Abstract
Purpose
Cancer survivors are more likely to report having a poor health status when compared to the general population. Few studies have focused on the impact of cancer on health status and healthcare utilization/access outcomes among women from medically underserved populations.
Methods
25,741 women with and without a history of cancer from the National Health and Nutrition Examination Survey from 1999 to 2016 contributed data. Adjusted odds ratios (aORs) and 95% confidence intervals (CIs) were estimated using multivariable logistic regression for associations between cancer status and perceived health and healthcare utilization/access outcomes stratified by race/ethnicity, poverty status, education, and comorbidities.
Results
1,897 (7.0%) women had a history of cancer with breast cancer as the most common (n = 671, 35.7%). While most survivors were non-Hispanic white (69.4%), 13.9% were Hispanic, 12.0% were non-Hispanic Black, and 4.6% were additional racial/ethnic groups. Survivors were 1.32 times more likely to be hospitalized within the last year (95% CI 1.11–1.58) and 1.32 times more likely to see a mental health provider within the last year (95% CI 1.05–1.66) compared to cancer-free women. Race/ethnicity was a significant effect modifier in the association between being a survivor and seeing a mental health provider, with Hispanic survivors having the highest odds (aOR 3.44; 95% CI 2.06–5.74; p-interaction < 0.00).
Conclusion
Our study identifies disparities in healthcare utilization among female cancer survivors, highlighting the importance of evaluating these associations among medically underserved populations. These findings can educate healthcare professionals working with these populations to inform gaps in survivorship care utilization/access.
Keywords: Cancer survivors, general health, Healthcare utilization, Disparities
Introduction
In 2020, there were an estimated 16.9 million cancer survivors living in the United States (US), with more than 67% surviving more than five years post-diagnosis [1]. The National Cancer Institute (NCI) [2] estimated that female cancers comprised 48.8% of all new cancers, with the most common, breast (30%), lung/bronchus (13%), and colorectal (8%) accounting for approximately 50% of new cancer cases. Surviving cancer does not guarantee higher quality of life (QOL) or overall betterment of health, as there are many complications from cancer treatment, recurrence, and related comorbid conditions that occur throughout survivorship [3-5]. Past literature has shown that cancer survivors, in general, are more likely to report poorer health status when compared to individuals without cancer [5]. Women are more likely to be long-term survivors of cancer [1, 6] and account for a large proportion of cancer survivors [1], which necessitates the importance of focusing on a female-only sample. Specifically, female cancer survivors face barriers to successful and long-term health, including several physical and psychosocial aspects (e.g., related comorbid conditions, recurrence, mental health outcomes, etc.) that span the entire cancer continuum, a framework that describes the understanding and experience from cancer etiology to survivorship [7].
Much of past healthcare utilization research focusing on female cancer survivors has concentrated on the role of fear of recurrence [8, 9], and by association, continuous cancer screening [10] and healthcare utilization [11, 12]. Despite increased utilization, there are groups such as medically underserved populations (e.g., racial/ethnic minorities, those of lower socioeconomic position [SEP], those with lower educational attainment, those with chronic conditions, etc.) that under-utilize routine healthcare during cancer survivorship [13, 14]. Cancer survivors have an increased risk of recurrence compared to the general population’s risk for initial cancer [15-18], and this risk is worsened by pertinent barriers to preventive cancer care, unfortunately leading to increases in cancer-oriented morbidity and mortality among these groups [19, 20]. Cancer survivors may experience fewer barriers to cancer care and healthcare than the general population due to previous care utilization [21], but it is especially important to note that these barriers remain widespread among those of medically underserved populations which may be exacerbated among cancer survivors [22]. Healthcare utilization relies on access, with cancer survivors noting barriers in communication, transportation, financial hardships, and social influences [23-26] as well as care quality [27-30]. Few studies have focused on the impact and resonance of cancer on perceived health as well as healthcare utilization and access among women from medically underserved populations on a national level [31]. While past literature has focused on how fear of recurrence [9] and how perceived health impacts adherence to survivorship care plans [32], there remain gaps in our understanding of these associations with perceived health and healthcare utilization post-diagnosis among medically underserved cancer populations.
Objectives
The current study aims to determine the association between being a female cancer survivor vs cancer-free women and a number of health-related outcomes (i.e., perceived health status, presence of routine healthcare, type of place visited for routine healthcare, seeing a mental health provider in the last year, hospitalizations in the last year), adjusting for covariates. Secondarily, we hope to determine such associations between survivor/cancer-free status and the health-related outcomes listed above stratified by FPL, education, race/ethnicity, and comorbidity status.
Materials and methods
NHANES data and sample
The current study utilized publicly available data from the continuous National Health and Nutrition Examination Survey (NHANES, administered and collected by the National Center for Health Statistics (NCHS) from the Centers for Disease Control and Prevention (CDC)). NHANES is national program that assesses the health of adults and children in the US. Since 1999, this survey is collected on 2-year continuous cycles of the civilian, non-institutionalized population, providing information on the health of the US population. Participants are recruited through a four-stage, complex stratified probability clustered sampling design [33-35] where approximately 7,000 US residents from 15 counties are randomly contacted for participation yearly. Data are collected via interviews, laboratory tests, and physical examinations with sample weights assigned to each participant based upon the number of people that the participant represents within the US Census population [33-35]. The data collection methods, participant information, and description of ancillary studies for NHANES are available on the NHANES website [36]. For the purposes of the current study, NHANES interview data collected from 1999 to 2016 were combined and weighted appropriately.
The NHANES was approved by the NCHS Research Ethics Review Board and written informed consent was obtained from all participants [34]. The current cross-sectional study included 27,607 women who contributed data from 1999 to 2016. Inclusion criteria included completing the NHANES questionnaire, being an adult female (NHANES adult age is ≥ 20 years), reporting whether a cancer or malignancy was ever diagnosed in the past and being less than two years post-primary cancer diagnosis. Figure 1 depicts a study flow diagram detailing exclusions.
Fig. 1.
Flow diagram of the process through which NHANES 1999–2016 participants were excluded for the current analysis
Model variables
Predictor variable
Participants were stratified into groups of those reporting a history of any type of cancer and those without a history of cancer according to the question, “Have you ever been told you had cancer or malignancy?” [36]. This variable was binary (cancer-free, cancer survivor) and denoted as survivor/cancer-free status. Participants who reported a previous non-melanoma skin cancer diagnosis, where this was the only cancer found, were removed from the analysis and were ineligible to be cancer-free status. Women who were within two years of primary cancer diagnosis were removed to account for the possibility of being in active treatment.
Outcome assessment
According to NHANES [36], the Hospital Utilization and Access to Care section (HUQ) provides respondent-level self-reported health status and access to healthcare questions. The current study utilized five outcomes from the NHANES HUQ section of the in-home interview to determine overall health and healthcare utilization: (1) general health perception (missing 12.4%), (2) routine place to go for healthcare (missing 0.01%), (3) type of place most often go for healthcare (missing 11.7%), (4) seen mental health professional in last year (missing 0.1%), and (5) hospitalized in the last year (missing 0.1%) [36]. The sixth NHANES HUQ outcome (time since last healthcare visit) was removed from the current analyses due to high missingness (86.0%).
Original polynomial response options were transformed for the purposes of analysis. General health perception, set upon a five-point Likert scale ranging from one (excellent) to five (poor), was dichotomized (excellent/very good/good, fair/poor). Having a routine place to go for healthcare presented with three response options (yes, there is no place, there is more than one place) but was transformed (no, yes, or more than one place). The type of place most often went for healthcare was only analyzed among the subset of individuals who had identified as having one or more routine place for healthcare. The original variable had six response options (clinic/healthcare center, doctor’s office/health management organization [HMO], hospital emergency room [ER], hospital outpatient department, some other place, does not go to one place most often) which was condensed (doctor’s office or health management office, clinic or health center, hospital ER or outpatient department, other place or no one place). The last two outcomes, seeing a mental health professional within the last year and being hospitalized within the last year, were both originally dichotomous with ‘no’ as the referent group.
Covariates and stratifications
The following variables were accounted for and included as covariates across all models: age at interview in years, education, marital status, FPL, BMI status, smoking status, alcoholic drinks per day, health insurance status, exercise, and years since initial cancer diagnosis. Age at interview and alcoholic drinks per day were treated as continuous. Race/ethnicity was originally a polynomial variable (Mexican American, other Hispanic, non-Hispanic white, non-Hispanic Black, other race [includes multi-racial]) but was condensed into a four-level variable for the purposes of analyses (non-Hispanic white, non-Hispanic Black, Hispanic [includes Mexican American and other Hispanic], additional races [includes multiracial]). Polynomial categorical variables were dichotomized into the following variables: education (less than or equal to high school, some college or more [includes college graduates and professional degrees]), marital status (not married, married), BMI status categorized from height/weight body measures (underweight/normal, overweight/obese), smoking status (never smoked, former/current smoker), health insurance status (no, yes), current exercise (no, yes), poverty status (below FPL, at or above FPL), and comorbidity status (no comorbidities, comorbidities). Participant comorbidity status was determined using NHANES medical condition (MCQ) variables denoting several chronic conditions in addition to cancer (e.g., asthma, hay fever, anemia, obesity, blood transfusions, arthritis, gout, heart disease, stroke, lung diseases, thyroid issues, liver disease, jaundice, etc.). If participants answered affirmatively to any of the chronic conditions presented, they were considered to have a comorbidity.
Smoking status was combined from NHANES cigarette smoking variables, currently smoke cigarettes, and time since quitting cigarettes. Participants were considered current smokers if they had answered current smoking status as ‘every day’ or ‘some days’ and considered former smokers if they had reported any amount of time since quitting. The FPL variable was created using the NHANES-calculated poverty–income ratio (PIR) continuous variable which ranged from zero to 5.00, with the latter indicating a PIR greater or equal to five [37]. A PIR value below 1.00 was indicative of living below the FPL and 1.00 or greater indicative of living above the FPL. Exercise status was determined from several NHANES physical activity variables outlining low/walking-, moderate-, and/or vigorous-intensity physical activity. The transformed variable (no/yes) was affirmative if the participant denoted participating in any form of the above PA. Analyses were stratified by several variables: education, FPL, race/ethnicity, and comorbidity status. All stratified variables were entered as covariates in models when they were not being used for stratification.
Statistical methods
The NHANES uses a complex, multistage sampling design with stratification, applying weights per participant to statistically represent a proportion of individuals in the general population using interview weighting mechanisms [36]. All analyses were performed using IBM SPSS complex survey sampling software version 27 [38] and Stata statistical software version 16 [39], following applicable NHANES analytic guidelines [40]. The Stata svyset code and SPSS Complex Sampling feature allows the inclusion of all sampling design elements, stratification, clusters, and appropriate weights [33]. Therefore, sampling weights were used in all analyses to account for the complex survey design and survey non-response. The current study approached missing data by excluding women from specific models if they were missing a variable in that model. Missing values are depicted per variable within Table 1, stratified by cancer survivor versus cancer-free group.
Table 1.
Participant covariate, predictor, and outcome characteristics—National Health and Nutrition Examination Survey, years 1999–2016, females only
| Characteristics | Predictor |
p-value | Total female sample (N = 27,089) No. (%) |
|
|---|---|---|---|---|
| Cancer-free women (n = 25,192) |
Survivors (n = 1,897) | |||
| No. (%) | No. (%) | |||
| Covariates | ||||
| Marital status | ||||
| Married | 11,129 (44.2) | 853 (45.0) | < 0.000 | 11,982 (44.2) |
| Widowed | 2,820 (11.2) | 487 (25.7) | 3,307 (12.2) | |
| Divorced | 2,603 (10.3) | 279 (14.7) | 2,882 (10.6) | |
| Separated | 921 (3.7) | 57 (3.0) | 978 (3.6) | |
| Never married | 4,975 (19.7) | 124 (6.5) | 5,099 (18.8) | |
| Living with partner | 1,686 (6.7) | 76 (4.0) | 1,762 (6.5) | |
| Missing | 1,058 (4.2) | 21 (1.1) | 1,079 (4.0) | |
| Obesity | ||||
| Underweight (BMI below 18.5) | 539 (2.1) | 40 (2.1) | 0.598 | 579 (2.1) |
| Normal (BMI 18.5–24.9) | 7,271 (28.9) | 511 (26.9) | 7,782 (28.7) | |
| Overweight (BMI 25.0–29.9) | 6,705 (26.6) | 514 (27.1) | 7,219 (26.6) | |
| Obese (BMI 30.0 +) | 9,001 (35.7) | 670 (35.3) | 9,671 (35.7) | |
| Missing | 1,676 (6.7) | 162 (8.5) | 1,838 (6.8) | |
| Smoking status | ||||
| Never smoked | 15,322 (65.0) | 998 (53.1) | 0.002 | 16,320 (60.2) |
| Former or current smoker | 8,259 (35.0) | 881 (46.9) | 9,140 (39.8) | |
| Missing | 0 (0.0) | 0 (0.0) | 0 (0.0) | |
| Covered by health insurance& | ||||
| No insurance coverage | 5,157 (20.5) | 170 (9.0) | < 0.000 | 21,576 (79.6) |
| Insurance coverage | 19,856 (78.8) | 1,720 (90.7) | 5,327 (19.7) | |
| Missing | 179 (0.7) | 7 (0.4) | 186 (0.7) | |
| Current exercise | ||||
| No | 8,520 (33.8) | 800 (42.2) | < 0.000 | 9,320 (34.4) |
| Yes | 16,660 (66.1) | 1,097 (57.8) | 17,757 (65.6) | |
| Missing | 12 (0.0) | 0 (0.0) | 12 (0.0) | |
| Education | ||||
| Less than 9th grade | 2,871 (11.4) | 206 (10.9) | 0.040 | 3,077 (11.4) |
| 9–11th grade | 3,560 (14.1) | 256 (13.5) | 3,816 (14.1) | |
| High school graduate or GED | 5,214 (20.7) | 457 (24.1) | 5,671 (20.9) | |
| Some college or associate degree | 6,815 (27.1) | 573 (30.2) | 7,388 (27.3) | |
| College graduate or above | 4,778 (19.0) | 403 (21.2) | 5,181 (19.1) | |
| Missing | 1,954 (7.5) | 2 (0.1) | 1,956 (7.2) | |
| Poverty status based on FPL | ||||
| Below FPL | 5,611 (22.3) | 323 (17.0) | < 0.000 | 5,934 (21.9) |
| At or above FPL | 17,190 (68.2) | 1,392 (73.4) | 18,582 (68.6) | |
| Missing | 2,391 (9.5) | 182 (9.6) | 2,573 (9.5) | |
| Race/ethnicity | ||||
| Mexican American | 4,957 (19.7) | 160 (8.4) | < 0.000 | 5,117 (18.9) |
| Other Hispanic | 2,234 (8.9) | 105 (5.5) | 2,339 (8.6) | |
| Non-Hispanic white (NHW) | 10,284 (40.8) | 1,317 (69.4) | 11,601 (42.8) | |
| Non-Hispanic Black | 5,576 (22.1) | 227 (12.0) | 5,803 (21.4) | |
| Other (including multi-racial) | 2,141 (8.5) | 88 (4.6) | 2,229 (8.2) | |
| Missing | 0 (0.0) | 0 (0.0) | 0 (0.0 | |
| Comorbidity status | ||||
| No comorbid conditions | 14,524 (57.7) | 1,633 (86.1) | < 0.000 | 16,157 (59.6) |
| Comorbid conditions | 10,668 (42.3) | 264 (13.9) | 10,932 (40.4) | |
| Missing | 0 (0.0) | 0 (0.0) | 0 (0.0) | |
| Outcomes | ||||
| General health perception | ||||
| Excellent | 2,309 (9.2) | 107 (5.6) | < 0.000 | 2,416 (8.9) |
| Very good | 5,976 (23.7) | 435 (22.9) | 6,411 (23.7) | |
| Good | 8,484 (33.7) | 650 (34.3) | 9,134 (33.7) | |
| Fair | 4,397 (17.5) | 386 (20.3) | 4,783 (17.7) | |
| Poor | 846 (3.4) | 135 (7.1) | 981 (3.6) | |
| Missing | 3,180 (12.6) | 184 (9.7) | 3,364 (12.4) | |
| Routine place for healthcare | ||||
| Yes | 21,923 (87.0) | 1,790 (94.4) | < 0.000 | 23,713 (87.5) |
| There is no place | 3,085 (12.2) | 94 (5.0) | 3,179 (11.7) | |
| There is more than one place | 182 (0.7) | 13 (0.7) | 195 (0.7) | |
| Missing | 2 (0.0) | 0 (0.0) | 2 (0.0) | |
| Type of place for routine healthcare¥ | ||||
| Clinic or health center | 5,529 (21.9) | 313 (16.5) | < 0.000 | 5,842 (21.6) |
| Doctor’s office | 15,333 (60.9) | 1,403 (74.0) | 16,736 (61.8) | |
| Hospital ER | 631 (2.5) | 37 (2.0) | 668 (2.5) | |
| Hospital outpatient department | 370 (1.5) | 37 (2.0) | 407 (1.5) | |
| Some other place | 217 (0.9) | 13 (0.7) | 230 (0.8) | |
| Does not go to one place most often | 20 (0.1) | 0 (0.0) | 20 (0.1) | |
| Missing | 3,123 (12.2) | 94 (5.0) | 3,181 (11.7) | |
| Hospitalized in the last year | ||||
| No | 21,708 (86.2) | 1,539 (81.1) | < 0.000 | 23,247 (85.8) |
| Yes | 3,471 (13.8) | 357 (18.8) | 3,828 (14.1) | |
| Missing | 13 (0.0) | 1 (0.1) | 14 (0.1) | |
| Seen a mental health provider in the last year | ||||
| No | 23,143 (91.9) | 1,700 (89.6) | 0.007 | 24,843 (91.7) |
| Yes | 2,036 (8.1) | 196 (10.3) | 2,232 (8.2) | |
| Missing | 13 (0.0) | 1 (0.1) | 1 (0.0) | |
| Covariates | Mean (SD) | Mean (SD) | p-value | Mean (SD) |
| Age at NHANES interview | 45.7 (19.2) | 63.2 (15.5) | < 0.000 | 47.0 (19.5) |
| Years since diagnosis | – | 15.3 (11.6) | – | – |
| Alcoholic drinks per day | 1.44 (19.1) | 1.45 (22.9) | 0.991 | 1.44 (19.4) |
FPL federal poverty level, as reported by NHANES interview
All analyses utilized NHANES sampling weights to account for the complex survey design and survey non-response
Covered by health insurance at the time of NHANES interview
Only asked if participant answered “yes” or “more than one place” to the question pertaining to routine place for healthcare; ER = emergency room
Bolded font indicates significant p-value (< .05)
All study variables were evaluated using descriptive statistics and graphical techniques to assess distributional assumptions. In preliminary analyses to identify confounders of interest, demographic, and other variables collected from NHANES were assessed by univariate analyses using Chi-square tests for categorical variables and t-tests for continuous variables. Adjusted odds ratios (aORs) and 95% confidence intervals (CIs) were calculated with multivariable and multinomial logistic regression models to measure the association between predictors and outcomes, while adjusting for covariates. Statistical significance was indicated if p-values or p-interaction terms were below 0.05.
Results
Characteristics of the study sample
Description of the study population and characteristics are shown in Table 1. A total of 27,089 women with and without a history of cancer meeting inclusion criteria were included in the study population from the continuous NHANES (1999 to 2016). A total of 1,897 women (7.0%), aged 20 to 85 years (M = 63.2, SD = 15.5, range = 20–85 years), reported a history of cancer with breast cancer being the most common site (n = 671, 35.7%). Most survivors were non-Hispanic white (69.4%), had some college education (51.4%), and were married (45.0%) (Table 1). Survivors reported an average of 15.3 years since initial cancer diagnosis (SD = 11.6, range = 2.0–84). The characteristics among the women without cancer (n = 25,192, 92.9%) differed from survivors. The majority of survivors were more educated, were married, lived above the FPL, never smoked, had health insurance, exercised, were non-Hispanic white, and were older (M = 63.2, SD = 15.5, range = 20–85 years). There were statistically significant differences between survivors and cancer-free groups for all covariates (e.g., age, education, marital status, FPL, smoking status, health insurance coverage, current exercise, race/ethnicity, comorbidity status), except BMI category, and all study outcomes.
Overall health and hospital utilization by survivor/control status and stratifications
Table 2 depicts the associations between survivor/cancer-free status and odds of reporting poor health status. Overall, survivors had 1.24 times the odds of reporting fair or poor perceived health compared to women without cancer (95% CI 1.02–1.50). Among women at or above the FPL, survivors had 2.13 greater odds of reporting fair or poor perceived health than cancer-free women (95% CI 1.46–3.12); however, among women below the FPL, the association was attenuated and was not statistically significant (aOR 1.09; 95% CI 0.88–1.36, p-interaction = 0.003). Survivors who had at least some college education were 1.29 times more likely to report fair or poor perceived health (95% CI 1.04–1.59) than cancer-free women with at least some college education. Survivors who were non-Hispanic white had 1.30 times the odds of reporting fair or poor perceived health compared to non-Hispanic white women without cancer (95% CI 1.04–1.62). Hispanic (aOR 1.79, 95% CI 1.02–3.11) and other race/multiracial survivors (aOR 2.43, 95% CI 1.14–5.18) also were more likely to report poor perceived health in comparison with Hispanic and other race/multiracial cancer-free women, respectively. Education, race/ethnicity, and comorbidity history did not modify the association between survivor/cancer-free status and general health perception.
Table 2.
Multivariable adjusted odds ratios and 95% confidence intervals for worse general health perception associated with survivor/cancer-free status, overall and stratified among women in NHANES 1999–2016
| Stratifications | Cancer-free women (n = 25,192) |
Survivors (n = 1,897) | p-interaction | ||||
|---|---|---|---|---|---|---|---|
|
|
|
||||||
| N | aOR | 95% CI | N | aOR | 95% CI | ||
| Overall | 22,012 | 1.00 | Reference | 1,890 | 1.24 | 1.02–1.50 | |
| FPL | |||||||
| At or above | 15,297 | 1.00 | Reference | 1,392 | 2.13 | 1.46–3.12 | 0.003 |
| Below | 4,805 | 1.00 | Reference | 323 | 1.09 | 0.880–1.36 | |
| Education | |||||||
| At least some college* | 10,178 | 1.00 | Reference | 976 | 1.29 | 1.04–1.59 | 0.648 |
| ≤ High school | 1,415 | 1.00 | Reference | 919 | 1.19 | 0.887–1.60 | |
| Race/ethnicity | |||||||
| Non-Hispanic white | 10,284 | 1.00 | Reference | 1,317 | 1.30 | 1.04–1.62 | |
| Non-Hispanic Black | 5,576 | 1.00 | Reference | 227 | 1.25 | 0.852–1.85 | 0.858 |
| Hispanic£ | 7,185 | 1.00 | Reference | 265 | 1.79 | 1.02–3.11 | 0.291 |
| Other race and multiracial | 2,141 | 1.00 | Reference | 88 | 2.43 | 1.14–5.18 | 0.111 |
| Comorbidity | |||||||
| Have comorbidities | 12,896 | 1.00 | Reference | 264 | 1.08 | 0.588–2.00 | 0.749 |
| No comorbid conditions | 9,116 | 1.00 | Reference | 1,633 | 1.20 | 0.984–1.47 | |
All analyses utilized NHANES sampling weights to account for the complex survey design and survey non-response
Bold font indicates statistically significant with corresponding p < 0.05
Models adjusted for age at interview in years, education, marital status, FPL, BMI status, smoking status, alcoholic drinks per day, health insurance status, and exercise
p-interaction indicates interaction between survivors and cancer-free women upon stratification
General health perception was dichotomous (excellent/very good/good; fair/poor)
FPL federal poverty level, BMI body mass index
Includes college graduates and professional degrees
Includes Mexican American and other Hispanic participants
Table 3 shows the relationship between survivor/cancer-free status and odds of having no one place for routine healthcare. The association between survivor status and presence of routine healthcare overall was not statistically significant (aOR 0.95, 95% CI 0.72–1.27) and associations were not statistically significant among any strata.
Table 3.
Multivariable adjusted odds ratios and 95% confidence intervals for having a place for routine healthcare associated with survivor/cancer-free status, overall and stratified among women in NHANES 1999–2016
| Stratifications | Cancer-free women (n = 25,192) |
Survivors (n = 1,897) | p-interaction | ||||
|---|---|---|---|---|---|---|---|
|
|
|
||||||
| N | aOR | 95% CI | N | aOR | 95% CI | ||
| Overall | 25,190 | 1.00 | Reference | 1,897 | 0.957 | 0.721–1.27 | |
| FPL | |||||||
| At or above | 17,189 | 1.00 | Reference | 1,392 | 1.24 | 0.782–1.99 | 0.231 |
| Below | 5,610 | 1.00 | Reference | 323 | 0.902 | 0.659–1.23 | |
| Education | |||||||
| At least some college* | 11,593 | 1.00 | Reference | 976 | 1.00 | 0.644–1.55 | 0.788 |
| ≤ High school | 13,540 | 1.00 | Reference | 919 | 0.927 | 0.649–1.32 | |
| Race/ethnicity | |||||||
| Non-Hispanic white | 10,284 | 1.00 | Reference | 1,317 | 0.833 | 0.603–1.15 | |
| Non-Hispanic Black | 5,575 | 1.00 | Reference | 227 | 2.58 | 0.701–9.52 | 0.101 |
| Hispanic£ | 7,185 | 1.00 | Reference | 265 | 1.46 | 0.794–2.69 | 0.107 |
| Other race & multiracial | 2,140 | 1.00 | Reference | 88 | 2.19 | 0.738–6.50 | 0.097 |
| Comorbidity | |||||||
| Have comorbidities | 14,523 | 1.00 | Reference | 264 | 0.745 | 0.421–1.31 | 0.401 |
| No comorbid conditions | 10,667 | 1.00 | Reference | 1,633 | 0.977 | 0.722–1.32 | |
All analyses utilized NHANES sampling weights to account for the complex survey design and survey non-response
Bold font indicates statistically significant with corresponding p < 0.05
Models adjusted for age at interview in years, education, marital status, FPL, BMI status, smoking status, alcoholic drinks per day, health insurance status, and exercise
p-interaction indicates interaction between survivors and cancer-free women upon stratification
Having a place for routine healthcare was dichotomous (yes or having more than one place; no one place)
FPL federal poverty level, BMI body mass index
Includes college graduates and professional degrees
Includes Mexican American and other Hispanic participants
Table 4 presents the association between survivor/cancer-free status and type of routine healthcare. Overall, there were no significant differences between cancer-free women and survivors. For associations stratified by FPL, cancer survivors living at or above the FPL had lower odds of reporting a clinic or health center than cancer-free women living above the FPL (aOR 0.61, 95% CI 0.43–0.87; p-interaction = 0.036), whereas the association was not statistically significant among women living below the FPL. Among women with some college, survivor status was associated with lower odds of utilizing clinic/healthcare centers compared to cancer-free women with some college (aOR 0.70, 95% CI 0.53–0.91), and this interaction was not significant. When stratified by race/ethnicity, multiracial or other race cancer survivors had significantly lower odds (aOR 0.14, 95% CI 0.30–0.0.69, p-interaction ≤ 0.00) of reporting some other place or no one place as their routine care location compared to multiracial or other race cancer-free women. Comorbidity status was not a significant modifier for the association with place for routine healthcare.
Table 4.
Multinomial adjusted odds ratios and 95% confidence intervals for place for routine healthcare associated with survivor/cancer-free status, overall and stratified among women in NHANES 1999–2016
| Outcome: Place for Routine Care | |||||||||
|---|---|---|---|---|---|---|---|---|---|
| Clinic or Healthcare Center (n = 5,842) vs Doctor’s Office/HMO (N = 16,736) |
Hospital ER or Outpatient Dept (N = 1,075) vs Doctor’s Office/HMO (N = 16,736) |
Some Other Place or No One Place (N = 250) vs Doctor’s Office/HMO (N = 16,736) |
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| aOR | 95% CI | p-int | aOR | 95% CI | p-int | aOR | 95% CI | p-int | |
| Overall | |||||||||
| Population cancer-free women | 1.00 | Referent | 1.00 | Referent | 1.00 | Referent | |||
| Female cancer survivors | 0.878 | 0.733–1.05 | 1.10 | 0.707–1.72 | 1.12 | .546–2.33 | |||
| Stratified variables | |||||||||
| Poverty level | |||||||||
| At or above | 0.609 | 0.427–0.870 | 0.036 | 0.901 | 0.478–1.69 | 0.496 | 0.566 | 0.117–2.73 | 0.407 |
| Below | 0.943 | 0.773–1.15 | 1.15 | 0.691–1.94 | 1.26 | 0.550–2.92 | |||
| Education | |||||||||
| At least some college* | 0.700 | 0.534–0.916 | 0.068 | 0.701 | 0.424–1.15 | 0.061 | 0.301 | 0.064–1.40 | 0.071 |
| ≤ High school | 1.02 | 0.786–1.32 | 1.72 | 0.949–3.12 | 1.43 | 0.648–3.16 | |||
| Race/ethnicity | |||||||||
| Non-Hispanic White | 0.932 | 0.757–1.14 | 1.28 | 0.753–2.20 | 1.16 | 0.526–2.58 | |||
| Non-Hispanic Black | 0.812 | 0.556–1.18 | 0.525 | 1.39 | 0.675–2.86 | 0.854 | 1.48 | 0.193–11.3 | 0.827 |
| Hispanic£ | 0.755 | 0.459–1.24 | 0.445 | 0.443 | 0.182–1.07 | 0.051 | 1.09 | 0.233–5.09 | 0.936 |
| Other race or multiracial | 1.07 | 0.465–2.46 | 0.751 | 1.98 | 0.485–8.08 | 0.564 | 0.146 | 0.308–0.697 | < 0.000 |
| Comorbidity status | |||||||||
| None | 0.731 | 0.451–1.18 | 0.383 | 1.20 | 0.473–3.04 | 0.816 | 1.80 | 0.521–6.25 | 0.422 |
| Yes | 0.915 | 0.757–1.10 | 1.06 | 0.648–1.74 | 0.933 | 0.361–2.41 | |||
All analyses utilized NHANES sampling weights to account for the complex survey design and survey non-response
Models adjusted for age at interview in years, education, marital status, poverty level, BMI status, smoking status, alcoholic drinks per day, health insurance status, and exercise
Place for routine healthcare (doctor’s office/HMO [referent], clinic or health center, hospital ER/outpatient, some other place/no one place)
Bond font indicates statistically significant with corresponding p < 0.05
p-interaction indicates interaction between survivors and cancer-free women upon stratification
HMO health maintenance office, ER emergency room, BMI body mass index
Includes college graduates and professional degrees
Includes Mexican American and other Hispanic participants
Table 5 depicts the relationship between survivors and cancer-free women and odds of seeing a mental health professional within the last year. Overall, survivors reported 1.32 greater odds (95% CI 1.05–1.66) of seeing a mental health provider within the last year versus cancer-free women. While FPL, education, and comorbidity status were not significant modifiers of the association between survivor/cancer-free status and seeing a mental health provider within the last year, race/ethnicity did significantly modify this association. Hispanic cancer survivors were 3.44 times more likely (95% CI 2.06–5.74, p-interaction = 0.00) to report seeing a mental health professional in the last year compared to cancer-free Hispanic women. Similarly, non-Hispanic Black cancer survivors (aOR 1.83, 95% CI 1.09–3.07) compared to non-Hispanic Black cancer-free women were more than two times more likely to report seeing a mental health provider. Cancer survivors living at or above the FPL were 1.62 times more likely (95% CI 1.01–2.61) to report seeing a mental health provider in the last year compared with cancer-free women living at or above the FPL. Survivors with a high school diploma or less were 1.38 times more likely to report seeing a mental health provider within this timeframe (95% CI 1.04–1.84) in comparison with cancer-free women with a high school diploma or less education.
Table 5.
Multivariable adjusted odds ratios and 95% confidence intervals for seeing a mental health provider in the last year associated with survivor/cancer-free status, overall and stratified among women in NHANES 1999–2016
| Stratifications | Cancer-free women (n = 25,192) |
Survivors (n = 1,897) | p-interaction | ||||
|---|---|---|---|---|---|---|---|
|
|
|
||||||
| n | aOR | 95% CI | n | aOR | 95% CI | ||
| Overall | 25,179 | 1.00 | Reference | 1,890 | 1.32 | 1.05–1.66 | |
| FPL | |||||||
| At or above | 17,183 | 1.00 | Reference | 1,392 | 1.62 | 1.01–2.61 | 0.354 |
| Below | 5,609 | 1.00 | Reference | 323 | 1.26 | 0.981–1.62 | |
| Education | |||||||
| At least some college* | 11,589 | 1.00 | Reference | 976 | 1.19 | 0.841–1.69 | 0.497 |
| ≤ High school | 13,534 | 1.00 | Reference | 919 | 1.38 | 1.04–1.84 | |
| Race/ethnicity | |||||||
| Non-Hispanic white | 10,278 | 1.00 | Reference | 1,317 | 1.18 | 0.919–1.51 | |
| Non-Hispanic Black | 5,573 | 1.00 | Reference | 227 | 1.83 | 1.09–3.07 | 0.132 |
| Hispanic£ | 7,184 | 1.00 | Reference | 265 | 3.44 | 2.06–5.74 | < 0.000 |
| Other race and multiracial | 2,138 | 1.00 | Reference | 88 | 0.948 | 0.365–2.46 | 0.664 |
| Comorbidity | |||||||
| Have comorbidities | 14,514 | 1.00 | Reference | 264 | 1.73 | 0.992–3.02 | 0.232 |
| No comorbid conditions | 10,665 | 1.00 | Reference | 1,633 | 1.21 | 0.956–1.53 | |
All analyses utilized NHANES sampling weights to account for the complex survey design and survey non-response
Bold font indicates statistically significant with corresponding p < 0.05
Models adjusted for age at interview in years, education, marital status, FPL, BMI status, smoking status, alcoholic drinks per day, health insurance status, and exercise
p-interaction indicates interaction between survivors and cancer-free women upon stratification
Seen a mental health provider in the last year (no, yes)
FPL federal poverty level, BMI body mass index
Includes college graduates and professional degrees
Includes Mexican American and other Hispanic participants
Table 6 outlines the association between survivors and cancer-free women and odds of being hospitalized within the last year. Survivors had 1.32 times the odds (95% CI 1.11–1.58) of reporting hospitalizations within the last year compared to cancer-free women. Overall, FPL, education, race/ethnicity, and comorbidity status were not significant modifiers of the association between survivor/cancer-free status and odds of being hospitalized in the last year. Both cancer survivors living at or above (aOR 1.61, 95% CI 1.16–2.22) or below the FPL (aOR 1.27, 95% CI 1.05–1.54) were significantly more likely to report being hospitalized within the last year compared to similar cancer-free women. Survivors reporting a high school diploma or less were 1.34 times more likely to be hospitalized within this timeframe (95% CI 1.08–1.66) compared to their cancer-free counterparts at similar educational levels. Cancer survivors without comorbidities were significantly more likely (aOR 1.36, 95% CI 1.15–1.60) to be hospitalized within the past year compared to cancer-free women without comorbidities. By race/ethnicity, non-Hispanic white (aOR 1.34, 95% CI 1.10–1.64) and non-Hispanic Black cancer survivors (aOR 1.52, 1.01–2.30) were significantly more likely to report being hospitalized during this time compared to their cancer-free counterparts, respectively.
Table 6.
Multivariable adjusted odds ratios and 95% confidence intervals for being hospitalized in the last year associated with survivor/cancer-free status, overall and stratified among women in NHANES 1999–2016
| Stratifications | Cancer-free women (n = 25,192) |
Survivors (n = 1,897) | p-interaction | ||||
|---|---|---|---|---|---|---|---|
|
|
|
||||||
| n | aOR | 95% CI | n | aOR | 95% CI | ||
| Overall | 25,179 | 1.00 | Reference | 1,890 | 1.32 | 1.11–1.58 | |
| FPL | |||||||
| At or above | 17,186 | 1.00 | Reference | 1,392 | 1.61 | 1.16–2.22 | 0.200 |
| Below | 5,606 | 1.00 | Reference | 323 | 1.27 | 1.05–1.54 | |
| Education | |||||||
| At least some college* | 11,587 | 1.00 | Reference | 976 | 1.31 | 0.994–1.73 | 0.904 |
| ≤ High school | 13,535 | 1.00 | Reference | 919 | 1.34 | 1.08–1.66 | |
| Race/ethnicity | |||||||
| Non-Hispanic white | 10,279 | 1.00 | Reference | 1,317 | 1.34 | 1.10–1.64 | |
| Non-Hispanic Black | 5,575 | 1.00 | Reference | 227 | 1.52 | 1.01–2.30 | 0.608 |
| Hispanic£ | 7,182 | 1.00 | Reference | 265 | .832 | 0.522–1.32 | 0.051 |
| Other race and multiracial | 2,137 | 1.00 | Reference | 88 | 1.75 | 0.854–3.60 | 0.489 |
| Comorbidity | |||||||
| Have comorbidities | 14,514 | 1.00 | Reference | 264 | .893 | 0.515–1.54 | 0.126 |
| No comorbid conditions | 10,665 | 1.00 | Reference | 1,633 | 1.36 | 1.15–1.60 | |
All analyses utilized NHANES sampling weights to account for the complex survey design and survey non-response
Bold font indicates statistically significant with corresponding p < 0.05
Models adjusted for age at interview in years, education, marital status, FPL, BMI status, smoking status, alcoholic drinks per day, health insurance status, and exercise
p-interaction indicates interaction between survivors and cancer-free women upon stratification
Being hospitalized in the last year (no, yes)
FPL federal poverty level, BMI body mass index
Includes college graduates and professional degrees
Includes Mexican American and other Hispanic participants
Discussion
Among women residing in the US, we examined the associations between having a history of cancer and odds of reporting several health-related outcomes overall and stratified by sociodemographic factors. Among cancer survivors, breast cancer was the most common site, mirroring the recent NCI-reported trends [2]. Most of the current sample was educated and lived above the FPL, which may account for the self-reported higher quality health-related outcomes, as these individuals are more likely to have continuous health insurance coverage and access to quality healthcare when needed [41, 42]. Despite the similarity of patterns among sociodemographic factors, there were differences observed between cancer-free women and survivors for all characteristics except for obesity status. Survivors were more likely to report being hospitalized and seeing a mental health provider within the last year, all of which coincides with higher utilization among cancer patients and survivors [21], particularly among Hispanic women utilizing mental healthcare services. Regardless, it appears as though despite the low indications of poor health outcomes within the current sample, disparities remain between female cancer survivors and population-based cancer-free women.
The perception of quality of healthcare and access to such care remains an important aspect of the cancer survivorship experience [43-47], as well as US females of the general population. Our study showed that female cancer survivors were more likely to be hospitalized and were more likely to visit a mental health provider when compared to cancer-free women. A strong consensus exists that most cancer survivors acclimate well to life post-treatment [48-52], but often depends on the individual and their biopsychosocial response to the cancer experience [53]. While we observed a borderline significant association between cancer survivors and perceived health status, recent literature shows that some cancer survivors may engage in better health behaviors (e.g., following physicians’ recommendations) immediately after diagnosis, but the majority of survivors have been shown to have worse perceived health than individuals without cancer [54]. It may be possible that cancer survivors may perceive their health status as poor due to their previous diagnosis or number of comorbid conditions [21]. This remains a possibility given the results; however, there has been support for a bidirectional relationship between health perception and psychological wellbeing [55], which is imperative for successful survivorship and disease management [56]. When stratified by sociodemographic factors, we found that survivors at or above the FPL exhibited greater chances of poor perceived health compared with women without cancer. Having poorer perceived health often leads to lapses in quality and access to medical care [57], indicative of worsening health over time coupled with cancer treatment toxicities and multimorbidity [58-60]. We also found that survivors who were non-Hispanic white, Hispanic, and those who were other race/multiracial were more likely to report poorer perceived health than non-Hispanic white, Hispanic, and other race/multiracial cancer-free women, respectively, which may suggest that survivors are not receiving necessary care [21, 61]. These women may also perceive their health as poor despite being in remission [62], and could also have greater fear of recurrence, which has been found to mitigate this relationship [63].
Cancer survivors also experience adverse psychological issues with ranging severities regarding fear of recurrence [48, 64] as well as anxiety, depression, and post-traumatic stress [65, 66] whose severity varies and, therefore, are more likely to see a mental health provider for assistance, mirroring current findings [67-70]. Although cancer survivors have a higher prevalence of adverse mental health symptomology [65, 66], they may be more likely to utilize mental healthcare when compared to the general population, possibly because they are already involved in the healthcare system for cancer care [9]. We observed that non-Hispanic Black and Hispanic survivors were more likely to see a mental health provider than non-Hispanic Black and Hispanic women without cancer, respectively. This finding somewhat differs with past literature showing that minority populations, and specifically minority cancer survivors, are less likely than non-Hispanic white survivors to seek mental health services during their survivorship or at diagnosis [71, 72]. Kaul et al. [73] found that survivors reported not being able to afford mental health care more often than cancer-free women, which fits in pattern with mental healthcare being an access and financial problem, not one of need. Additionally, we observed significant differences by race/ethnicity, educational background, and poverty status with the association between cancer history and place of routine healthcare. This finding mirrors past literature, as cancer care into survivorship is often a financial hardship for those with less access to healthcare, such as those from socioeconomic and racial/ethnic minority populations [41].
Research has shown that cancer survivors, on average, are living longer, due to the increase in screening and technology associated with early detection and treatment. [74] Clinically, there exists a potential to preemptively discuss physical and psychosocial health with cancer patients prior to survivorship, aligning a care plan with those at most risk for poor perceived physical and mental health prior to treatment ending. Primary care physicians should continue to promote regular healthcare practices during survivorship, focusing on the overall health of the individual, not solely on cancer-related care. Recently, personalized approaches such as risk-stratified pathways for cancer survivors have been utilized to manage ongoing survivorship care based upon both cancer-related and non-cancer-related factors such as prognosis, risk of recurrence, effects of treatment, functional ability, management of care, knowledge level regarding one’s health, and subsequent chronic conditions [75]. The current study may contribute to developing these pathways for risk-oriented survivorship care, especially within the US, where care access and utilization vary widely. Thus, conversations regarding quality of continued cancer care, for both physical and psychosocial aspects of survivorship, including educating their patients about the late health effects of cancer treatment to attenuate these risks, and maintaining such care are imperative among this population.
Study strengths
The current study has several strengths. Our study utilized the continuous NHANES (from 1999 to 2016) and included over 25,000 women, allowing for generalizability to the adult female population in the US, both with a history of cancer and those without. We were also able to compare associations with healthcare utilization patterns among women with a history of cancer to cancer-free women. Because NHANES collects numerous lifestyle, sociodemographic, and health-related variables, we were able to adjust and stratify associations by numerous variables, which few studies have done previously [76, 77].
Limitations
The current study’s findings should be considered in light of its limitations. While the current study provided a large sample, the data were cross-sectional and based on self-report which can lead to misclassification or recall bias. Future studies could focus on more concrete variables of care utilization and access, such as using medical record abstraction and/or insurance claims to connect perceived wellbeing to care usage. The NHANES are also collected in two-year cycles, which prohibits longitudinal analyses to capture changes over time. We did not have information regarding pain, hospitalization records, stage at diagnosis, time since cancer treatment(s), or type of cancer treatment(s) to control for in our analyses; however, we did exclude women who were possibly under active treatment to address some of these limitations. Lastly, it is possible that dichotomizing outcome variables lead to the loss of detailed information.
Conclusion
Our study focused on the impact and resonance of cancer on perceived health status and health care utilization among women and focused on subgroups of women from medically underserved populations. Our results indicate that female cancer survivors were more likely to perceive their health to be worse, were more likely to report being hospitalized, and were more likely to report visiting a mental health provider. The current study provides important information to inform future cancer survivorship care and discerns the importance of evaluating the effects of comprehensive healthcare among medically underserved populations.
Funding
KD received research support from the National Cancer Institute (T32CA009314) and MK was supported by the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK) Clinical Research and Epidemiology in Diabetes and Endocrinology Training Grant (T32DK062707).
Footnotes
Code availability Syntax coding is available upon reasonable request from the corresponding author.
Conflict of interest Dr. Kate Dibble has no conflicts of interest to disclose.
All contributions by Dr. Maneet Kaur were during her affiliation with Johns Hopkins Bloomberg School of Public Health; however, at the time of manuscript revision, Dr. Kaur was employed by Flatiron Health, an independent subsidiary of Roche. Dr. Kaur has reported stock ownership in Roche. Junrui Lyu has no conflicts of interest to disclose. Dr. Avonne Connor has no conflicts of interest to disclose.
Ethical approval This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the NCHS Research Ethics Review.
Informed consent Informed consent was obtained from all individual participants included in the study.
Data availability
The datasets generated during and/or analyzed during the current study are available via the National Center for Health Statistics (NCHS) website at https://wwwn.cdc.gov/nchs/nhanes/Default.aspx
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets generated during and/or analyzed during the current study are available via the National Center for Health Statistics (NCHS) website at https://wwwn.cdc.gov/nchs/nhanes/Default.aspx