Abstract
Objectives
To explore changes in distribution of stage at diagnosis among individuals with oral and pharyngeal cancers over the past two decades, and whether the changes differ by race.
Methods
We obtained 1991–2008 cancer incidence data for nine anatomic sites of the oral and pharyngeal structure from the Florida Cancer Data System. These cancers were grouped into oral squamous cell carcinoma (SCC), pharyngeal SCC, and other head and neck cancers. Annual percent change was calculated for each group to characterize trends in age-adjusted cancer incidence over time by race and stage at diagnosis.
Results
During 1991–2008, the overall age-adjusted oral SCC incidence was decreasing for both races, with a greater decline observed among Blacks. There was a large drop in incidence of regional-stage diagnoses among Blacks. For pharyngeal SCC, the age-adjusted incidence of localized- and regional-stage diagnoses was increasing for Whites during 1991–2008, with the largest increase in the incidence of regional-stage diagnoses. The percentage of localized-stage diagnoses was increasing for both races for oral SCC. A slight increase in percentage of localized-stage diagnoses was observed for Blacks for pharyngeal SCC, whereas no obvious change was observed among Whites.
Conclusions
Blacks continued to have lower percentages of localized-stage diagnoses than Whites for nearly all sites, but an increasing percentage of localized-stage diagnoses was observed for oral SCC among Blacks. For pharyngeal SCC, the increase in incidence among Whites was accompanied by an increasing percentage of late-stage diagnoses. Coordinated public health approaches with a special emphasis on screening underserved populations are needed.
Keywords: oral and pharyngeal cancers, racial disparity, stage at diagnosis, incidence, trends
Introduction
Oral and pharyngeal cancers (OPC) are deadly diseases. In 2010, approximately 36,540 Americans developed OPC, among whom 7,880 died and many more were disfigured from the treatment (1). Oral and pharyngeal cancers are often considered a single entity, but these are a heterogeneous collection of sites with unique outcomes (2, 3). OPCs are also frequently considered a disease of men, with the probability for developing cancer of the oral cavity and pharynx between the 50th and 70th birthdays at 0.77%, but women are not risk-free (0.26% for women) (4). Over the past decades, a decreasing trend for overall incidence rates of OPCs has been reported (5, 6). Reductions in tobacco use and alcohol consumption are cited as factors for this decreased incidence (7–9). More recently, however, increasing incidence rates have been detected for specific OPC sites (5, 10, 11), with some suggestion of differences by racial groups. However, limited detailed information about trends in age-adjusted incidence rates by anatomic site by racial group is available. In addition, the Surveillance, Epidemiology and End Results (SEER) database, which is often used for such analyses, has limited representation from the Southeastern United States; thus, reports from alternative data sources including state tumor registries are of importance, given regional variations in access to care, treatment, environmental factors, and racial diversity.
Healthy People 2020 sets as a goal that 35.8% of all oral and pharyngeal cancers will be diagnosed at the localized stage, representing a 10% improvement since 2007 (12). The percentage diagnosed at the localized stage, however, varies by anatomic site within the oral and pharyngeal structures. Sethi and colleagues (2), using data from the Henry Ford Health System, reported early stage diagnosis rates ranging from 22% for oropharynx to 46% for larynx. In addition, there appears to be a wide discrepancy between the stage of diagnosis for Blacks versus Whites for most oral and pharyngeal sites (1, 2, 13, 14). Molina and colleagues reported that, for Blacks, 32% of the oral and pharyngeal tumors were diagnosed at the localized stage, whereas for tumors of the same sites, 45% of Whites were diagnosed at the localized stage (15).
The two purposes of this investigation are to characterize trends in age-adjusted incidence by specific sites of the oral and pharyngeal structure by stage at diagnosis and by racial groups, and to document progress toward meeting the Healthy People 2020 goal (OH-6 from Healthy People 2020). Overall, we expected to see a trend toward earlier-stage diagnosis, given the greater public health emphasis on cancer detection and prevention (16, 17). Racial disparities in stage of diagnosis for most anatomic sites were expected, as limited progress has been made in access to care for vulnerable populations (18, 19).
Materials and Methods
Data source
De-identified data were provided by the Florida Cancer Data System (FCDS), a statewide population-based registry supported by the Florida Department of Health and National Program of Cancer Registries for the Centers of Disease Control and Prevention. The FCDS collects incidence data throughout Florida from hospitals, pathology laboratories, radiation therapy facilities, ambulatory surgery centers, and dermatopathologists’ offices. Florida statutes require that all malignant cancers be reported to FCDS, with limited exceptions for some types of skin cancers. Data are collected at least quarterly by trained personnel, and case-finding strategies are used to insure completeness of the data. FCDS has achieved the highest standard defined by the North American Association of Central Cancer Registries for quality, timeliness, and completeness of its data (20).
Case selection and variable definitions
Subjects included in the analysis were Florida residents diagnosed with OPC who were at least 20 years old at the time of diagnosis. Primary anatomic sites were identified using International Classification of Disease (ICD-O-3) codes C00.0 through C14.8 (21). Since there were modifications made to the ICD classifications prior to 1991, only patients diagnosed with OPC between 1991 and 2008 were included. Based on the etiology of these cancers, they were grouped into oral squamous cell carcinoma (floor of mouth, tongue, and palate), pharyngeal squamous cell carcinoma (base of tongue, tonsil, oropharynx, and hypopharynx), and other head and neck cancers (salivary glands and nasopharynx). Nasopharyngeal carcinomas can be classified as squamous cell carcinoma (the most common subtype in sporadic cases), undifferentiated carcinoma, or basaloid squamous cancers. As each subtype has a distinct biology, and the breakdown of histological subtypes was not available, nasopharyngeal cancers were analyzed separately from other, more characteristic, OPCs (22). Race was restricted to Blacks and Whites since only 1% of the study population were classified as belonging to other race groups. Staging classification was based on SEER summary stage information and classified as localized, regional, or distant/systemic. This study was approved by the University of Florida Institutional Review Board (IRB-01).
Statistical analysis
Descriptive statistics were calculated to summarize the demographic characteristics of the study population. Age-adjusted incidence rates were calculated as the primary outcome of interest. In addition, trends of age-adjusted incidence rates for each of the anatomic sites were evaluated using the annual percentage change (APC). APC was calculated by first fitting a regression line to the natural logarithms of the age-adjusted incidence rates using calendar year as the independent variable. Then, APC was calculated as APC = 100 × (em − 1), where e was the base of the natural logarithm and m was the slope of the regression line. The hypothesis that the APC was equal to zero was tested at the 0.01 significance level. A positive APC corresponds to an increasing trend, while a negative APC corresponds to a decreasing trend. All analyses were performed with SAS 9.2 (SAS Institute Inc., Cary, NC, USA).
Results
Characteristics of those diagnosed with OPC in Florida from 1991 through 2008 are shown in Table 1. A total of 33,963 OPC cases was included in this study. A little more than two-thirds of all cases were diagnosed in males. More than 90% of all OPC cases were diagnosed among those older than 44 years.
Table 1.
Demographic characteristics of the population studied.
| Characteristic | Squamous cell carcinoma | Other head and neck cancers | Total n=33,963 |
||
|---|---|---|---|---|---|
| Oral n=10,643 |
Pharyngeal n=17,084 |
Salivary n=4,261 |
Nasopharynx n=1,975 |
||
| Sex | |||||
| Male | 62.2% | 75.8% | 62.0% | 66.7% | 69.3% |
| Female | 37.8% | 24.2% | 38.0% | 33.3% | 30.7% |
| Race | |||||
| White | 92.0% | 90.8% | 93.2% | 86.9% | 91.3% |
| Black | 8.0% | 9.2% | 6.8% | 13.1% | 8.8% |
| Age at diagnosis |
7.8% | 5.3% | 9.8% | 13.4% | 7.1% |
| 20–44 | 42.8% | 51.0% | 27.3% | 45.0% | 45.1% |
| 45–64 | 49.5% | 43.7% | 62.9% | 41.6% | 47.8% |
| >64 | |||||
Percentages may not add to 100% due to rounding.
The trends in overall age-adjusted incidence rate for each of the four anatomic sites stratified by race are shown in Figure 1. For the oral squamous cell carcinoma (SCC), the overall incidence rate was decreasing for both Blacks (APC = −5.17, p < 0.0001) and Whites (APC = −1.78, p < 0.0001) during 1991–2008. For the pharyngeal SCC, the overall incidence rate was decreasing for Blacks (APC = −4.03, p < 0.0001), but was increasing for Whites (APC = 1.22, p < 0.0001) during 1991–2008. As for other head and neck cancers, the overall incidence rate remained unchanged for both Blacks and Whites for cancers of the salivary glands during 1991–2008. The overall incidence rate was decreasing for both races for nasopharynx cancer, with APCs of −4.01 for Blacks (p = 0.0021) and −1.96 for Whites (p < 0.0001).
Figure 1. Trends in age-adjusted incidence by cancer and race.
(A) Squamous cell carcinomas.
(B) Other head and neck cancers.
We further examined the racial disparities in stage of diagnosis by studying trends in the age-adjusted incidence rate for each anatomic site, stratified by race and stage of diagnosis (Figure 2). The results for the SCCs are summarized in Figure 2A. For the oral SCC, the incidence rate of localized-stage diagnoses remained unchanged for Blacks (p = 0.5025), but was decreasing for Whites (APC = −1.03, p = 0.0066) during 1991–2008. Furthermore, the incidence rate of regional-stage diagnoses was decreasing for both Blacks (APC = −6.58, p < 0.0001) and Whites (APC = −1.84, p = 0.0005), whereas the incidence rate of distant-stage diagnoses remained unchanged for both races. For the pharyngeal SCC, the incidence rate of localized-stage diagnoses remained unchanged for Blacks (p = 0.1248), but was increasing for Whites (APC = 1.21, p = 0.0054) during 1991–2008. The incidence rate of regional-stage diagnoses was decreasing for Blacks (APC = −4.84, p < 0.0001), but increasing for Whites (APC = 1.75, p < 0.0001). Again, the incidence rate of distant-stage diagnoses remained unchanged for both races.
Figure 2. Trends in age-adjusted incidence by cancer, stage of diagnosis, and race.
(A) Squamous cell carcinomas.
(B) Other head and neck cancers.
For the cancers of the salivary glands and nasopharynx, the change in age adjusted incidence rate was not statistically significant for Blacks at all stages (Figure 2B). For Whites, the incidence rate of regional-stage diagnoses was decreasing for both salivary gland cancers (APC = −2.46, p = 0.0040) and nasopharynx (APC = −2.01, p = 0.0011). On the other hand, incidence rate of distant-stage diagnoses of salivary gland cancer was significantly increasing for Whites (APC = 6.18, p = 0.0008).
The percentages of localized-stage diagnoses by race and year of diagnosis for the anatomic sites of interest are shown in Table 2. Considering SCC of oral structures, the percentage of localized-stage diagnoses for the combined oral sites increased from 23.0% in 1991–96 to 32.2% in 2003–08 among Blacks. Among Whites, the percentage of localized-stage diagnoses increased from 45.4% in 1991–96 to 49.0% in 2003–08. During the latest time period, 2003–08, the percentages of localized-stage diagnoses for the floor of mouth, tongue, and palate were 38.2%, 28.8%, and 31.2% for Blacks and 46.9%, 51.2%, and 45.1% for Whites. Considering SCC of pharyngeal structures, the percentage of localized-stage diagnoses for the combined pharyngeal sites slightly increased from 10.7% in 1991–96 to 14.0% in 2003–08 among Blacks. Among Whites, the percentage of localized-stage diagnoses remained nearly constant, ranging from 17.3% (1997–02) to 18.1% (1991–96). Overall, however, significantly lower percentages of localized-stage diagnoses were observed for the pharyngeal SCCs than the oral SCCs. During the latest time period, 2003–08, the percentages of localized-stage diagnoses for the base of tongue, tonsil, oropharynx, and hypopharynx were only 13.2%, 11.7%, 10.0%, and 20.8% for Blacks and 17.0%, 16.2%, 17.5%, and 22.7% for Whites.
Table 2.
Percentage of diagnosis at the localized stage by race and year of diagnosis.
| (A) Squamous cell carcinoma (SCC). | |||||||
|---|---|---|---|---|---|---|---|
| Black | White | ||||||
| `91-`96 | `97-`02 | `03-`08 | `91-`96 | `97-`02 | `03-`08 | ||
| Oral SCCa |
23.0% (282b) |
28.2% (308) |
32.2% (264) |
45.4% (3149) |
48.2% (3345) |
49.0% (3295) |
|
| Floor of mouth | 23.7% (97) |
26.5% (102) |
38.2% (76) |
41.6% (1094) |
44.1% (1002) |
46.9% (847) |
|
| Tongue | 26.7% (101) |
25.5% (102) |
28.8% (111) |
50.7% (1354) |
52.9% (1646) |
51.2% (1876) |
|
| Palate | 17.9% (84) |
32.7% (104) |
31.2% (77) |
41.1% (701) |
43.0% (697) |
45.1% (572) |
|
| Pharyngeal SCCc |
10.7% (505) |
11.5% (514) |
14.0% (551) |
18.1% (4162) |
17.3% (5046) |
17.7% (6306) |
|
| Base of tongue | 11.5% (113) |
9.8% (112) |
13.2% (151) |
17.4% (1311) |
16.9% (1657) |
17.0% (2274) |
|
| Tonsil | 13.2% (182) |
15.9% (189) |
11.7% (180) |
19.0% (1305) |
16.0% (1842) |
16.2% (2301) |
|
| Oropharynx | 6.7% (75) |
7.3% (82) |
10.0% (90) |
16.3% (516) |
19.1% (529) |
17.5% (687) |
|
| Hypopharynx | 8.9% (135) |
9.2% (131) |
20.8% (130) |
18.8% (1030) |
19.4% (1018) |
22.7% (1044) |
|
| (B) Other head and neck cancers. | ||||||
|---|---|---|---|---|---|---|
| Black | White | |||||
| `91-`96 | `97-`02 | `03-`08 | `91-`96 | `97-`02 | `03-`08 | |
| Salivary | 44.9% (78) |
53.7% (95) |
51.3% (117) |
37.2% (1196) |
40.8% (1403) |
40.7% (1372) |
| Nasopharynx | 15.9% (82) |
6.1% (82) |
10.5% (95) |
13.2% (559) |
15.9% (586) |
12.3% (571) |
includes sites of floor of mouth, tongue, and palate.
Total number of cancer cases in this category: a total of 282 cases of oral SCC were reported for Blacks between 1991 and 1996.
includes sites of base of tongue, tonsil, oropharynx, hypopharynx.
For cancers of the salivary glands, a higher percentage of Blacks were diagnosed at the localized stage than Whites. The percentages of localized-stage diagnoses were 44.9%, 53.7%, and 51.3% across the three time periods for Blacks, compared to 37.2%, 40.8%, and 40.7% for Whites. No clear pattern of localized-stage diagnoses across time was observed for cancers of the nasopharynx; however, note that only a small number of incident cases were available compared to the SCCs.
In summary, the overall age-adjusted incidence rate was decreasing for Blacks for both oral and pharyngeal SCCs during 1991–2008. For Whites, a decrease in incidence was observed for the oral SCC; however, the overall age-adjusted incidence rate was increasing for the pharyngeal SCC. After studying the trends in incidence for each stage of diagnosis separately, it was observed that the age-adjusted incidence rates of localized- and regional-stage diagnoses were increasing for Whites for the pharyngeal SCC, with the largest increase in the incidence of regional-stage diagnoses. For other head and neck cancers, the age-adjusted incidence rate was either decreasing or remained unchanged for both Blacks and Whites across all stages of diagnosis, with one exception: the incidence of distant-stage diagnoses was increasing for Whites for cancers of the salivary glands. Furthermore, significantly lower percentages of localized-stage diagnoses were observed for the pharyngeal SCC sites than the oral SCC sites. The percentage of localized-stage diagnoses was increasing for both Blacks and Whites for the combined oral SCC sites. A slight increase in the percentage of localized-stage diagnoses was observed for Blacks for the combined pharyngeal SCC sites, whereas no obvious change was observed among Whites.
Discussion
Key findings
The key findings of our study include 1) For oral SCC, the overall age-adjusted incidence rate was decreasing for both Blacks and Whites during 1991–2008. For the pharyngeal SCC, the overall age-adjusted incidence rate was decreasing for Blacks, whereas the rate was increasing for Whites during 1991–2008; 2) further examination of the increasing incidence rate for the pharyngeal SCC for Whites showed that the largest increase was in the incidence of regional-stage diagnoses; and 3) the Healthy People 2020 goal of 35.8% localized-stage diagnoses was only met by Whites for oral SCC. We are far from meeting the goal for pharyngeal SCC for both races. The percentage of localized-stage diagnoses was increasing for both races for the oral SCC. However, no obvious progress was made for the pharyngeal SCC.
Racial disparity in trends in age-adjusted incidence by stage of diagnosis
Our observation of overall decreasing incidence rates for the oral SCC for both Blacks and Whites is consistent with previous studies based on the SEER data (23, 24). Reduction in tobacco use in the past few decades has almost certainly contributed to the declining incidence of oral cancers. However, further research is needed to quantitatively measure the contribution of reduction in tobacco use. In our study population, Blacks had a significantly larger drop in overall oral SCC incidence than Whites during 1991–2008. This strong decreasing trend for Blacks came from a large drop in incidence of regional-stage diagnoses, as no changes were observed in the incidence of localized- or distant-stage diagnoses (Figure 2A). Therefore, it is not surprising that the percentage of localized-stage diagnoses for the oral SCC kept increasing for Blacks over the past twenty years (Table 2). In other words, the probability of identifying an oral squamous cell carcinoma at the earliest, localized, stage was significantly increased for Blacks. These intriguing results indicate a diminishing racial disparity in the diagnosis of the oral SCC.
At the national level, it has been reported that the incidence of cancer in several anatomic sites of pharyngeal structures increased dramatically among Whites during the past few decades (5, 25). Our results showed that there were similar increasing trends among Whites in Florida, especially for cancers of the base of tongue and tonsil (Table 2). This increase in incidence among Whites is believed to be associated with the increasing recognition of HPV-related cancers in the relatively younger population (25, 26). Because of the location of these tumors, visual and tactile examinations are unlikely to identify these lesions. In addition, the age and demographics of the patient may fall outside the usual criteria for screening. Thus, selective examinations of asymptomatic persons in defined higher-risk populations, including more in-depth testing than the usual dental screening examination, may be a more realistic and effective means for the earlier diagnosis of these lesions.
Another worrying observation was that, over the past few decades, no obvious improvement has been made in diagnosing early SCC at these pharyngeal sites. In other words, we did not observe a trend toward the earlier-stage diagnoses that we had expected. Our analysis showed that the increase in the overall age-adjusted incidence was driven by a large increase in the incidence of regional-stage diagnoses. This indicates that these cancers became increasingly more likely to be diagnosed at the regional stage during the past two decades, adding to the already very large proportion of regional-stage diagnoses for these pharyngeal cancers. By the years of 2003–2008, only 17.0% of base of tongue cancers and 16.2% of tonsil cancers were diagnosed in Whites at the localized stage (Table 2). As the demographic profiles and risk factors for pharyngeal cancers have been changing in the past a few decades, the screening procedures for these cancers also need to be changed accordingly to favor their being diagnosed at the localized stage.
Disparities in percentages of localized-stage diagnoses
For all the oral or pharyngeal SCCs in our study, Whites had consistently higher percentages of localized-stage diagnoses than Blacks across the time periods. In addition, the percentages of localized-stage diagnoses for the pharyngeal SCCs were smaller than those for the oral SCCs, regardless of race. For the oral SCCs, the percentage of Whites diagnosed at the localized stage was at least 40% across the periods. On the other hand, for the pharyngeal SCCs, the percentage of individuals diagnosed at the localized stage was consistently below 23% for both Blacks and Whites across the periods. However, compared with the SEER data, our study population had a higher percentage of localized-stage diagnoses at many oral and pharyngeal sites. For example, for floor of mouth and tongue cancers, the percentages of localized-stage diagnoses were 43.4% and 36.5% for Whites and 29.5% and 21.9% for Blacks between 2000 and 2008 in the SEER report (4), compared to 46.9% and 51.2% for Whites and 38.2% and 28.8% for Blacks during a similar period of time in our data.
For the most part, it is not surprising that higher percentages of localized-stage diagnoses were observed for oral SCCs than for pharyngeal SCCs. One obvious reason is that the greater visual and tactile access to this anatomic region for both medical and dental personnel, as well to patients themselves, makes direct detection of early lesions possible. It stands to reason that patients could identify anomalies (27) and, if properly informed about the early signs, might self-refer to an appropriate healthcare provider. Anatomically, pharyngeal sites are less visible without the aid of a special, lighted endoscope, and may not be directly examined unless an endoscopy procedure is performed. Therefore, while cancers of oral sites could potentially be identified during a regular dental or medical exam, cancers of the pharyngeal sites are less likely so without more sophisticated techniques. It would be helpful if more studies could focus on the identification of lesions of the pharyngeal sites through pre-symptomatic, opportunistic examinations involving non-invasive techniques.
The racial disparity in stage of diagnosis for OPC observed in our study is consistent with previous findings (15, 23, 28, 29). With lower percentages of localized-stage diagnoses, Blacks were more likely to be diagnosed at an advanced stage, except for cancers of the salivary glands. Lower socioeconomic status and less accessibility to health care were proposed to explain the higher percentage of advanced-stage diagnoses observed in Blacks (28). Several studies have found that communities with greater poverty had higher percentages of advanced-stage OPC diagnoses (15, 30). Better techniques for diagnosing earlier-stage lesions are important, but a more serious issue is how such life-saving procedures can be translated to local communities and at-risk community members, so that improvements in diagnosis do not result in a widening of existing health disparities gaps (31, 32).
Meeting the Healthy People 2020 goal
Based on our results, there is concern that the Healthy People 2020 goal of 35.8% localized-stage diagnoses cannot be met, especially for pharyngeal SCCs. This may be especially true for the state of Florida, but may also be true throughout the United States. During the 2003–2008 time period, the percentage of localized-stage diagnoses for any of the four pharyngeal SCCs was no more than 22.7% for both Blacks and Whites. On the other hand, better results were observed for the oral SCCs. The FCDS data demonstrate that the 2020 goal was met by Whites for all oral SCCs but was not met by Blacks for tongue (28.8%) and palate (31.2%).
Unexpected findings for cancers of the salivary glands
Our results for cancers of the salivary glands may present a hopeful note in reduction of health disparities. The overall incidence rate of the salivary gland cancer remained unchanged for both Blacks and Whites during 1991–2008; Blacks had higher percentages of localized-stage diagnoses than Whites across all three time periods. Fluctuating around 50% across the years, the percentage of localized stage diagnosis is remarkably high for salivary gland cancer among Blacks, compared to cancers of other anatomic sites. Our observation is similar to data from SEER, in which 51.2% and 43.5% of salivary gland cancers were localized stage diagnosis from 2000–2008 for Blacks and Whites, respectively (4).
Potential factors associated with early-stage diagnosis
Several factors are potentially associated with early-stage diagnoses of OPC, including receiving a proper screening examination from the patient’s regular primary-care dentist or physician and increased patient awareness of early signs of cancer (27). However, a widespread lack of awareness and knowledge regarding OPC was still present in Florida, resulting in disproportionally high prevalence of advanced-stage diagnoses (33–36). Apparently, many of the individuals diagnosed at an advanced stage were not aware of OPC or that an OPC examination existed. Therefore, increasing awareness of OPC and an OPC examination as well as informing individuals of risk factors and signs and symptoms of early stage disease are important steps in improving outcomes. On the other hand, early-stage diagnosis of the pharyngeal sites provides additional challenges. Current screening methods lack either sensitivity, low cost, ease of performance, or availability of properly trained personnel. Coordinated efforts, including new, inexpensive, more sensitive, and specific detection methods and new procedures involving both medical and dental personnel will be needed if we are to meet the Healthy People 2020 goal of 35.8% localized stage diagnosis for the pharyngeal sites.
Acknowledgement
This study was partially supported by NIDCR U54DEO19261-01 (H. Logan PI). The Florida cancer incidence data used in this study were collected by the Florida Cancer Data System under contract with the DOH. The views expressed herein are solely those of the authors and do not necessarily reflect those of the contractor of DOH.
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