 |
|
Head and Neck Cancer Incidence Trends in Young Americans, 1973-1997, With a Special Analysis for Tongue Cancer
Stimson P. Schantz, MD;
Guo-Pei Yu, MD
Arch Otolaryngol Head Neck Surg. 2002;128:268-274.
ABSTRACT
| |
Objective To examine the temporal changes in head and neck cancer in young adults
in the United States.
Methods Using the cancer surveillance database from the National Cancer Institute
Surveillance, Epidemiology, and End Results (SEER) Program, we calculated
age-adjusted incidence rates for head and neck cancers. Using the joinpoint
regression model, we described tongue cancer incidence trends and established
the statistical significance of temporal changes. We also compared changes
in 5-year survival rates for tongue cancer.
Results From 1973 to 1997, there were 63 409 patients with head and neck
cancer in the 9 SEER registries. Of these, 3339 patients were younger than
40 years. The incidence of head and neck cancer remained stable in groups
older than 40 years comparing the 1973-1984 and 1985-1997 data. In contrast,
tongue cancer in adults younger than 40 years increased approximately 60%
during the same period. We detected a significant increase until 1985, the
estimated annual percentage change being 6.7% (95% confidence interval, 2.7%-10.8%; P<.001). After 1985, incidence rates stopped rising
but remained steadily high. The change in tongue cancer incidence rates for
young adults was related to birth cohorts between 1938 and 1948. The absolute
increase in 5-year survival for tongue cancer ranged from 11.7% (<40 years
old) to 6.6% (40-64 years old) between 1973-1984 and 1985-1997, with the most
significant improvement occurring in young Americans with regional or distant
disease (27% and 21%, respectively).
Conclusions A sharp increasing trend in tongue cancer in young Americans may be
attributed to persons born after 1938. The reason for the increase is uncertain.
Improved survival rates in young patients suggest the emergence of a distinct
disease process that is apparent in white but not black populations.
INTRODUCTION
THE RESULTS of many studies1-7
suggest that head and neck cancer, particularly oral tongue cancer, is increasing
in young adults internationally. In the United States, Depue4
found an increase in the tongue cancer mortality rate in adults younger than
30 years. The increase was cited as beginning in the mid-1970s. In addition,
Chen et al7 reported that between the 1960s
and the mid-1980s, men aged 30 to 39 years had a nearly 4-fold increase in
oral cancer incidence in Connecticut. Results of a recent clinical analysis8 indicated that the percentage of young patients in
the total tongue cancer population seen at the M.D. Anderson Cancer Center
(Houston, Tex) increased from 4% in 1971 to 18% in 1993. Franchesci et al5 examined mortality trends from 24 European countries
based on death certificates recorded between 1955 and 1989. Ten countries
showed greater than a 2-fold increase in oral cancer for men younger than
44 years, and 3 countries showed a similar increase for women. The countries
represented in this increase were principally those in central Europe, including
Austria, Germany, Hungary, Poland, and Bulgaria.5
Because incidence rates for overall head and neck cancer have remained
stable and have even shown a declining trend since the 1970s,6, 9
the increase in the number of young adult patients is concerning. Factors
that may account for oral cancer in young adults remain unknown. Suspected
etiologic agents include smokeless tobacco,10-11
various forms of drug abuse,12 virus,13 and host susceptibility factors.14
However, no clear evidence exists to support the significance of any single
determinant, including the role of tobacco.15
The goal of this study is to update and confirm the changes of trend
in the incidence of young adult oral tongue cancer and other head and neck
cancers using a large cancer surveillance database in the United States. A
unique feature of our analysis is the use of a new statistical method, joinpoint regression, to describe incidence trends and
to establish the statistical significance of changes in trend.
MATERIALS AND METHODS
Data for the analysis were obtained from the Surveillance, Epidemiology,
and End Results (SEER) Program Public-Use CD-ROM (1973-1997) (National Cancer
Institute, Bethesda, Md, Division of Cancer Control and Population Sciences,
Cancer Surveillance Research Program, Cancer Statistics Branch, released April
2000) based on the August 1999 submission. We applied information on all head
and neck cancers diagnosed in the residents of 9 population-based registries,
ie, 5 states (Connecticut, Hawaii, Iowa, New Mexico, and Utah) and 4 standard
metropolitan statistical areas (Atlanta, Ga; Detroit, Mich; San Francisco–Oakland,
Calif; and Seattle–Puget Sound, Wash). These registries cover approximately
10% of the US population.
The SEER Program uses the International Classification
of Diseases for Oncology (second edition) to code site (topography),
histologic features (morphology), and behavior for all cancers.16
The site codes for tongue cancer cases used in this article are C019 (base
of tongue), C020 (dorsal surface of tongue), C021 (border of tongue), C022
(ventral surface of tongue), C023 (anterior of tongue), C024 (lingual tonsil),
C028 (overlapping lesion of tongue), and C029 (tongue, not otherwise specified).
Only tongue cancer cases considered to be invasive (malignant), that is, with
a behavior code of 3, are included in this analysis. Oral tongue cancers with
histologic codes 9590 to 9989 (lymphomas) were excluded. The site grouping
included in this analysis is consistent with that published previously by
the SEER Program.17 Between 1973 and 1997,
in SEER Program areas, there were 76 patients whose race was unknown with
tongue cancer. To keep the totality of cases, we included them to calculate
overall incidence and survival rates.
Incidence rates are expressed per 100 000 population and are age
adjusted using the direct method to the 1970 US population. We classified
incidence data into 3 age groups (<40, 40-64, and  65 years) and calculated
age-adjusted rates within the groups according to every calendar year from
1973 to 1997. To better describe tongue cancer data, we also calculated race-
and sex-specific age-adjusted incidence rates in 5-year intervals beginning
in 1973-1977 and extending to 1993-1997.
We applied the joinpoint regression model to characterize trends in
tongue cancer incidence to determine when the incidence started rising, when
it peaked, and the degree to which it has returned to the background trend
before the change.18-19 The approach
allows more flexible and accurate analyses in detecting temporal changes in
incidence over time, thus reducing the effect of possible variable observations.
In the joinpoint model, the response variables for analysis are the natural
logarithms of age-adjusted rates, and the independent variables are the calendar
years of diagnosis. For tongue cancer data, we coded the values of years as
0 to 24, representing a calendar year range from 1973 to 1997. We fitted the
heteroscedastic/uncorrelated error joinpoint model and conducted a series
of permutation tests based on 1000 Monte Carlo replicates. The models were
estimated by use of weighted least squares, with the weights proportional
to the inverse of variance of age-adjusted rates. For each hypothesized model,
the best-fitting joinpoints were found by use of a grid search algorithm.
In the courses, we first tested H0 (no joinpoints) vs H (3 joinpoints). The testing then proceeded sequentially and decreased
the number of joinpoints under the alternative hypothesis by 1 if 3 joinpoints
are insignificant. The statistics derived from these models are the estimated
annual percentage change (EAPC), 95% confidence intervals (CIs) for the EAPCs,
and any possible joinpoints (calendar years) at which there is a change in
the trends.
To explore the possible effects of birth cohort on tongue cancer incidence
rates over time, we calculated 5-year birth cohort incidence rates according
to the method of Robertson and Boyle.20 We
stratified the incidence data into 22 birth cohorts (1883-1887, 1888-1892,
. . . , 1983-1987, and 1988-1992), based on SEER Program data with 18 age
groups (0-4, 5-9, . . . , and 85 years) and 5 periods (1973-1977, 1978-1982,
. . . , and 1993-1997). All individuals 85 years and older were assumedly
classified as the 85- to 89-year-old group. In the stratification, each age
group was split into 2 constituent cohorts.
In this descriptive analysis, we further calculated sex-, race-, and
stage-specific 5-year relative survival rates according to 2 periods, 1973-1984
and 1985-1997. The analysis excluded patients with a tongue cancer diagnosed
as a second or later cancer, patients whose cancer was identified only by
a death certificate or autopsy report, and patients with unknown survival
time. Classification of tumor stage was based on the standard of SEER Program
historic stage A.21
RESULTS
The SEER Program reported 63 409 patients with head and neck cancer
(oral and pharynx: C000-C148) between 1973 and 1997. Of these, 3339 patients
were younger than 40 years. Between the 1973-1984 and 1985-1997 periods, the
overall incidence for head and neck cancer was stable. A slight decrease could
be seen in 1985-1997 in groups aged 40 to 64 years and 65 years and older.
However, the number of patients with head and neck cancer increased among
Americans younger than 40 years during the same period. The increase seemed
to be mainly caused by increased tongue cancer. Tongue cancer in young Americans
ranked second to salivary gland cancer in all head and neck cancers and increased
62% comparing 1985-1997 and 1973-1984. Laryngeal cancer showed no significant
change in incidence during the 2 periods (Table 1).
|
|
|
|
Table 1. Observed Incident Cases and Rates for Oral, Pharyngeal, and
Laryngeal Cancers by Age and Period, SEER Program, 1973-1997*
|
|
|
Table 2 gives race- and
sex-specific age-adjusted incidence rates for tongue cancer according to 3
age groups and five 5-year intervals. Overall age-adjusted rates significantly
increased in young Americans in both sexes. Rates increased only slightly
in men aged 40 to 64 years and in women 65 years and older. Age-adjusted incidence
increased almost 1-fold in the young white population during the past 25 years;
from 0.11 in 1973-1984 to 0.19 in 1985-1997 in young white men and from 0.06
to 0.10 in young white women. Rates fluctuated in the nonwhite population,
although an obvious upward incidence with time could be seen in young black
women.
|
|
|
|
Table 2. Race- and Sex-Specific Age-Adjusted Incidence Rates for Tongue
Cancer by Age and 5-Year Interval*
|
|
|
Figure 1 displays incidence
trends for tongue cancer and the fitting curves of the joinpoint regression
model. Incidence trends for young and old Americans changed at different rates.
In Americans younger than 40 years, there was a significant upward trend from
1973 through 1997 (Figure 1A). The
overall EAPC was 2.69 (95% CI, 1.4-4.1; P<.001)
during these 25 years. A sharp acceleration was seen from 1973 until 1985,
with the EAPC being 6.68 (95% CI, 2.7-10.8; P<.001).
The significant joinpoint was at the year 1985 (95% CI, 1979-1989). After
1985, the incidence stopped rising but remained steadily high (EAPC, 0.002;
95% CI, -2.7-2.9). In contrast to young Americans, however, the age-adjusted
incidence trends for Americans older than 40 years remained level (Figure 1B-C). The EAPCs in slope were 1.13
for the group aged 40 to 64 years and 0.31 for those 65 years and older from
1973 to 1997.
|
|
|
|
Figure 1. Age-adjusted tongue cancer incidence
rates per 100 000 population in 9 National Cancer Institute Surveillance,
Epidemiology, and End Results Program registries, 1973-1997, in Americans
younger than 40 years (A), 40 to 64 years (B), and 65 years and older (C).
The dotted line segments are obtained from the fits of the joinpoint regression
models. EAPC indicates estimated annual percentage change; CI, confidence
interval.
|
|
|
Examining changes in cohort-specific incidence rates by age groups show
increased incidence rates in individuals born between 1943-1947 in all workable
age groups (ie, 30-34, 35-39, 40-44, and 45-49 years) (Figure 2). The effect of birth cohort was particularly evident in
the incidence curve of the group aged 35 to 39 years. A large acceleration
began in the 1938-1942 cohort and peaked in the 1943-1947 cohort (Figure 2A). Cohorts born after 1947 also
showed an upward trend among Americans younger than 40 years. Although we
calculated cohort-specific rates for the group 65 years and older according
to subgroups aged 65 to 69 years, 70 to 74 years, 75 to 79 years, 80 to 84
years, and 85 years and older, we could not present these curves owing to
overlapping incidence rates. In the group 65 years and older, the earliest
birth cohort was 1883-1887 and the latest was 1923-1927; their incidence rates
were 8.35 and 8.43, respectively.
|
|
|
|
Figure 2. Tongue cancer incidence rates
per 100 000 population by age group and birth cohort, National Cancer
Institute Surveillance, Epidemiology, and End Results Program, 1973-1997.
A, Americans younger than 40 years. B, Americans aged 40 to 64 years.
|
|
|
Table 3 gives 5-year survival
rates for patients with tongue cancer by age group and period. During 1985-1997,
survival declined with increasing age: 70.6% for the group younger than 40
years, 49.8% for those aged 40 to 64 years, and 45.8% for those 65 years and
older. From 1973 to 1997, 5-year survival rates for tongue cancer increased
in all age groups. The absolute increase in survival was largest in Americans
younger than 40 years (11.7%; P = .009). Survival
improvement was more pronounced in young patients who were male, white, and
at an advanced tumor stage. However, survival rates somewhat decreased in
young nonwhite patients. Five-year relative survival in 1985-1997 for young
patients with local stage, regional stage, and distant stage tumor were 83.6%,
52.7%, and 44.3%, respectively. More than 20% survival improvement was seen
in young patients with regional or distant stage compared with data from 1973-1984.
The absolute increase in survival was only 3% in young patients with localized
disease. Among older Americans, the increased survival rates were similar
in different sexes, races, and stages, except for the black population aged
40 to 64 years, which showed a decreased survival rate.
|
|
|
|
Table 3. Sex-, Race-, and Stage-Specific 5-Year Survival for Patients
With Tongue Cancer by Age and Period*
|
|
|
Between 1973-1984 and 1985-1997, the stage distribution of tongue cancer
did not significantly change in the 3 age groups (Table 4). Fifty-five percent of young patients were at the localized
stage. The proportion of local-stage disease was approximately 30% to 40%
higher for younger patients than for older patients.
|
|
|
|
Table 4. Stage Distribution of Tongue Cancer by Age at Diagnosis and
Period*
|
|
|
COMMENT
The present study exhibits a significantly increased trend of tongue
cancer in Americans born after 1938. The acceleration began in 1973, peaked
in 1985, and subsequently has been stable. In contrast to oral tongue cancer,
the incidence rates of other head and neck cancers in younger Americans, such
as cancers of the pharynx and larynx, remained relatively stable during the
same period. The marked increase in tongue cancer in young Americans is particularly
impressive compared with the stable incidence in older populations. Tongue
cancer is a rare malignancy in young adults; therefore, we need to interpret
the trends with caution. We do not think that rate fluctuations, caused by
relatively small numbers in several single years, would change the direction
of the trend owing to true randomness. On the other hand, joinpoint regression
modeling actually accounts for the limited robustness of data and allows us
to improve accuracy in trend estimates. It seems unlikely that certain artefactual
factors, for instance, improved diagnostic methods, various screening activities,
and changes in tumor coding, have led to an increased incidence trend for
tongue cancer in young Americans. First, diagnostic methods have not significantly
changed for tongue cancer since the 1970s. Second, no specific screening strategies
for head and neck cancer in the SEER Program registries have existed during
the past 25 years. In addition, the SEER Program has not instituted any changes
in either anatomic or histologic coding.
Our analysis reveals that the most significant increase in tongue cancer
in young Americans was related to birth cohorts between 1938 and 1948. If
birth cohorts since 1938 are primarily responsible for the increase in young
adult tongue cancer, then a similar cohort-specific increase should also emerge
in other age groups as the population ages. In fact, we found an increase
in cohort-specific incidence rates in the age groups of 40 to 44 and 45 to
49 years when corresponding birth cohorts are available (Figure 2). This suggests that birth cohorts since 1938 may have
experienced a changing carcinogenic effect on the oral tongue, carcinogen(s)
distinct from those contained within tobacco. According to the National Health
Interview Survey, the prevalence of cigarette smoking has markedly decreased
among Americans since the mid-1960s.22 Similarly,
cigarette smoking prevalence among youths also declined sharply in the 1970s,
although the decline slowed significantly in the 1980s.23
Similar to cigarette smoking, alcohol use shows a decline since the 1970s.24-25 Results of other studies9, 26-27 indicate that smoking-related
cancers such as those of the lung, larynx, and oral cavity are actually declining
in North America. Age-specific analyses of lung cancer revealed that rates
in males first declined at younger ages and then for each older age group
successively over time.26 Our analysis of upper
aerodigestive tract cancers other than tongue cancer would support that conclusion
(Table 1). Thus, some time-dependent
factors associated with changing behavior and environmental exposures should
be reviewed in relation to the decreasing effect of tobacco use and alcohol
consumption.
One such factor may be smokeless tobacco use (moist snuff and chewing
tobacco). There has been strong evidence that smokeless tobacco can cause
oral cancer and precancerous oral lesions (leukoplakia).7, 28-31
Smokeless tobacco use has increased dramatically in the United States during
the past 30 years.28, 32 An unexplainable
fact, however, is that young American women showed significant increases in
tongue cancer from 1973 to 1997 but their prevalence of smokeless tobacco
use is extremely low, only 0.3%,33 and has
not significantly changed since the 1970s. Likewise, smokeless tobacco should
induce cancer in regions where it is held in contact, such as the cheek or
gum, but the incidence of these nontongue oral cancers has remained relatively
stable.
Another significant factor may be marijuana use. Approximately 31% of
the US population 12 years or older in 1992 had ever used marijuana.34 The prevalence of marijuana use sharply increased
in the United States in male and female teenagers and young adults in the
mid- to late-1960s, that is, in cohorts born between 1941 and 1955 (Figure 3).34-36
Assuming that marijuana use is associated with cancer risk with an induction
or latency period of 20 to 30 years, persons born between 1941 and 1955 will
be the earliest possible group to experience and clinically manifest elevated
risks of tongue cancer. The assumption seems consistent with our findings
(ie, a higher incidence of tongue cancer in birth cohorts beginning in 1938).
The carcinogenic effect of marijuana has been concluded from a series of case
report, laboratory, and experimental evidence.37-40
Recently, Zhang et al41 reported a dose-dependent
association between marijuana smoking and head and neck cancer risk. The risk
was more pronounced in young patients.41 However,
current studies could not prove causation between marijuana use and tongue
cancer; therefore, a well-designed study is necessary in the future.
|
|
|
|
Figure 3. Lifetime prevalence of marijuana
use in the US population according to birth cohort. Data from Johnson and
Gerstein.34
|
|
|
A third suspected factor may be human papillomavirus (HPV) infection.
There is evidence for the correlation of HPV infection with oral cavity carcinoma.42 Positivity for HPV in oral neoplastic tissues varies
from 14% to 91%.43-45
An approximately 5-fold higher expression of HPV can be seen in oral squamous
carcinoma than in normal oral mucosa.43 Two
types of HPV (types 16 and 18) seem to be carcinogenic and show a close correlation
with p53 mutation.46 Results of laboratory
studies show that HPV integration into the oral epithelial cell genome will
lead to cellular immortalization and set the stage for enhancing the carcinogenic
potential of relevant chemical compounds.47
To date, however, we are not clear whether HPV infection increases over time
in young Americans, and the increase is one of the responsible factors for
the rising trend of oral tongue cancer.
In our analysis, the stage and survival characteristics of tongue cancer
in individuals born since the early 1940s suggest a distinct disease process.
In these younger Americans, the disease typically presents itself in earlier
stages and is associated with a higher 5-year determinant survival rate than
in older adults. This observation supports the conclusions of Lacy et al,48 who, likewise, concluded in their analysis of a hospital
registry that young adults have a more favorable disease process. Approximately
56% of the young adults in the SEER Program presented with localized disease
compared with 37% and 43% localized disease in the 40 to 64 year olds and
those 65 years and older, respectively. We found that 5-year survival of 70.5%
in young patients in 1985-1997 reported by 9 SEER Program registries was comparable
with that seen in several other hospital-based observations.8, 49-50
The 5-year survival rate did not appreciably change in young patients with
localized disease between 1973-1984 and 1985-1997. In contrast, 5-year survival
has improved more than 20% in young patients with regional and metastatic
disease. The improved survival rate and earlier staged disease were not observed
in the young black population, which has a dismal prognosis and a far greater
percentage of individuals dying of metastatic disease. This suggests the possibility
that various socioeconomic strata are contributing to the emergence of a distinctly
different disease process. The survival disadvantage for young black patients
with tongue cancer needs further investigation.
CONCLUSIONS
There has been a sharply increasing trend in the incidence of tongue
cancer in young Americans since the mid-1970s. The increase may be attributed
to persons who were born between 1938 and 1947 and is associated with a less
virulent disease course. One contributing factor for the rising trend of tongue
cancer in young Americans may be the use of marijuana. Its possible association
should continue to be monitored. In addition, other etiologic clues may be
gleaned from the changing incidence patterns associated with race and, most
likely, socioeconomic status. One must look to lifestyle factors that changed
during the 1940s that seem to be more prevalent in the higher socioeconomic
strata. Potential factors are diverse and could reflect changes in dental
care, diet, food processing, nutritional supplementation, sexual habits, etc.
The potential for interaction of each of these factors on biologic processes
involving oral tongue mucosa must also be considered. The concern is that
observed trends are a "tip-of-the-iceberg" phenomenon. As the current North
American population ages, will the incidence of this changing tongue cancer
disease process also increase? Continued vigilance involving this phenomenon
is required.
AUTHOR INFORMATION
Accepted for publication September 4, 2001.
Presented in part at the annual meeting of the American Head and Neck
Society, Palm Desert, Calif, May 12, 2001.
Corresponding author and reprints: Stimson P. Schantz, MD, Department
of Otolaryngology, The New York Eye and Ear Infirmary, 310 E 14th St, New
York, NY 10003 (e-mail: sschantz{at}nyee.edu).
From the Department of Otolaryngology (Drs Schantz and Yu) and the
Biostatistics and Epidemiology Service (Dr Yu), The New York Eye and Ear Infirmary,
New York Medical College; and the Strang Cancer Prevention Center (Dr Schantz),
New York, NY.
REFERENCES
| |
1. Macfarlane GJ, Boyle P, Scully C. Rising mortality from cancer of the tongue in young Scottish males
[letter]. Lancet. 1987;2:912.
2. Macfarlane GJ, Boyle P, Scully C. Oral cancer in Scotland: changing incidence and mortality. BMJ. 1992;305:1121-1123.
3. Shemen LJ, Klotz J, Schottenfeld D, Strong EW. Increase of tongue cancer in young men [letter]. JAMA. 1984;252:1857.
FULL TEXT
|
ISI
| PUBMED
4. Depue RA. Rising mortality from cancer of the tongue in young white males [letter]. N Engl J Med. 1986;315:647.
ISI
| PUBMED
5. Franchesci S, Levi F, Lucchini F. Trends in cancer mortality in young adults in Europe, 1955-1989. Eur J Cancer. 1994;30A:2096-2118.
6. Shiboski CH, Shiboski SC, Silverman SJ. Trends in oral cancer rates in the United States, 1973-1996. Community Dent Oral Epidemiol. 2000;28:249-256.
FULL TEXT
|
ISI
| PUBMED
7. Chen JK, Eisenberg E, Krutchkoff DJ, Katz RV. Changing trends in oral cancer in the United States, 1935 to 1985:
a Connecticut study. J Oral Maxillofac Surg. 1991;49:1152-1158.
ISI
| PUBMED
8. Myers JN, Elkins T, Roberts D, Byers RM. Squamous cell carcinoma of the tongue in young adults: increasing incidence
and factors that predict treatment outcomes. Otolaryngol Head Neck Surg. 2000;122:44-51.
FULL TEXT
|
ISI
| PUBMED
9. McKean-Cowdin R, Feigelson HS, Ross RK, Pike MC, Henderson BE. Declining cancer rates in the 1990s. J Clin Oncol. 2000;18:2258-2268.
FREE FULL TEXT
10. Mattson ME, Winn DM. Smokeless tobacco: association with increased cancer risk. NCI Monogr. 1989;8:13-16.
11. Sankaranarayanan R, Mohideen MN, Nair MK, Padmanabhan TK, Ainslie N. Aetiology of oral cancer in patients less than or equal to 30 years
of age. Br J Cancer. 1989;59: 439-440.
12. Endicott JN, Skipper P, Hernandez L. Marijuana and head and neck cancer. Adv Exp Med Biol. 1993;335:107-113.
PUBMED
13. Das C, Schantz SP, Shillitoe EJ. Antibody to a mutagenic peptide of herpes simplex virus in young adult
patients with cancer of the head and neck. Oral Surg Oral Med Oral Pathol. 1993;75:610-614.
FULL TEXT
|
ISI
| PUBMED
14. Schantz SP, Hsu TC, Ainslie N, Moser RP. Young adults with head and neck cancer express increased susceptibility
to mutagen-induced chromosomal damage. JAMA. 1989;262:3313-3315.
ABSTRACT
15. Schantz SP, Byers RM, Goepfert H, Shallenberger RS, Beddingfield N. The implication of tobacco use in the young adult with head and neck
cancer. Cancer. 1988;62:1374-1380.
FULL TEXT
|
ISI
| PUBMED
16. Percy C, Van Holten V, Muir C. International Classification of Diseases for Oncology. 2nd ed. Geneva, Switzerland: World Health Organization; 1990.
17. Ries LAG, Eisner MP, Kosary CL, et al. SEER Cancer Statistics Review, 1973-1997. Bethesda, Md: National Cancer Institute; 2000.
18. Kim HJ, Fay MP, Feuer EJ, Midthune DN. Permutation tests for joinpoint regression with applications to cancer
rates. Stat Med. 2000;19:335-351.
FULL TEXT
|
ISI
| PUBMED
19. Hankey BF, Feuer EJ, Clegg LX, et al. Cancer surveillance series: interpreting trends in prostate cancer,
part I: evidence of the effects of screening in recent incidence, mortality,
and survival rates. J Natl Cancer Inst. 1999;91:1017-1024.
FREE FULL TEXT
20. Robertson C, Boyle P. Age, period and cohort models: the use of individual records. Stat Med. 1986;5:527-538.
ISI
| PUBMED
21. National Institutes of Health. Summary Staging Guild for the Cancer Surveillance,
Epidemiology and End Results Reporting (SEER) Program. Bethesda, Md: National Institutes of Health; 1986.
22. US Department of Health and Human Services. Preventing Tobacco Use Among Young People: A Report
of the Surgeon General. Atlanta, Ga: US Dept of Health and Human Services, Public Health
Service, Centers for Disease Control and Prevention, National Center for Chronic
Disease Prevention and Health Promotion, Office on Smoking on Health; 1994.
23. US Department of Health and Human Services. Tobacco Use Among U.S. Racial/Ethnic Minority Groups. Atlanta, Ga: US Dept of Health and Human Services, Public Health
Service, Centers for Disease Control and Prevention, National Center for Chronic
Disease Prevention and Health Promotion, Office on Smoking on Health; 1998.
24. The Gallup Organization. Percentage of Americans who drink alcoholic beverages, 1939-2000. Available at:
http://www.gallup.com/poll/indicators/indalcohol.asp. Accessed November 20, 2001.
25. Johnson LD, O'Malley PMOH, Bachman JG. University of Michigan, Institute for Social Research,
National Survey Results on Drug Use From the Monitoring the Future Study,
1975-1997, Volume I: Secondary School Students. Rockville, Md: National Institutes of Health; 1999.
26. Wingo PA, Ries LA, Giovino GA, et al. Annual report to the nation on the status of cancer, 1973-1996, with
a special section on lung cancer and tobacco smoking. J Natl Cancer Inst. 1999;91:675-690.
FREE FULL TEXT
27. Cole P, Rodu B. Declining cancer mortality in the United States. Cancer. 1996;78:2043-2044.
FULL TEXT
|
ISI
| PUBMED
28. Cullen JW, Blot W, Henningfield J, Boyd G, Mecklenburg R, Massey MM. Health consequences of using smokeless tobacco: summary of the Advisory
Committee's report to the Surgeon General. Public Health Rep. 1986;101:355-373.
ISI
| PUBMED
29. Martin GC, Brown JP, Eifler CW, Houston GD. Oral leukoplakia status six weeks after cessation of smokeless tobacco
use. J Am Dent Assoc. 1999;130:945-954.
FREE FULL TEXT
30. Grady D, Greene J, Daniels TE, et al. Oral mucosal lesions found in smokeless tobacco users. J Am Dent Assoc. 1990;121:117-123.
ABSTRACT
31. Schantz SP, Byers RM, Goepfert H. Tobacco and cancer of the tongue in young adults. JAMA. 1988;259:1943-1944.
32. US Department of Health and Human Services. Spit Tobacco and Youth. Washington, DC: US Dept of Health and Human Services, Office of the
Inspector General; 1992.
33. Centers for Disease Control and Prevention. Use of smokeless tobacco among adults—United States, 1991. MMWR Morb Mortal Wkly Rep. 1993;42:263-266.
PUBMED
34. Johnson RA, Gerstein DR. Initiation of use of alcohol, cigarettes, marijuana, cocaine, and other
substances in US birth cohort since 1919. Am J Public Health. 1998;88:27-33.
FREE FULL TEXT
35. Johnston LD, O'Malley PMOH, Bachman JG. National Survey Results on Drug Use From Monitoring
the Future Study, 1975-1994, Volume I: Secondary School Students. Washington, DC: National Institute on Drug Abuse; 1995.
36. Johnston LD, O'Malley PMOH, Bachman JG. National Survey Results on Drug Use From Monitoring
the Future Study, 1975-1994, Volume II: College Students and Young Adults. Washington, DC: National Institute on Drug Abuse; 1996.
37. Fligiel SE, Roth MD, Kleenup EC, Barsky SH, Simmons MS, Tashkin DP. Tracheobronchial histopathology in habitual smokers of cocaine, marijuana,
and/or tobacco. Chest. 1997;112:319-326.
FREE FULL TEXT
38. Tashkin DP. Is frequent marijuana smoking harmful to health? West J Med. 1993;158:635-637.
ISI
| PUBMED
39. Barsky SA, Roth MD, Kleenup EC, Simmons MS, Tashkin DP. Histopathologic and molecular alterations in bronchial epithelium in
habitual smokers of marijuana, cocaine, and/or tobacco. J Natl Cancer Inst. 1998;90:1198-120 |
