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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 62:892-898 (2007)
© 2007 The Gerontological Society of America

The Influence of Marital Status on Stage at Diagnosis and Survival of Older Persons With Melanoma

Carlos A. Reyes Ortiz, Jean L. Freeman, Yong-Fang Kuo and James S. Goodwin

Sealy Center on Aging, Department of Internal Medicine, University of Texas Medical Branch, Galveston.

Address correspondence to Carlos A. Reyes Ortiz, MD, PhD, Sealy Center on Aging, Department of Internal Medicine, University of Texas Medical Branch, 301 University Blvd., Galveston, TX 77555-0460. E-mail: careyeso{at}utmb.edu


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
Background. Melanoma incidence and mortality had a sustained increase in the last 3 decades in the United States, especially among white older men. Little is known about the relationship between marital status and melanoma outcomes in older people. The objective of this study was to determine the association between marital status and stage at diagnosis and survival of older persons with cutaneous melanoma.

Methods. Data are from the Surveillance, Epidemiology and End Results (SEER) registries–Medicare–linked database (1991–1999). The sample consisted of 14,630 men and women 65 years old and older. The outcomes were melanoma stage at diagnosis and melanoma specific survival. The main independent variable, marital status, was used in four categories: married, single, separated or divorced, and widowed. Other covariates include sociodemographics, stage at diagnosis, tumor characteristics (body site and histology), and comorbidity index. Logistic regression and survival analyses techniques were used.

Results. Multivariate analyses showed that, compared with married persons, widowed persons were more likely to be diagnosed with late-stage (regional or distant) versus early-stage (in situ or localized) melanoma (odds ratio = 1.31, 95% confidence interval [CI], 1.13–1.52). In addition, after controlling for all other variables (sociodemographics, stage at diagnosis, tumor characteristics, and comorbidity), widowed persons were at increased risk of death from melanoma (hazard ratio = 1.23, 95% CI, 1.06–1.44).

Conclusion. Older widowed persons were more likely to be diagnosed at late stage and to die from melanoma than were older married persons.

Melanoma incidence and mortality rates have increased in the last 3 decades in the United States. For example, Geller and colleagues (1) reported that mortality rates increased from 7.5 to 19.3/100,000 in white men 65 years old and older, a more than 3-fold greater increase than for women of the same age and race.

In 2003, 53% of women 65–74 years old were married and 29% were widowed, compared with 74% of men who were married and 9% who were widowed in the same age group in the United States (2). As age increased, the proportion of married persons decreased and the proportion of widowed persons increased. Indeed, at age 85 and older, the majority of women were widowed (78%), compared with 35% of men.

Marital status may influence cancer stage at diagnosis and survival. Married persons living with cancer have higher odds of localized disease and greater survival than do unmarried persons (3–5). Some mechanisms have been proposed to explain the survival disadvantage of unmarried persons. Unmarried persons are more likely to: (i) be diagnosed at a regional or distant stage; (ii) be untreated for cancer; and (iii) have less social support and fewer social relations (4).

However, there is limited information about the influence of marital status on melanoma outcomes (3,4). The Surveillance Epidemiology and End Results (SEER) tumor registry, which has been linked to Medicare claims data at the National Cancer Institute, was used in this study (6). The objective of this study was to determine the association between marital status and stage at diagnosis and survival of older persons on Medicare with cutaneous melanoma.


   METHODS
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 Abstract
 Methods
Results
 Discussion
 References
 
Data Source
Data were obtained from a database of linked tumor registry records from the SEER program and Medicare claims from the Health Care Financing Administration (HCFA; now called the Centers for Medicare and Medicaid Services). Cases reported by the SEER registries from 1991 through 1999 were matched against Medicare's master enrollment file (6,7).

Study Sample
There was a total of 19,479 cases of melanoma among individuals 65 years old and older from 1991 through 1999. Due to our interest in marital status, individuals with unknown marital status (4849, 25%) were excluded from this study. A similar percentage of persons with unknown marital status (21%) has been reported in another study on melanoma using data from SEER and including individuals of all ages (8). The sample for this study includes 14,630 persons 65 years old and older with known marital status who were Medicare beneficiaries, resided in a SEER area (one of 11 areas), and received a new diagnosis of melanoma from 1991 through 1999. Compared to persons with known marital status (married, single, divorced or separated, widowed), persons with unknown marital status were more likely to be classified in the "other" ethnic group, but were no different in age or gender. They were also more likely to have a higher percentage of in situ and lower percentages of regional or distant stages of melanoma at diagnosis, a higher percentage of lentigo maligna (LM) melanoma and a lower risk of death. In addition, when compared to married persons, those persons with unknown marital status had a lower risk of death from melanoma.

Measures
The outcomes were melanoma stage at diagnosis and specific survival. Stage of melanoma at diagnosis includes five categories: (i) in situ, (ii) local, (iii) regional, (iv) distant, and (v) unstaged (defined by SEER when the information is not sufficient to assign a stage) or unknown stage (missing values). Using the same design published by Van Durme and colleagues (3), we dichotomized the outcome stage into late stage (regional and distant, code = 1) versus early stage (in situ or local, code = 0); and persons with unstaged or unknown stage (898, 6.2%) were excluded from the analysis of this outcome. Compared to individuals with known stage at diagnosis, those with unstaged or unknown stage at diagnosis were more likely to be older or to be unmarried or widowed. They were less likely to have LM or superficial spreading melanoma, but were more likely to die from melanoma. In addition, when compared to persons with in situ stage at diagnosis, those with unstaged or unknown stage at diagnosis had a higher risk of death from melanoma (see Table 4).


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  		Table 4. Multivariate Cox Proportional Hazards Models for Marital Status and Other Variables Predicting Death From Melanoma.

 
The second outcome, survival, is the period of time between date of diagnosis and date of death from melanoma, measured in months. The date of censoring was at death from other causes or December 31, 2000, whichever came first.

Marital status was the main independent variable, and was categorized into married, single, separated or divorced, and widowed. For analyses of interactions it was dichotomized into married (code = 1) and unmarried (single, separated or divorced, or widowed; code = 0).

Age (years) was used as continuous variable. Gender includes male and female. Ethnicity includes non-Hispanic whites, blacks, Hispanics, and others. Socioeconomic status was measured by median annual household income per year collected at the census tract level, and was used as a continuous variable (natural logarithm [ln] of [income/1000)]). According to the International Classification of Diseases for Oncology, Third Edition [ICD-0-3] SEER codes, histology of melanoma was categorized into the four main types of melanoma: nodular (8721), LM (8742), superficial spreading (8743), acral lentiginous (8744), plus other (8722, 8723, 8730, 8740, 8741, 8745, 8760, 8761, 8770, 8771, 8772, 8773, and 8780 with a number of 623 cases, 4.3%) or nonspecified (8720, which corresponds to melanoma not otherwise specified, with a total of 5533 cases, 37.8%). Site of the tumor was categorized into trunk, face, upper limb, lower limb, and nonspecified. Comorbidity was ascertained from Medicare inpatient and outpatient claims through diagnoses (or procedures) made 1 year before the diagnosis of melanoma. We used the comorbidity index created by Charlson and colleagues (9) and later validated by Romano and colleagues (10) using the International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM) diagnosis and procedure codes. Comorbidity index was categorized into 0, 1, and ≥ 2.

Analyses
Descriptive statistics were used to describe the study population and the distribution of variables across marital status categories. Pearson's chi-square was used to test bivariate differences in late-stage melanoma across marital status categories. Adjusted logistic regression analysis was used to estimate the odds of having late-stage melanoma at diagnosis by marital status and to control for other variables. Survival analysis techniques were used to estimate the risk of death from melanoma after diagnosis. Kaplan–Meier product limit was used to estimate survival rates (%, 95% confidence intervals [CI]) for marital status categories, and differences were tested by the log–rank test. Adjusted Cox regression proportional hazard regression model (PHREG procedure) was used to predict the risk of death from melanoma at follow-up and to determine the independent influence of marital status and other potential predictors on the event (death from melanoma). Additionally, we assessed the influence of age, gender, site, and histology on the relationship between marital status and the two outcome variables. Assumptions underlying the regression models were tested and found to be met. Significance level (two tailed) was set at p <.05. All analyses were completed using version 9.1 of the SAS system for Windows (SAS Institute, Cary, NC).


   RESULTS
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 Abstract
 Methods
 Results
Discussion
 References
 
Table 1 presents the characteristics of the study population diagnosed with cutaneous melanoma in SEER areas from 1991 through 1999. Individuals had a mean age of 75 years, and mean household income by area where they live was $43,733/year. Sixty percent of these persons were men, 67% were married, 21% were widowed, and 94% were non-Hispanic whites. In terms of their disease, 31% had in situ and 49% had localized stage at diagnosis, 8% were nodular, 27% were LM, and 21% were superficial spreading melanomas. By location, 36% of lesions were in the face, and 23% were in the trunk.


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  		Table 1. Distribution of Men and Women Aged 65 Years or Older With Melanoma Diagnosed in 1991–1999 in SEER (N = 14,630).

 
Table 2 presents the distribution of demographic and tumor characteristics across marital status categories. Compared to married individuals, those who were widowed were more likely to be older and female, to have lower income, to have nodular or acral lentiginous melanoma, to have less melanoma of the face or more of the lower limb, and to have a high number of comorbidities. Widowed persons were less likely to have in situ or localized melanomas but more likely to have regional or distant melanomas.


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  		Table 2. Distribution of Demographic and Tumor Characteristics Across Marital Status Categories.

 
Late-Stage Melanoma as the Outcome
Table 3 presents the multivariate logistic regression analysis for marital status and other variables predicting late stage (regional or distant vs early stage, in situ or localized) of melanoma at diagnosis. Single (odds ratio [OR] = 1.34, 95% CI, 1.09–1.64) and widowed (OR = 1.31, 95% CI, 1.13–1.52) persons were more likely to have late-stage melanoma at diagnosis than were married persons. Other factors predicting higher odds of having late-stage melanoma were age, male gender, Hispanic ethnicity, nodular melanoma, and lesions located in the face, upper limbs, or lower limbs. In contrast, the increase of income in the census tract area was associated with lower odds of having late-stage melanoma. In addition, we found an interaction of gender and marital status (married vs unmarried) on stage at diagnosis (p =.0105); married women were less likely than married men to have a late-stage melanoma, but there was no difference between unmarried men and unmarried women (Figure 1).


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  		Table 3. Multivariate Logistic Regression Analysis for Marital Status and Other Variables Predicting Late-Stage Melanoma at Diagnosis (N = 13,732)*.

 

Figure 01
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  		Figure 1. Interaction effect between gender and marital status (married vs unmarried) on melanoma stage at diagnosis (late stage = regional or distant)

 
Risk of Death From Melanoma as the Outcome
The overall 5-year Kaplan–Meier survival rate was 90.0% (95% CI, 89.4–90.6). Figure 2 presents the 5-year Kaplan–Meier survival rates (%, 95% CI) by gender and marital status categories. In both genders, widowed persons had significantly lower survival rates than did married persons. These survival rates were 89.8% (95% CI, 88.9–90.6) for married men, 85.3% (95% CI, 81.9–88.0) for widowed men, 93.6% (95% CI, 92.5–94.6) for married women, and 88.2% (95% CI, 88.5–89.7) for widowed women. In addition, we found an interaction of gender and marital status (married vs unmarried) on melanoma survival (p =.0013), where married women were less likely to die than were married men (CI values do not overlap), but there was no difference between unmarried men (87.3%, 95% CI, 85.3–89.1) and unmarried women (88.4%, 95% CI, 87.0–89.7).


Figure 02
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  		Figure 2. Five-year Kaplan–Meier survival rates (%, 95% confidence interval [CI]) by gender and marital status categories (1 = married, 2 = single, 3 = separated or divorced, 4 = widowed, 5 = unmarried [this is a combined category of 2, 3, and 4])

 
Table 4 presents the adjusted Cox proportional regression analyses predicting death from melanoma after diagnosis, according to marital status and other variables. Widowed persons had a higher risk of death (hazard ratio [HR] = 1.23, 95% CI, 1.04–1.44) than did married persons. Other factors independently associated with an increased risk of death from melanoma were increased age, male gender, and residing in areas with low income. Individuals with advanced stages at diagnosis of melanoma (localized, regional, and distant) had increased risk of death compared to those with in situ stage. Persons with LM, superficial spreading, acral lentiginous, and other histological types had a lower risk of death than did persons with the nodular type of melanoma. Persons with melanomas of the face and upper limb had a lower risk of death than persons with melanomas located in the trunk. Persons with melanomas in a nonspecified site had a higher risk of death than did persons with melanomas located in the trunk.


   DISCUSSION
Top
 Abstract
 Methods
 Results
 Discussion
References
 
This study showed that widowed older persons have an increased frequency of late-stage melanoma at diagnosis and increased risk of death from melanoma compared to married persons. The increased late stage and risk of death remain even after adjusting for age, gender, income, ethnicity, and tumor characteristics such as histology and lesion location. Risk of death was also adjusted for stage at diagnosis and comorbidity. This finding suggests that being widowed is an independent prognostic factor for having a late stage of melanoma at diagnosis and a lower survival.

Research has shown that widowhood negatively affects the health and survival of the surviving spouse (2,11,12). Studies suggest that, although both men and women who are widowed have increased mortality, it is higher for men; this gender difference does not tend to persist beyond the first year or two, due to both the healing effect over time as well as the selection effect due to the death of the most fragile individuals early in widowhood (12,13).

Although some studies in the literature relate to the association between marital status and cancer (4,5,14–16), only one examines the specific relationship between being widowed and cancer (17). Furthermore, less is known about the relationship between being widowed and having melanoma. Being widowed has been associated with increased melanoma incidence (18,19) but not with mortality (20). We found only two studies that reported an association between unmarried persons and late stage of melanoma at diagnosis (3,4), but those studies have no results specific for widowed persons.

Possible explanations for our results include the fact that widowhood is associated with high emotional stress (e.g., grief), loss of social support (e.g., decrease of networks), and loss of material support (e.g., decrease in income). In addition, widowed older patients are more likely to receive nonadherent treatment or to use lower quality hospitals than are married counterparts (8,21). Finally, bereaved persons show alterations of immunity such as reduced responsiveness of peripheral blood lymphocytes to mitogens, and decreased natural killer cell activity (22,23).

Our findings that increased age and male gender were associated with increased risk of death from melanoma agree with some previous studies. Some studies have shown that increased age has been associated with lower melanoma survival (24–28). Age may affect host response to the disease; older patients are usually screened less often than younger patients, present with late stages of melanoma, and are more likely to have nodular melanomas, known to have a high potentiality for metastases (24–28). Melanoma has a worse prognosis in men than in women. Women are more likely to seek screening methods, present with a lower proportion of thicker lesions, and may have melanoma lesions localized to more favorable anatomic sites than men (3,24). Our finding that residing in low-income areas was associated with increased odds of having late-stage melanoma at diagnosis, and increased risk of death agrees with previous reports (27–29).

An additional finding of our study was the interaction effect of gender and marital status on stage at diagnosis and survival from melanoma. First, we showed that married women were less likely than married men to have a late stage, but there was no difference between unmarried men and women. Second, married women were less likely to die than were married men, but there was no difference between unmarried men and unmarried women. To our knowledge, there are no previous reports showing the lack of gender effect on melanoma stage of diagnosis or survival among unmarried older persons.

The distribution of histology of melanoma in our study differs from that in other studies. Although superficial spreading melanoma (SSM) is considered the most common type of melanoma in the general population, its percentage in our study (21.5%) is lower than that reported by Cormier and colleagues (30) (42% for whites, 29% for Hispanics, 23% for African Americans) using the SEER data (11 areas, 1992–2002); however, they included cases of melanoma in all ages, and our study included only persons 65 years old and older. One reason for a lower percentage of SSM in our study is because, in the SEER data, about 40% of histology cases correspond to "other" (different from the four main types of melanoma: nodular, acral lentiginous, superficial spreading, or LM) or nonspecified histological type of melanoma (30,31). Similarly, in a study by Chang and colleagues (32) using hospital-based cancer registries, 27% of cases in all ages were SSM and 53% were "other or not otherwise specified" melanomas. Another reason for a lower percentage of SSM in our study is that the percentage of SSM tends to decrease with age, whereas that of LM tends to increase with age (25,26,31). Indeed, in our data, 27% of persons 65–74 years old had SSM and 25% had LM, whereas persons 75 years old or older had 18% and 33%, respectively.

This study has limitations. First, study findings apply mainly to older patients enrolled in Medicare. Second, we did not have data for other host factors (e.g., nutritional status, depression) or treatment that could affect survival from melanoma in widowed persons (33,34). However, this study has some strengths. First, we demonstrated the effect of marital status, specifically being widowed, on stage at diagnosis and survival from melanoma adjusting for other relevant variables. Second, the SEER–Medicare–linked database used in our study is considered a complete database, whereas SEER maintains a standard case ascertainment of 98%, the SEER–Medicare link is able to capture 88% of melanoma cases (35).

Our results have implications. Our finding that widowed persons were more likely to be diagnosed as having late-stage melanoma is consistent with the finding that patients had difficulty detecting less visible lesions on self-examination. A study confirmed the importance of a spouse in detecting many melanomas (36). Indeed, a spouse was the third most common person (after the index patient and a physician) to detect a melanoma. Then, skin-screening programs should target unmarried older persons with the goal of early melanoma detection. Also, teaching about skin self-examination or physician surveillance of melanoma is especially important for widowed older patients.

Conclusion
Older widowed persons were more likely to be diagnosed at a late stage of melanoma and were more likely to die from melanoma than were older married persons. Further research is needed to determine whether widowhood leads to worse biologic characteristics of the tumor (e.g., ulceration) or reduced early detection and/or resection of melanoma in older adults.


   Acknowledgments
Top
 Abstract
 Methods
 Results
 Discussion
 References
 
This work was supported by grant R24 HS011618-04 from the Agency for Healthcare Research and Quality and in part by the University of Texas Medical Branch, Center on Population Health and Health Disparities (grant NIH P50CA105631).

We thank Dr. Sarah Toombs-Smith for her editing assistance.

An earlier version of this work was presented as a poster at the 2006 Annual Scientific Meeting of The Gerontological Society of America in Dallas, Texas.


   Footnotes
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 Methods
 Results
 Discussion
 References
 
Decision Editor: Luigi Ferrucci, MD, PhD

Received September 11, 2006

Accepted November 8, 2006


   References
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 Abstract
 Methods
 Results
 Discussion
 References
 

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