's lung cancer rates was unknown. Genetic differences in susceptibility to carcinogenic agents have been identified and shown in part to underlie differing rates by racial or ethnic groups⁶ and perhaps could contribute to regional variation.

The Duval County Lung Cancer Study confirmed that cigarette smoking was the dominant cause of lung cancer among area residents.¹²

Indeed, 99% of the male patients and 94% of the female patients had at some time smoked tobacco. For smoking to account for Duval County's excessive rate of lung cancer, however, the prevalence of tobacco use (or the amount smoked) must be higher than that observed nationally and/or the effect of smoking must be more pronounced. Furthermore, the differences should vary by race, since the excess of lung cancer in Jacksonville over national rates is primarily limited to whites. Overall, among the control sample, with a median age slightly above 65 years, about 70% of white men and 50% of white women had smoked cigarettes, though most had quit. These prevalences of "ever smokers" among men and women in Duval County were higher, by up to 5%, than reported in U.S. government surveys of similarly aged whites in the early 1990s in randomly selected households throughout the country.¹³ The higher prevalence was mainly accounted for by more ex-smokers. After adjusting for age and education, the percentages of current smokers were about the same in Jacksonville as nationally, except for the city's black men, whose current smoking rate was considerably less than among black men across the country. In addition, among smokers the prevalence of heavy smoking (>25 cigarettes/day) was slightly higher in Jacksonville. Similar higher prevalences of smoking were also observed in an independent survey of a random sample of the Duval population ages 18 and older.¹⁴ Overall, these differences in smoking prevalence would be expected to yield a higher rate of lung cancer among whites in Jacksonville than nationally.

This study also found relative increases in risk of lung cancer among smokers, with odds ratios exceeding 60 in male and 30 in female current smokers, to be higher than usually reported.^5,6 The initial large-scale cohort studies of American smokers typically reported about a 10-fold increased risk of lung cancer in current smokers, though relative risks exceeded 20 for the heaviest smokers.

There is some suggestion that relative risks may be increasing, however. In the American Cancer Society (ACS) follow-up of nearly 1,000,000 participants into the 1990s, risks of lung cancer were 22 times higher in male current smokers than in lifelong nonsmokers, double the relative increase reported in the first ACS cohort study with follow-up mostly during the 1960s.¹⁵ Similarly, the most recent report from the 40-year cohort study of British physicians showed the excess risk among smokers to have doubled in the second vs. the first half of follow-up.¹⁶ The Duval County Lung Cancer Study relative risk estimates are higher still than those reported in these recent cohort studies, but the odds ratios have wide confidence limits and are sensitive to the small numbers of nonsmoking patients with lung cancer, especially among men. Indeed, addition of only a few cases into the nonsmoking category would substantially lower the odds ratios. Furthermore, those participating in the control group were more highly educated than the total Jacksonville and U.S. populations (bases on 1990 census data) and may have differed in other ways that relate to lower smoking, based on the control group used. This would also tend to inflate the odds ratios. Thus, we are reluctant to suggest that the high odds ratios estimated from the Duval County Lung Cancer Study survey truly reflect a greater hazard from smoking in Jacksonville than nationally.

In any case, the combination of the differences observed in smoking prevalence and in relative risks associated with smoking would be expected to produce a rate of lung cancer in Jacksonville among whites (but not blacks) that is considerably higher than the U.S. rate. This would appear to account for most if not all of the excessive risk of lung cancer among white men and women in Duval County. Indeed, based on calculations of attributable risk, it is estimated that 94% of all lung cancers among men and 88% among women are due to use of tobacco (predominantly cigarettes). These figures are higher than the 90% and 79% of lung cancer among American men and women, respectively, listed by the U.S. Surgeon General as attributable to smoking for the 1980s.⁵

No uniform rise in risk of lung cancer was observed with increasing duration of residence in Jacksonville. Risks were lower among the shortest-term residents (<10 years), but little trend was seen thereafter in either men or women. The odds ratios tended to decline with increasing length of residence. In other parts of Florida many residents are part-time, maintaining a second residence outside the state. Although this is less common in North Florida, including Jacksonville, it is conceivable that some cases among shorter-term part-time residents may have been diagnosed and treated in other states or may have been more difficult to locate for interview and thus missed in this study. Such selective elimination would be less likely to affect controls and would result in lower odds ratios among short-term residents. Explanations for the highest odds ratios being among women residing in Jacksonville for 10 to 20 years, and declines with longer residence (and no increased risk for >40-year residents), are not clear. The pattern is concordant with the excessive rate of lung cancer among area women becoming apparent mainly in the past 20 years, with less of an excess in earlier years.

Examination of within-county geographic variation in risk revealed no hints that lung cancer affects some broad regions of the Jacksonville community much differently than other regions. Earlier investigation by the community task force of lung cancer mortality rates across 14 regions of Duval County also failed to detect significant clustering of excessive rates.¹⁷ The residential/industrial mix of the areas does differ, with higher concentrations of larger manufacturing sites, including those with the heaviest particulate emissions, in the northern sectors, but differences in cancer rates across quadrants or neighborhoods were small and not consistent between men and women. A historical record of air quality revealed little evidence of noncompliance with federal standards for six criteria pollutants from 1966 through 1990.⁸

It is notable that the listing of the top 50 metropolitan areas of the country ranked by particulate matter (PM10) concentration from 1990 to 1994 did not include Jacksonville.⁹

Although workplace exposures may have been involved in some lung cancers, no major role of occupational factors was seen in this study. Heavy industry is uncommon in Jacksonville, and risks of  lung cancer were about the same among those employed vs. those not employed or with long-term employment in manufacturing industries. Case-control studies of lung cancer conducted in the late 1970s in Duval County⁴ and neighboring coastal Georgia¹⁸ revealed significant increases in risk among men associated with employment in the shipbuilding industry, which flourished in the area during World War II. The impact of such exposures now appears to have diminished, with no increase in risk observed among the small percentage of men with 10 or more years of employment in shipbuilding and repair. A small increased risk was seen among construction workers, consistent with earlier observations,⁴ but the excess was not significant and could not account for the area's high rates of lung cancer.

Several dietary correlates of risk were observed. Space limitations preclude detailed description in this report of the multiple diet and nutrition variables examined, but the general dietary habits of the lung cancer patients and the controls differed significantly. One of the most notable differences concerned fat intake, with nearly doubled risks among those with high vs. low percent of caloric intake from fat.

The findings are in line with those recently reported from investigations of lung cancer elsewhere in the United States and abroad, implicating fat intake in lung cancer risk.^19,20

Despite the association with dietary fat, no excessive risk of lung cancer was found among those who were obese or had high weight for their height. Other studies have raised the possibility that risk is increased among those with lean body mass,^21,22 but this study found little such effect. Similar to most other lung cancer investigations,¹¹ risks were lower among those in the highest quartile of fruit and vegetable intake (corresponding to 5 or more servings per day), though little reduction was seen in men, and the trend among women was not statistically significant.

Similar to findings of other studies in high-risk areas,^6,23 the Duval County Lung Cancer Study revealed a familial component to lung cancer in Jacksonville, with nearly a doubled risk among those with a first-degree family member with lung (but not other) cancer. The prevalence of lung cancer in families for both cases and controls was particularly high, especially for women, in part reflecting the high underlying rate of this disease in the area. Indeed, 28% of the women with lung cancer reported a parent, sibling, or child with lung cancer. Data on the smoking habits, residences, or other characteristics of the relatives were not available, so genetic traits could not be separated from shared environmental exposures (e.g., smoking). Whilt it seems unlikely that genetic factors play a major role in Jacksonville's elevated lung cancer rates, the high prevalence of familial lung cancer does suggest the potential for some influence of inherited susceptibilities.

REFERENCES

1. Mason TJ, Mackay FW, Hoover R, et al: Atlas of Cancer Mortality for US Counties, 1950-69. Washington, DC; US Department of Health, Education, and Welfare; 1975. Publication No. 75-78.
2. Pickle LW, Mason TJ, Howard M, et al: Atlas of US Cancer Mortality Among Whites 1950-80. Washington, DC: US Department of Health and Human Services; 1987. Publication No. 87-2900
3. Riggin WB, VanBruggen J, Acquavella JF, et al: US Cancer Mortality rates and Trends 1950-79. Washington, DC; US Government Printing Office; 1983. EPA-600/1-83-015b
4. Blot WJ, Davies JE, Brown LM, et al: Occupation and the high risk of lung cancer in northeast Florida. Cancer 1982; 50:364-371
5. US Department of Health and Human Services: Reducing the Health Consequences of Smoking, 25 Years of Progress. A Report of the Surgeon General. Rockville, Md; US Department of Health and human Services; 1989. Publication No. 89-8411
6. Blot WJ, Fraumeni JF Jr: Cancer of the lung and pleura. Cancer Epidemiology and Prevention. Schottenfeld D, Fraumeni J Jr (eds). New York, Oxford University Press, 2^nd Ed., 1996, pp 637-665
7. Air Quality Division, Environmental Protection Board, Jacksonville, Fla: Environment Status Report. Jacksonville, Regulatory and Environmental Services Department, 1995, pp 6-16
8. Delumyea RD, Mackay T, Horowitz J: (1) Literature search for air quality studies conducted in Jacksonville, Florida, (2) Trends in air quality research in northeast Florida 1945-1995 and comparison of air quality in Jacksonville with nine other cities in the United States. Florida Scientist 1997; 60:166-192
9. Shprentz DS: Breath-Taking: Premature Mortality Due to Particulate Air Pollution in 239 American Cities. New York, National Resources Defense Council, 1996; pp 78-79
10. Shy C: Air pollution. Cancer Epidemiology and Prevention. Schottenfeld D, Fraumeni JF Jr (eds). New York, Oxford University Press, 2^nd Ed, 1996, pp 406-417
11. Steinmetz KA, Potter JD: Vegetables, fruit, and cancer: I. Epidemiology. Cancer Causes Control 1991; 2:325-357
12. Tousey PM, Wolfe KW, Mozelleski A, et al: Determinants of the Excessive Rates of Lung Cancer in Northeast Florida. South Med J 1999; 92 (No. 5): 493-501
13. Giovino GA, Schooley MW, Zhu B-P, et al: Surveillance for selected tobacco-use behaviors _ United States, 1900-1994. CDC Surveillance Summaries, November 18, 1994. MMWR 1994: 43(No. SS-3):8-15
14. Sa P, Tousey PM, Blot WJ, et al: Tobacco smoking: a survey in a community with excess lung cancer. South Med J 1997; 90:601-605.
15. Thun M, Day-Lally CA, Calle EE, et al: Excess mortality among cigarette smokers: changes in a 20-year interval. Am J Public Health 1995; 85:1220-1223
16. Doll R, Peto R, Wheatley K, et al: Mortality in relation to smoking: 40 years observation on male British doctors. BJM 1994: 309:901-911
17. Wolfe KW: Lung cancer in Duval County: the Duval County lung cancer study. Jacksonville Med 1994; 45:177-182
18. Blot WJ, Harrington JM, Toledo A, et al: Lung cancer after employment in shipyards during World War II. N Engl J Med 1978; 299:620-624
19. Wynder EL, Hebert JR, Kabat GC: Association of dietary fat and lung cancer. J Natl Cancer Inst 1987; 79:631-637.
20. Alavanja M, Brown C, Swanson C, et al: Saturated fat intake and lung cancer risk among nonsmoking women in Missouri. J Natl Cancer Inst 1993; 85:1906-1916
21. Goodman MT, Wilkens LR: Relation of body size and risk of lung cancer. Nutr Cancer 1993; 20:179-186
22. Drinkard CR, Sellers TA, Potter JD, et al: Association of body mass index and body fat distribution with risk of lung cancer in older women. Am J Epidemiol 1995; 142:600-607
23. Ooi WL, Elston RC, Chen VW, et al: Increased familial risk for lung cancer. J Natl Cancer Inst 1986; 76:217-222

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