Endometrial cancer is the most common gynecological cancer in the Western world and consequently has considerable impact on health care use.1 In Europe, endometrial cancer is diagnosed in 82,500 women each year,1 and this number rises as a result of an increase of both elderly and obese women.2,3 Moreover, owing to the generally good prognosis of 80% 5-year survival, there is a large and growing group of endometrial cancer survivors.3
Survivors show an increased specialist care use even long after the end of treatment,4,5 whereas for primary care use, results are more diverse. Some studies report an increased primary care use among cancer survivors compared to the general population,6,7 whereas others could not confirm this, possibly owing to small samples.4,5,8 Health care use differs by cancer type; and therefore, a specific description for endometrial cancer is needed.
Health care use is influenced by a variety of factors. To start with, increased health care use is likely to be influenced by the number of regular follow-ups and the physical and psychological complaints of survivors related to their tumor and treatment history.9 Moreover, recent studies found increased health care use among cancer survivors who had more comorbid conditions and who were married.4,8 An association of health care use with educational level was studied in one prior study, where no association was found.4 Because obesity is related to increased health care use in the general population,10 this might also be the case among endometrial cancer suvivors,11 although no research on this topic has been published. Furthermore, it is known that radiotherapy, which is often given postoperatively, affects quality of life of endometrial cancer survivors12,13 and is likely to be associated with health care use accordingly. From these studies, we hypothesize that comorbid conditions, body mass index (BMI), marital status, and treatment are related to health care use among endometrial cancer survivors. Understanding these associations can help in directing the health care system to cope with the increasing number of cancer survivors while keeping a good quality of health care.
The aims of this study were the following: (1) to describe health care use (general practitioner (GP), medical specialist (MS), additional care services) of long-term endometrial cancer survivors; (2) to compare this health care use with that of the general population; and (3) to assess associations between patient and treatment characteristics (age, years since diagnosis, marital status, educational level, BMI, comorbid conditions, radiotherapy, and time since diagnosis) with health care use among endometrial cancer survivors.
MATERIALS AND METHODS
Setting and Participants
A population-based cross-sectional survey was conducted in 2008. In total, 1478 patients with newly diagnosed International Federation of Gynecology and Obstetrics stage I or stage II endometrial cancer in the south of the Netherlands between 1999 and 2007 were registered by the Eindhoven Cancer Registry (ECR) of the Comprehensive Cancer Center South covering 10 community hospitals. Of these patients, 198 patients were deceased, 81 patients were 85 years or older and therefore excluded, 108 patients were treated in a hospital declining participation, and 126 patients had addresses that could not be verified. As a result, 965 endometrial cancer survivors were invited for participation; and 742 women (77%) completed the questionnaire. Details on this survey are described elsewhere.14 The Medical Ethics Committees of the participating hospitals approved this study.
Trained registration clerks of the ECR actively collected data on demographics and tumor and treatment information from hospital medical records. Patient-reported outcomes were obtained by questionnaires through Patient-Reported Outcomes Following Initial Treatment and Long-term Evaluation of Survivorship. Patient-Reported Outcomes Following Initial Treatment and Long-term Evaluation of Survivorship is a registry for the study of the physical and psychosocial impact of cancer and its treatment from a dynamic growing population-based cohort of both short- and long-term cancer survivors. Patient-Reported Outcomes Following Initial Treatment and Long-term Evaluation of Survivorship is linked directly to clinical data of the ECR. Data from the Patient-Reported Outcomes Following Initial Treatment and Long-term Evaluation of Survivorship registry is available for noncommercial scientific research, subject to study question, privacy and confidentially restrictions, and registration (www.profilesregistry.nl).15 A letter to inform about the study and the questionnaire was sent to endometrial cancer survivors by their attending gynecologist. By returning the enclosed questionnaire, survivors consented to participate in the study and agreed to the linkage of the questionnaire data with their disease history in the ECR. Nonrespondents were sent a reminder letter and questionnaire within 2 months.14
Information on the number of visits to a GP and MS in the general population was obtained from CentERdata, a Dutch research institute at Tilburg University specialized in online survey research (www.centerdata.nl). The CentERpanel is an online household panel consisting of more than 2000 Dutch households. The panel is designed to be representative of the Dutch population, including those without Internet access. Data from 2012 were matched on sex, age (in 3 categories), and educational level (in 3 levels), resulting in 78 patients who could be matched with our sample.
Tumor, treatment, and patient background information (ie, date of birth, date of diagnosis, stage of disease, and treatment-related aspects) were registered in the ECR. Questionnaires assessed the weight, height, marital status, educational level, comorbid conditions, and health care use. Body mass index was calculated (weight [kg]/height [m]2) and categorized according to standard guidelines; normal weight (BMI, <25), overweight (BMI, 25 to <30), obese class I (BMI, 30 to <35) and obese class II (BMI, ≥35).16 Socioeconomic status was determined by postal code.17 Comorbid conditions were assessed with the validated Self-administered Comorbidity Questionnaire.18 Survivors were asked to identify comorbid conditions present in the past 12 months. The adapted Self-administered Comorbidity Questionnaire lists 14 medical conditions.
Five items were used to assess health care use: (1) How often did you contact a general practitioner in the past 12 months? (2) How many of these visits were related to cancer or the consequences of your cancer? (3) How often did you visit a medical specialist in the past 12 months? (4) How many of these visits were related to cancer or the consequences of your cancer? These 4 questions could be answered by filling in the number of visits. These questions were asked in a similar way as is done by Statistics Netherlands (http://statline.cbs.nl). The last question was (5) Did you receive care after the treatment of your cancer? To answer this question, women could either choose “No” or “Yes” and then choose multiple additional care services from a list: psychologist, sexologist, social work, pastoral care, dietician, physical therapist, rehabilitation course, creative therapy, oncology nurse, or contact with other cancer survivors.
For the descriptive statistics, continuous variables were represented by means and standard deviations and categorical variables by frequencies and percentages. Differences in sociodemographic and clinical characteristics (dependent variables) between respondents, nonrespondents, and patients with unverifiable addresses were compared using analysis of variance for continuous variables and the χ2 test for categorical variables. Data from the general population were matched on age and educational level. Differences in health care use between the general population and study participants were compared using analysis of variance.
Multiple logistic regression analyses were conducted to evaluate the relationship between health care use as the dependent variable and the independent variables age, years since diagnosis, marital status, educational level, number of comorbid conditions, and radiotherapy. Variables entered in the regression models were determined a priori and based on our hypotheses. Because health care use was not normally distributed, this variable was dichotomized using median split into the following: visits to GP, zero to 1 versus 2 or more; visit to GP related to cancer, zero versus 1 or more; visit to MS, zero to 1 versus 2 or more; and visit to MS in relation to cancer, zero versus 1 or more. All analyses were performed using Statistical Analysis System (SAS) version 9.2 (SAS Institute, Cary, NC; 1999). P values were regarded as significant if P < 0.05 and tests were 2 sided.
Sociodemographic characteristics of respondents, nonrespondents, and patients with unverifiable addresses are shown in Table 1. Respondents were younger and had a higher socioeconomic status than nonrespondents. There were no differences with respect to years since diagnosis, International Federation of Gynecology and Obstetrics stage, and primary treatment.
Health Care Use
Endometrial cancer survivors did not report significantly more visits to the GP than women in the general population (Table 2), and only a small proportion of the visits to the GP was related to cancer. However, endometrial cancer survivors reported more visits to the MS than women in the general population. In addition, only a minority (14%) of survivors used additional care, except for younger survivors up to 55 years of whom 33% used additional care. The physical therapist and psychologist were the most frequently used additional care services.
Logistic regression analyses (Table 3) showed that women visiting their GP twice or more were more likely to have a low educational level, report more comorbid conditions, and have a more recent diagnosis of endometrial cancer than women who reported none or one GP visit. Moreover, women visiting their GP in relation to their cancer were more likely to be younger, report more comorbid conditions, and have a more recent diagnosis than women who did not visit their GP in relation to their cancer. Women visiting their MS twice or more were more likely to report more comorbid conditions and have a more recent diagnosis than women with less than 2 visits to the MS. Women visiting their MS in relation to their cancer were more likely to be more highly educated and have a more recent diagnosis than women with no visits to the MS related to cancer. No association was seen between BMI or radiotherapy and health care use.
With increasing numbers of comorbid conditions, the number of visits to the GP and the MS increases (Fig. 1). However, this association was absent for cancer-specific visits. Interestingly, less highly educated survivors had a higher use of GP care in general, whereas use of MS care related to the cancer was higher among highly educated survivors (Fig. 2). Visits to the GP tend to decrease slightly over time after cancer diagnosis (Fig. 3). Visits to the MS decrease steadily during the first 10 years after diagnosis.
Endometrial cancer survivors use more MS care compared to the general population. Younger endometrial cancer survivors incline to more cancer-related visits to the GP and use more additional care services compared to older survivors. Moreover, highly educated women make more cancer-related visits to their MS than less highly educated women. Health care use was related to more comorbid conditions but not to BMI and radiotherapy treatment.
Our results did not show increased GP use among endometrial cancer survivors compared to the general population. This is in concordance with the results of earlier studies among gynecological,8 endometrial,4 and breast cancer survivors.5 However, analyses of combined groups of cancer survivors showed increased use of the GP.4,6–8 Differences in GP use might be explained by divergent cancer types or sex related.4 Regarding gynecological cancer survivors, data are conflicting. Our study and the data of Mols et al4 show a tendency for increased use, whereas Nord et al8 describe a tendency for decreased use. The observed discrepancy might be related to differences in health care systems in these countries. Mols et al and our study were situated in the Netherlands, whereas the study of Nord et al was situated in a rural county of Norway, possibly leading to decreased access to GP care.
It is interesting to note that both our study and a study among breast cancer survivors5 reported more additional care use in younger cancer survivors. This seems in contradiction with the fact that young endometrial cancer survivors experience better physical and role functioning compared to older survivors.19 However, several explanations are possible. First, the higher health care use of younger endometrial cancer survivors might be related with the higher demands of younger survivors owing to work and/or responsibility for children and a more assertive attitude to access of care. Second, younger women who enter menopause due to the cancer treatment have a decreased comparability with their age-matched norm population, which might lead to increased health care use. And third, younger survivors might experience better health as a consequence of their increased health care use. Furthermore, we found that women who are more highly educated use more MS care in relation to their cancer, indicating possible social inequality in access to health care. Explanations for this might be that more highly educated survivors more actively look for MS care when having questions or complaints, that their follow-up is more frequently scheduled, that they attend the follow-up visits more accurately, or that they perceive a higher threat of the cancer diagnosis. The more frequent use of specialist care by more highly educated women warrants further research: do they perceive more fear and need specific counseling, do they perceive more complaints, or do they find their way into specialist care more easily?
In concordance with our study, recent studies demonstrated that in cancer survivors, increased GP and MS consultation is associated with having comorbid conditions.4,8 For many cancer survivors, cancer is only one of the health problems they seek medical attention for, as 60% of them have one or more comorbid diseases.20 This is important to keep in mind when considering the follow-up care for cancer survivors.
Surprisingly, we did not find a relation between radiotherapy or BMI and increased health care use. Because radiotherapy has a negative impact on morbidity,14 it is surprising that this higher morbidity does not translate into higher health care use for either GP or MS. However, the nonsignificant result might be related to insufficient power in this study, as we observed an odds ratio of 1.5 (CI, 0.94–2.41) for MS use related to cancer. In addition, for BMI, the expected relation was not found. Because it is known that obesity is related to decreased quality of life21 and increased GP use in the general population,10 we expected BMI to be related to health care use in endometrial cancer survivors. A sensitivity multiple regression analysis to assess the association of BMI and health care use without having comorbid condition in the model showed no association. We do not have other possible explanations for this finding.
A variety of strategies might be useful to lower health care costs for cancer follow-up care, although research on this topic is still needed for endometrial cancer care. Although not all hospitals in the Netherlands have a specialized nurse for gynecologic oncology patients, their role in follow-up care might be enlarged by transition medical specialist care to specialized nurse care. Alternatively, follow-up care could be transitioned to the general practitioner, or the intensity of follow-up care could be diminished, as evidence for current follow-up practice is largely lacking.22
Strengths and Limitations
Health care use was based on self-reported data, where recall bias might have led to selective variation in response. However, effects are probably similar for the cancer survivors and the general population. Moreover, nonresponse might be related to health care use. This is especially the case if nonresponse is caused by illness.23 In that case, our results are an underestimation of the true health care use.
Despite the limitations noted, strengths could also be identified. The current study is one of the first studies that examine the health care use of a large group of endometrial cancer survivors and evaluates characteristics associated with health care use. A second strength is the large population-based study sample and high response rate, which enhances the generalizability of this study. Finally, the age and educational level–matched norm sample makes a good comparison to the general population possible.
The increase in the number of endometrial cancer survivors will put an increasing pressure on the specialist care, as we found that endometrial cancer survivors more frequently visit the MS than women in the general population. Younger women seem to have higher health care needs. Moreover, more highly educated survivors visit their MS more often in relation to their cancer, indicating that they find their way to hospital care more easily, which can be a signal of inequality in access of care. Transition of care to the primary care physician or nurse practitioners might support long-term accessibility of care for endometrial cancer survivors. In addition, research into the effect of decreasing the number of follow-up visits as formulated in the national guideline might be a feasible alternative. However, special attention should be given to more highly educated and younger women, as they currently have a higher MS use.
The authors thank all patients and their doctors for their participation in the study. Special thanks go to Dr M van Bommel, who was willing to function as an independent advisor and to answer questions of the patients. In addition, the authors also thank the following hospitals for their cooperation: Amphia Hospital, Breda; Catharina Hospital, Eindhoven; Elkerliek Hospital, Helmond and Deurne; Jeroen Bosch Hospital, ’s Hertogenbosch; Maxima Medical Centre, Eindhoven and Veldhoven; Sint Anna Hospital, Geldrop; St Elisabeth Hospital, Tilburg; Twee Steden Hospital, Tilburg and Waalwijk; VieCuri Hospital, Venlo and Venray, Instituut Verbeeten, Tilburg.
1. Ferlay J, Parkin DM, Steliarova-Foucher E. Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer
. 2010; 46: 765–781.
2. Renehan AG, Tyson M, Egger M, et al. Body-mass index and incidence of cancer: a systematic review and meta-analysis of prospective observational studies. Lancet
. 2008; 371: 569–578.
3. Karim-Kos HE, Kiemeney LA, Louwman MW, et al. Progress against cancer in the Netherlands since the late 1980s: an epidemiological evaluation. Int J Cancer
. 2011; 130: 2981–2989.
4. Mols F, Helfenrath KA, Vingerhoets AJ, et al. Increased health care utilization among long-term cancer survivors compared to the average Dutch population: a population-based study. Int J Cancer
. 2007; 121: 871–877.
5. van de Poll-Franse LV, Mols F, Vingerhoets AJ, et al. Increased health care utilisation among 10-year breast cancer survivors. Support Care Cancer
. 2006; 14: 436–443.
6. Heins M, Schellevis F, Rijken M, et al. Determinants of increased primary health care use in cancer survivors. J Clin Oncol
. 2012; 30: 4155–4160.
7. Khan NF, Watson E, Rose PW. Primary care consultation behaviours of long-term, adult survivors of cancer in the UK. Br J Gen Pract
. 2011; 61: 197–199.
8. Nord C, Mykletun A, Thorsen L, et al. Self-reported health and use of health care services in long-term cancer survivors. Int J Cancer
. 2005; 114: 307–316.
9. Stein KD, Syrjala KL, Andrykowski MA. Physical and psychological long-term and late effects of cancer. Cancer
. 2008; 112: 2577–2592.
10. Twells LK, Bridger T, Knight JC, et al. Obesity predicts primary health care visits: a cohort study. Population Health Management
. 2012; 15: 29–36.
11. Modesitt SC, Tian C, Kryscio R, et al. Impact of body mass index on treatment outcomes in endometrial cancer patients receiving doxorubicin and cisplatin: a Gynecologic Oncology Group study. Gynecol Oncol
. 2007; 105: 59–65.
12. Nout RA, van de Poll-Franse LV, Lybeert ML, et al. Long-term outcome and quality of life of patients with endometrial carcinoma treated with or without pelvic radiotherapy in the post operative radiation therapy in endometrial carcinoma 1 (PORTEC-1) trial. J Clin Oncol
. 2011; 29: 1692–1700.
13. van de Poll-Franse LV, Mols F, Essink-Bot ML, et al. Impact of external beam adjuvant radiotherapy on health-related quality of life for long-term survivors of endometrial adenocarcinoma: a population-based study. Int J Radiat Oncol Biol Phys
. 2007; 69: 125–132.
14. van de Poll-Franse LV, Pijnenborg JM, Boll D, et al. Health related quality of life and symptoms after pelvic lymphadenectomy or radiotherapy vs. no adjuvant regional treatment in early-stage endometrial carcinoma: a large population-based study. Gynecol Oncol
. 2012; 127: 153–160.
15. van de Poll-Franse LV, Horevoorts N, van Eenbergen M, et al. The Patient Reported Outcomes Following Initial treatment and Long term Evaluation of Survivorship registry: scope, rationale and design of an infrastructure for the study of physical and psychosocial outcomes in cancer survivorship
cohorts. Eur J Cancer
. 2011; 47: 2188–2194.
16. James PT, Leach R, Kalamara E, et al. The worldwide obesity epidemic. Obes Res
. 2001; 9: 228S–233S.
17. Van Duijn C, Keij I. Sociaal-economische status indicator op postcodeniveau [in Dutch]. Maandstatistiek van de bevolking
. 2002; 50: 32–35.
18. Sangha O, Stucki G, Liang MH, et al. The Self-Administered Comorbidity Questionnaire: a new method to assess comorbidity for clinical and health services research. Arthritis Rheum
. 2003; 49: 156–163.
19. Mols F, Coebergh JW, van de Poll-Franse LV. Health-related quality of life and health care utilisation among older long-term cancer survivors: a population-based study. Eur J Cancer
. 2007; 43: 2211–2221.
20. Janssen-Heijnen ML, Houterman S, Lemmens VE, et al. Prognostic impact of increasing age and co-morbidity in cancer patients: a population-based approach. Crit Rev Oncol Hematol
. 2005; 55: 231–240.
21. Oldenburg CS, Boll D, Nicolaije KA, et al. The relationship of body mass index with quality of life among endometrial cancer survivors: a study from the population-based PROFILES registry. Gynecol Oncol
. 2013; 129: 216–221.
22. Fung-Kee-Fung M, Dodge J, Elit L, et al. Follow-up after primary therapy for endometrial cancer: a systematic review. Gynecol Oncol
. 2006; 101: 520–529.
23. Gundgaard J, Ekholm O, Hansen EH, et al. The effect of non-response on estimates of health care utilisation: linking health surveys and registers. Eur J Public Health
. 2008; 18: 189–194.