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The combined effect of cancer and chronic diseases on general practitioner consultation rates
Cancer Epidemiology 39 (2015) 109–114
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Cancer Epidemiology The International Journal of Cancer Epidemiology, Detection, and Prevention journal homepage: www.cancerepidemiology.net
The combined effect of cancer and chronic diseases on general practitioner consultation rates M.J. (Marianne) Heins a,*, J.C. (Joke) Korevaar a, G.A. (Ge´) Donker a, P.M. (Mieke) Rijken a, F.G. (Franc¸ois) Schellevis a,b a b
Netherlands Institute for Health Services Research (NIVEL), Utrecht, The Netherlands Department of General Practice/EMGO Institute for Health and Care Research, VU University Medical Centre, Amsterdam, The Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history: Received 24 September 2014 Received in revised form 2 December 2014 Accepted 7 December 2014 Available online 2 January 2015
Aim: More than two-thirds of cancer patients have one or more chronic diseases besides cancer. The purpose of this study was to get detailed insight into the combined effect of cancer and chronic diseases on general practitioner (GP) consultation rates. Methods: From the NIVEL Primary Care Database we identified cancer patients with diabetes mellitus (n = 629), osteoarthritis (n = 425), coronary artery disease (n = 466), COPD (n = 383) or without a chronic disease (n = 1507), diagnosed with cancer between 2002 and 2010. They were matched on sex, age, practice and chronic disease to 6645 non-cancer controls. Results: 2–5 years after diagnosis, cancer patients without a chronic disease had on average 6.5 GP contacts per year, those with a comorbid disease almost twice as many (ranging from 10 for osteoarthritis to 12.4 for COPD). A similar difference was seen in non-cancer controls. The number of GP contacts for chronic diseases did not differ between cancer patients and controls. The increase in the number of GP consultations with age and number of chronic diseases was similar in cancer patients and controls. Consultation rates were similar in cancer patients and controls if they were stratified by number of chronic diseases while counting cancer as a chronic disease. Conclusions: Two to five years after diagnosis, cancer leads to an increase in GP contacts that is similar to having a chronic disease. This increase does not differ between those with and without a chronic disease and cancer does not seem to increase the impact of having a chronic disease. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Cancer Chronic disease Comorbidity Primary care General practice Health care use
1. Introduction Cancer is mostly diagnosed above the age of 50, and as the general population ages, the number of older cancer patients is increasing [1]. In old age chronic diseases are common [2], and consequently more than two-thirds of cancer patients have one or more chronic diseases besides cancer [3–5]. The most common chronic diseases in cancer patients are similar to those in the general population, e.g. diabetes mellitus (DM), cardiovascular disease, chronic obstructive pulmonary disease (COPD) and osteoarthritis (OA) [3,4,6]. These chronic diseases may have important clinical implications. First, patients with chronic diseases seem more vulnerable to the complications of cancer treatments [7–9], which may lead to
* Corresponding author at: Netherlands Institute for Health Services Research (NIVEL), P.O. Box 1568, 3500 BN Utrecht, The Netherlands. Tel.: +31 30 27 29 827; fax: +31 30 27 29 729. E-mail address: [email protected] (M.J. (Marianne) Heins). http://dx.doi.org/10.1016/j.canep.2014.12.002 1877-7821/ß 2014 Elsevier Ltd. All rights reserved.
increased symptom burden [10,11]. Reversely, cancer and its treatment may also negatively impact existing chronic diseases, like diabetes [12] and may even increase the risk of developing new chronic diseases, such as cardiac disease [13] and osteoporosis [14]. Previous studies showed that several years after the diagnosis of cancer, patients have significantly more general practitioner (GP) consultations than noncancer controls of the same age and sex. This is seen both in patients with and without a comorbid chronic disease. Patients with both cancer and a comorbid chronic disease have the highest number of GP consultations. It is likely that this effect is different for each chronic disease. However, it has not been studied which chronic diseases have a relatively large effect on GP consultations in cancer patients and should therefore receive increased attention. The exact reason for the increase in GP consultations is also unclear. It does not seem to be because health care use for chronic diseases is increased in cancer patients [15]. In fact, cancer patients are less likely to receive recommended care for their chronic diseases [16–18]. Another explanation may be that cancer patients
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with a chronic disease are more vulnerable to the effects of cancer and its treatment. Or the combination of cancer and a chronic disease may make patients more frail in general. We aimed to get more insight into this synergistic effect of cancer and chronic disease. First of all, we aimed to study whether cancer is related to higher GP consultation rates in patients with specific chronic diseases. We also aimed to study whether the combination of cancer and a chronic disease increases the number of GP contacts specifically related to cancer or the chronic disease. Finally, we aimed to study whether known factors that lead to increased GP consultation rates, such as higher age and a higher number of chronic diseases, have a larger effect in patients with cancer and a chronic disease than in those without cancer, as these patients may be more frail. Studying these aspects may elucidate the reason for the increased GP consultation rates and identify especially vulnerable subgroups that should receive increased attention from their GP. We therefore examined GP consultation rates in cancer patients for four different chronic diseases that are common in cancer survivors and also treated in primary care (DM, OA, coronary artery disease (CAD), and COPD) and compared them with those of patients with the same chronic disease but without cancer. 2. Patients and methods 2.1. Database For this study, data were derived from the NIVEL Primary Care Database (formerly known as LINH). This nationally representative Dutch network consisted of approximately 90 practices at the time data were collected. Participating GPs routinely record data on all patient contacts, including diagnoses made. Diagnoses are coded according to the ICPC-1 (International Classification of Primary Care) [19]. In the Netherlands all inhabitants are obligatorily insured for standard medical care and listed with a GP [20]. 2.2. Patients Based on the ICPC codes recorded in the electronic medical record (EMR), all patients diagnosed with cancer between January 2002 and December 2010 were selected. We excluded skin cancer (ICPC S77), as its clinical impact is often relatively small, and musculoskeletal neoplasms (ICPC L71), as this ICPC code also includes benign tumours. Patients had to be at least 55 years of age at diagnosis, as chronic diseases are less prevalent below this age, and they had to have at least two years of follow-up data available starting from diagnosis. We did not exclude cancer patients in the palliative phase as this phase is not easily discernible in our data and patients may have died due to other reasons than cancer. 2.3. Chronic disease We defined five groups: (1) cancer patients with no chronic disease; (2) cancer patients with DM (ICPC code T90); (3) cancer patients with OA (ICPC codes L89 to L91); (4) cancer patients with CAD (ICPC codes K74 to K76); and (5) cancer patients with COPD (ICPC codes R91 and R95). These diseases were selected from a list of chronic diseases [21], because they have a high prevalence in cancer survivors and are mainly treated in primary care. Presence of these diseases was determined two years after diagnosis based on prior occurrence of the ICPC code(s) in the EMR. 2.4. Control patients We matched each cancer patient to two controls without a known diagnosis of cancer in their EMR from the same group (no
chronic disease/DM/OA/CAD/COPD) based on age (5 years), sex and practice. We chose a ratio of 1:2 for cancer patients and control patients to increase the power of our study. Controls had to have at least two years of data available starting from the date of diagnosis of the cancer patient they were matched to. 2.5. GP consultation rates Annual GP consultation rates two to five years after diagnosis or inclusion were determined from data in the EMR; i.e. contacts with the practice (office visits, home visits or telephone consultations with the GP or nurse specialist) and ICPC codes related to these contacts. Only data from patients who had been registered in the practice during the whole year, and practices that had provided data for at least 48 weeks per year and fulfilled quality requirements (accuracy of diagnostic codes and type of contact) were selected. 2.6. Statistical analyses First we assessed the effect of cancer in each group (no chronic disease/DM/OA/CAD/COPD) by comparing the mean annual number of GP consultations in cancer patients and matched controls. We also compared the mean annual number of consultations with an ICPC code related to cancer. To assess the effect of cancer on chronic diseases, we compared the mean number of GP consultations specifically related to DM, OA, CAD or COPD in cancer patients and matched controls. Next, two factors that could influence consultation rates were examined, i.e. age and the number of chronic diseases. The impact of these factors was tested using multivariate negative binomial regression analyses [22]. We chose this type of regression analysis since our outcome variable, the annual number of GP consultations, is a rate and this type of regression analysis predicts the rate of an event. For each group we built a model with cancer/control patient and age as independent variable. To assess the possible effect of age on the difference between patients and controls we added an interaction variable between both. We built similar models for number of chronic diseases. To correct for repeated measurements, we relaxed the assumption of independence of observations in calculating the variance–covariance estimate using the option vce (cluster). Analyses were performed using STATA1 SE version 12.1. A p-value <0.05 was considered statistically significant. The study was carried out according to the precepts of the Helsinki Declaration, Dutch legislation on privacy and the regulations of the Dutch Data Protection Authority. According to Dutch legislation, approval by a Medical Ethics Committee was not obligatory for this study. 3. Results In our database, 9752 patients were diagnosed with cancer between January 2002 and December 2010, of which 3875 had at least 2 years of follow-up. The others had died, moved, or their practice did not fulfil quality criteria in these years. Two years after the diagnosis of cancer 1507 of the patients with at least two years follow-up (39%) had no chronic disease, 629 (16%) had been diagnosed with DM, 425(11%) had been diagnosed with OA, 466 (12%) with CAD and 383 (10%) with COPD. Cancer patients without a chronic disease were somewhat younger than the other groups (see Table 1). Cancer patients with OA were predominantly female (64%), while those with CAD and COPD were predominantly male. The percentage of patients with breast cancer was lowest in these latter two groups, while lung cancer was much more common in those with COPD. For each of the five groups (no chronic disease/DM/OA/CAD/ COPD) we matched each cancer patient to two controls from the
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Table 1 Background characteristics. No chronic disease
Agea Sex (male)
No-cancer controls (n = 2988)
Cancer (n = 629)
67.1 (8.8) 1453 (49%)
66.8 (8.8) 738 (49%)
70.5 (8.7) 297 (47%)
2.5 (2.3) 3.8 (1.8)
2.5 (2.3) 4.2 (2.1)
2.6 (2.4) 3.8 (1.7)
– – – – –
Number of chronic diseasesb 1 – 2 – 3 – 4 – 5 – Cancer type Breast Prostate Colorectal Bladder Lung Other a b * **
OA
Cancer (n = 1507)
Follow-up (year) Before diagnosis After diagnosis Comorbidity DM CAD OA COPD Other
DM
395 274 256 80 80 422
– – – – –
629 123 89 89 432
(100%) (20%) (14%) (14%) (66%)
– – – – –
196 190 113 64 66
(31%) (30%) (18%) (10%) (11%)
160 118 118 40 34 159
(26%) (19%) (19%) (6%) (5%) (25%)
(26%) (18%) (17%) (5%) (5%) (28%)
No-cancer controls (n = 1223)
CAD
COPD
Cancer (n = 425)
No-cancer controls (n = 825)
Cancer (n = 466)
No-cancer controls (n = 893)
Cancer (n = 383)
No-cancer controls (n = 716)
70.1 (8.4) 574 (47%)
72.5 (8.6) 152 (36%)
72.2 (8.6) 284 (34%)
72.1 (8.3) 294 (63%)
71.7 (8.3) 559 (64%)
71.3 (8.1) 226 (59%)
70.8 (7.8) 432 (60%)
2.6 (2.4) 4.0 (1.8)
3.0 (2.5) 3.9 (1.6)
3.0 (2.5) 4.1 (1.8)
2.8 (2.3) 3.8 (1.5)
2.8 (2.3) 4.0 (1.7)
2.7 (2.4) 3.5 (1.4)
2.7 (2.4) 3.8 (1.5)
1223 246 203 135 807
405 361 227 136 94
(100%) (20%) (17%) (11%) (69%)
82 76 425 58 322
(19%) (18%) (100%) (14%) (76%)
164 120 825 93 604
(20%) (15%) (100%) (11%) (73%)
121 466 80 89 340
(26%) (100%) (17%) (19%) (73%)
238 893 141 135 666
(27%) (100%) (16%) (15%)* (75%)**
84 83 52 383 293
(22%) (22%) (14%) (100%) (77%)
166 141 114 716 563
(23%) (20%) (16%) (100%) (79%)
(33%) (30%) (19%) (11%) (8%)
102 138 74 51 60
(24%) (32%) (17%) (12%) (14%)
225 251 172 93 84
(27%) (30%) (21%) (11%) (10%)
100 139 101 57 69
(25%) (30%) (22%) (12%) (15%)
220 271 189 117 96
(25%) (31%) (22%) (13%) (11%)
85 101 83 56 58
(22%) (27%) (22%) (15%) (15%)
145 202 168 90 111
(20%) (28%) (23%) (13%) (16%)
130 74 74 25 22 100
(31%) (17%) (17%) (6%) (5%) (24%)
74 112 77 39 40 124
(16%) (24%) (17%) (8%) (9%) (27%)
64 68 67 29 66 89
(17%) (18%) (17%) (8%) (17%) (23%)
Age at diagnosis for cancer patients and age at inclusion for controls. Both chronic disease that were prevalent two years after diagnosis and new ones that developed between 2 and 5 years after diagnosis. p = 0.03. p = 0.046.
chronic disease (see Table 2). Patients with DM had the highest number of consultations related to their chronic disease (mean 2.7 per year) and those with OA and CAD the lowest (mean 0.3 and 0.4 per year). These numbers did not differ between cancer patients and matched controls. The number of GP consultations increased with age (Fig. 1a–d) and with the number of chronic diseases (Fig. 2a–d). Both increases were similar in cancer patients and matched controls (see Table 3). If the average number of GP consultations was stratified by the number of chronic diseases and cancer was counted as a chronic disease, no differences were found between patients with and without cancer (Fig. 2a–d). Although the figures for diabetes and CAD may indicate some differences between patients with and without cancer, these were non-significant (see Table 3).
same group, practice, age (5 years) and sex. 225 cancer patients, equally divided between the 5 groups, could not be matched to a control and 175 patients could only be matched to one control. No significant differences in baseline characteristics were found between cancer patients and controls (see Table 1), except for the fact that cancer patients with CAD were more likely also to have COPD (19% versus 15%, p = 0.03) and less likely to have another chronic disease (73% versus 75%, p = 0.046). Cancer patients without a chronic disease had the lowest number of GP consultations in the period of 2–5 years after diagnosis; on average 6.4 per year. For cancer patients with a comorbid disorder this number ranged from a mean of 10.1 consultations per year for those with OA to 12.3 for those with COPD. In all five groups, cancer patients had significantly more GP contacts (p < 0.001) than the matched controls. The difference between those with and without cancer was somewhat higher in those with CAD or COPD than in those with DM or OA (see Table 2). The number of consultations specifically related to cancer was on average one per year, both in patients with and without a
4. Discussion We studied the combined effect of cancer and chronic diseases (i.e. diabetes mellitus, osteoarthritis, coronary artery disease and
Table 2 Mean number (standard deviation) of GP consultations (total number/consultations for chronic disease and for cancer) per year in the period of 2–5 years after diagnosis/ inclusion for patients with a chronic disease and cancer. Chronic diseasea
Cancer
Non-cancer controls
Cancer patients
Non-cancer controls
Cancer patients
Non-cancer controls
Cancer patients
Non-cancer controls
4.0 10.0 8.7 8.4 9.7
– 2.7 0.3 0.4 1.3
– 2.9 0.2 0.4 1.3
0.9 0.9 0.8 0.9 1.1
– – – – –
5.6 8.3 9.0 10.0 9.8
4.0 7.1 8.5 8.1 8.4
Total Cancer patients No chronic disease DM OA CAD COPD a *
6.4 11.9 10.1 11.2 12.3
(9.3)* (12.5)* (11.1)* (11.9)* (13.7)*
(4.9) (8.9) (8.3) (8.0) (9.1)
(3.7) (1.1) (1.0) (3.7)
Consultations related to specific chronic disease (DM/OA/CAD/COPD). p < 0.005.
(3.7) (0.9) (1.1) (4.2)
(5.0) (5.6) (3.6) (3.6) (5.7)
Other
(6.7) (9.4) (9.8) (10.7) (10.3)
(4.9) (7.4) (8.2) (7.9) (7.6)
M.J.M. Heins et al. / Cancer Epidemiology 39 (2015) 109–114
15 10 5 0
55-64
65-69
70-74
75-79
>=80
Age (years)
CAD
20 15 10 5 0
55-64
65-69
70-74
75-79
>=80
Age (years)
DM
20 15 10 5 0
55-64
65-69
70-74
75-79
>=80
Age (years)
Number of GP consultaons per year
No comorbidity Number of GP consultaons per year
20
Number of GP consultaons per year
Number of GP consultaons per year
Number of GP consultaons per year
112
OA
20 15 10 5 0
55-64
65-69
70-74
75-79
>=80
Age (years)
COPD
20 15 10
Cancer
5 0
Controls 55-64
65-69
70-74
75-79
>=80
Age (years)
Fig. 1. Mean number of GP consultations per year in the period of 2–5 years after diagnosis of cancer with and without comorbid chronic diseases by age.
Number of GP consultaons per year
DM
20 15 10 5 0
1
2
3
4
5
Number of chronic condions (pre-exisng & new)
CAD
20
20
15
15
10
10
5 0
our sample size was relatively large, it did not allow us to study the combined effects of cancer with less common chronic diseases. Data were derived from EMRs, which could be incomplete, but (1) practices used these files for reimbursement claims with insurance companies, (2) it is unlikely that EMRs of cancer patients were more incomplete than those of non-cancer patients, especially as cancer patients and controls were matched on practice, (3) we applied recording quality criteria for practices (more than 50% valid ICPC codes, data available for at least 48 weeks per year). In the
Number of GP consultaons per year
Number of GP consultaons per year
Number of GP consultaons per year
COPD). We found that two to five years after diagnosis, cancer leads to an increase in GP contacts, both in patients with and without a chronic disease. Cancer does not seem to affect the impact of chronic diseases and does not affect the impact of age or the number of chronic diseases on health care use. Using a large primary care registry with routinely recorded data, we could include a large number of cancer patients. This enabled us to study the effect of individual chronic diseases and several determinants of GP consultation rates of cancer patients. Although
5 1
30
OA
20 15 10 5 0
1
2
3
4
20
COPD
15 10 5 0
1 2 3 4 4 Number of chronic 5 1 2 3 condions (pre-exisng & new) Number of chronic condions (pre-exisng & new) Number of chronic condions (pre-exisng & new) 2
4
5
Cancer
5
Number of chronic condions (pre-exisng & new)
5
Controls
Fig. 2. Mean number of GP consultations per year in the period of 2–5 years after diagnosis of cancer for patients with different comorbid chronic diseases by number of chronic conditions (cancer counted as a chronic condition).
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Table 3 p-Values of regression models examining the effects of age sex and comorbidity. Model
1. Age
Cancer Age (years)
Cancer Age
2. Comorbidity
Cancer No. of chronic diseases (cancer included)
Cancer No. of chronic diseases
55–64 (ref) 65–69 70–74 75–79 80 Cancer 65–69 Cancer 70–74 Cancer 75–79 Cancer 80 1 2 (ref) 3 4 5 Cancer 3 Cancer 4 Cancer 5
No. chronic disease
Diabetes
Arthritis
CAD
COPD
p-Value
p-Value
p-Value
p-Value
p-Value
<0.001 – 0.02 <0.001 <0.001 <0.001 0.99 0.84 0.83 0.85
<0.001 – 0.72 0.008 0.002 <0.001 0.74 0.46 0.74 0.43
0.03 – 0.26 <0.001 <0.001 <0.001 0.92 0.51 0.89 0.85
0.007 – 0.13 0.01 0.001 <0.001 0.20 0.65 0.98 0.77
0.003 – 0.06 0.008 0.001 <0.001 0.29 0.24 0.76 0.66
0.20 0.008 – 0.001 <0.001 <0.001 0.50 0.28 0.15
0.90 <0.001 – <0.001 <0.001 <0.001 0.50 0.81 0.89
0.14 0.004 – 0.027 <0.001 <0.001 0.76 0.93 0.56
0.06 0.146 – 0.055 0.001 <0.001 0.69 0.43 0.37
– – – – – – – – –
Netherlands, disease management programmes for diabetes have been widely implemented within primary care since 2010. Consultations related to these programmes are missing in our data, but mean number of GP consultations in diabetes patients was only slightly lower when excluding data from 2010 to 2011 (11.4 instead of 11.9 consultations per year for cancer patients and 9.7 instead of 9.8 for controls). Previous studies have also found that several years after diagnosis, cancer patients with chronic diseases have increased GP consultation rates, when compared to those without chronic disease [17,18]. These studies were also based on data from the NIVEL Primary Care Database. However, in the paper of Jabaaij et al. repeat prescriptions were included and in the paper of Heins et al. effects of individual chronic diseases were not examined so results cannot be directly compared. Heins et al. did find that in patients with colorectal cancer and matched non-cancer controls with a chronic disease, the difference between both groups increased with age [17]. This was not found in patients with breast or prostate cancer, so the effect of chronic diseases may differ between cancer types. In the current study, the difference between cancer patients and controls did not decrease with age, which may be because in the current study we included all cancer types. Although we used a large primary care registry, we could only study the impact of relatively common chronic diseases. We therefore do not know whether our results apply to other, less common chronic diseases. Besides, effects of chronic diseases may also differ by cancer type. This question can only be answered by studying a very large cohort of cancer patients. Another limitation is that we could not determine the exact date of diagnosis of the chronic disease if this was long before the cancer diagnosis. We therefore could not take this variable into account in our analyses. It would also be interesting to see whether GP contact rates increase when cancer patients develop more chronic diseases. Future research could also focus on designing and implementing primary care programmes for cancer. We found that two to five years after diagnosis, cancer leads to an increase in GP consultations, both in those with and without a chronic disease. The increase is similar to that caused by having a chronic disease. As many cancer patients have one or more chronic diseases, their care is complex. Specialists and GPs should therefore collaborate in the care for these patients. It is necessary that GPs adapt their way of treating patients with cancer, which is
currently often reactive [23]. They could learn from the approach with which they are treating patients with chronic diseases and develop care programmes for cancer patients, based on principles derived from the Chronic Care Model, i.e. proactive, patientcentred care that meets the needs of cancer patients with or without co-morbidity [24]. GPs may be trained and reassured in their capability of offering aftercare to cancer patients in the period 2–5 years after diagnosis Conflict of interest The authors have no conflict of interest to declare. Funding This study was financially supported by Alpe d’HuZes/Dutch Cancer Society, grant no. 4870. The sponsor did not have any role in study design; in the collection, analysis and interpretation of data; in the writing of the report; or in the decision to submit the article for publication Authorship contribution Study concepts: all authors Study design: all authors Data acquisition: JK Quality control of data and algorithms: MH Data analysis and interpretation: all authors Statistical analysis: MH, JK Manuscript preparation: MH Manuscript editing: JK, GD, MR, FS Manuscript review: all authors. References [1] Ferlay J, Parkin DM, Steliarova-Foucher E. Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer 2010;46(March (4)):765–81. [2] van Oostrom SH, Picavet HS, van Gelder BM, Lemmens LC, Hoeymans N, van Dijk CE, et al. Multimorbidity and comorbidity in the Dutch population – data from general practices. BMC Public Health 2012;12:715. [3] Ogle KS, Swanson GM, Woods N, Azzouz F. Cancer and comorbidity: redefining chronic diseases. Cancer 2000;88(February (3)):653–63.
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Cancer Epidemiology The International Journal of Cancer Epidemiology, Detection, and Prevention journal homepage: www.cancerepidemiology.net
The combined effect of cancer and chronic diseases on general practitioner consultation rates M.J. (Marianne) Heins a,*, J.C. (Joke) Korevaar a, G.A. (Ge´) Donker a, P.M. (Mieke) Rijken a, F.G. (Franc¸ois) Schellevis a,b a b
Netherlands Institute for Health Services Research (NIVEL), Utrecht, The Netherlands Department of General Practice/EMGO Institute for Health and Care Research, VU University Medical Centre, Amsterdam, The Netherlands
A R T I C L E I N F O
A B S T R A C T
Article history: Received 24 September 2014 Received in revised form 2 December 2014 Accepted 7 December 2014 Available online 2 January 2015
Aim: More than two-thirds of cancer patients have one or more chronic diseases besides cancer. The purpose of this study was to get detailed insight into the combined effect of cancer and chronic diseases on general practitioner (GP) consultation rates. Methods: From the NIVEL Primary Care Database we identified cancer patients with diabetes mellitus (n = 629), osteoarthritis (n = 425), coronary artery disease (n = 466), COPD (n = 383) or without a chronic disease (n = 1507), diagnosed with cancer between 2002 and 2010. They were matched on sex, age, practice and chronic disease to 6645 non-cancer controls. Results: 2–5 years after diagnosis, cancer patients without a chronic disease had on average 6.5 GP contacts per year, those with a comorbid disease almost twice as many (ranging from 10 for osteoarthritis to 12.4 for COPD). A similar difference was seen in non-cancer controls. The number of GP contacts for chronic diseases did not differ between cancer patients and controls. The increase in the number of GP consultations with age and number of chronic diseases was similar in cancer patients and controls. Consultation rates were similar in cancer patients and controls if they were stratified by number of chronic diseases while counting cancer as a chronic disease. Conclusions: Two to five years after diagnosis, cancer leads to an increase in GP contacts that is similar to having a chronic disease. This increase does not differ between those with and without a chronic disease and cancer does not seem to increase the impact of having a chronic disease. ß 2014 Elsevier Ltd. All rights reserved.
Keywords: Cancer Chronic disease Comorbidity Primary care General practice Health care use
1. Introduction Cancer is mostly diagnosed above the age of 50, and as the general population ages, the number of older cancer patients is increasing [1]. In old age chronic diseases are common [2], and consequently more than two-thirds of cancer patients have one or more chronic diseases besides cancer [3–5]. The most common chronic diseases in cancer patients are similar to those in the general population, e.g. diabetes mellitus (DM), cardiovascular disease, chronic obstructive pulmonary disease (COPD) and osteoarthritis (OA) [3,4,6]. These chronic diseases may have important clinical implications. First, patients with chronic diseases seem more vulnerable to the complications of cancer treatments [7–9], which may lead to
* Corresponding author at: Netherlands Institute for Health Services Research (NIVEL), P.O. Box 1568, 3500 BN Utrecht, The Netherlands. Tel.: +31 30 27 29 827; fax: +31 30 27 29 729. E-mail address: [email protected] (M.J. (Marianne) Heins). http://dx.doi.org/10.1016/j.canep.2014.12.002 1877-7821/ß 2014 Elsevier Ltd. All rights reserved.
increased symptom burden [10,11]. Reversely, cancer and its treatment may also negatively impact existing chronic diseases, like diabetes [12] and may even increase the risk of developing new chronic diseases, such as cardiac disease [13] and osteoporosis [14]. Previous studies showed that several years after the diagnosis of cancer, patients have significantly more general practitioner (GP) consultations than noncancer controls of the same age and sex. This is seen both in patients with and without a comorbid chronic disease. Patients with both cancer and a comorbid chronic disease have the highest number of GP consultations. It is likely that this effect is different for each chronic disease. However, it has not been studied which chronic diseases have a relatively large effect on GP consultations in cancer patients and should therefore receive increased attention. The exact reason for the increase in GP consultations is also unclear. It does not seem to be because health care use for chronic diseases is increased in cancer patients [15]. In fact, cancer patients are less likely to receive recommended care for their chronic diseases [16–18]. Another explanation may be that cancer patients
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with a chronic disease are more vulnerable to the effects of cancer and its treatment. Or the combination of cancer and a chronic disease may make patients more frail in general. We aimed to get more insight into this synergistic effect of cancer and chronic disease. First of all, we aimed to study whether cancer is related to higher GP consultation rates in patients with specific chronic diseases. We also aimed to study whether the combination of cancer and a chronic disease increases the number of GP contacts specifically related to cancer or the chronic disease. Finally, we aimed to study whether known factors that lead to increased GP consultation rates, such as higher age and a higher number of chronic diseases, have a larger effect in patients with cancer and a chronic disease than in those without cancer, as these patients may be more frail. Studying these aspects may elucidate the reason for the increased GP consultation rates and identify especially vulnerable subgroups that should receive increased attention from their GP. We therefore examined GP consultation rates in cancer patients for four different chronic diseases that are common in cancer survivors and also treated in primary care (DM, OA, coronary artery disease (CAD), and COPD) and compared them with those of patients with the same chronic disease but without cancer. 2. Patients and methods 2.1. Database For this study, data were derived from the NIVEL Primary Care Database (formerly known as LINH). This nationally representative Dutch network consisted of approximately 90 practices at the time data were collected. Participating GPs routinely record data on all patient contacts, including diagnoses made. Diagnoses are coded according to the ICPC-1 (International Classification of Primary Care) [19]. In the Netherlands all inhabitants are obligatorily insured for standard medical care and listed with a GP [20]. 2.2. Patients Based on the ICPC codes recorded in the electronic medical record (EMR), all patients diagnosed with cancer between January 2002 and December 2010 were selected. We excluded skin cancer (ICPC S77), as its clinical impact is often relatively small, and musculoskeletal neoplasms (ICPC L71), as this ICPC code also includes benign tumours. Patients had to be at least 55 years of age at diagnosis, as chronic diseases are less prevalent below this age, and they had to have at least two years of follow-up data available starting from diagnosis. We did not exclude cancer patients in the palliative phase as this phase is not easily discernible in our data and patients may have died due to other reasons than cancer. 2.3. Chronic disease We defined five groups: (1) cancer patients with no chronic disease; (2) cancer patients with DM (ICPC code T90); (3) cancer patients with OA (ICPC codes L89 to L91); (4) cancer patients with CAD (ICPC codes K74 to K76); and (5) cancer patients with COPD (ICPC codes R91 and R95). These diseases were selected from a list of chronic diseases [21], because they have a high prevalence in cancer survivors and are mainly treated in primary care. Presence of these diseases was determined two years after diagnosis based on prior occurrence of the ICPC code(s) in the EMR. 2.4. Control patients We matched each cancer patient to two controls without a known diagnosis of cancer in their EMR from the same group (no
chronic disease/DM/OA/CAD/COPD) based on age (5 years), sex and practice. We chose a ratio of 1:2 for cancer patients and control patients to increase the power of our study. Controls had to have at least two years of data available starting from the date of diagnosis of the cancer patient they were matched to. 2.5. GP consultation rates Annual GP consultation rates two to five years after diagnosis or inclusion were determined from data in the EMR; i.e. contacts with the practice (office visits, home visits or telephone consultations with the GP or nurse specialist) and ICPC codes related to these contacts. Only data from patients who had been registered in the practice during the whole year, and practices that had provided data for at least 48 weeks per year and fulfilled quality requirements (accuracy of diagnostic codes and type of contact) were selected. 2.6. Statistical analyses First we assessed the effect of cancer in each group (no chronic disease/DM/OA/CAD/COPD) by comparing the mean annual number of GP consultations in cancer patients and matched controls. We also compared the mean annual number of consultations with an ICPC code related to cancer. To assess the effect of cancer on chronic diseases, we compared the mean number of GP consultations specifically related to DM, OA, CAD or COPD in cancer patients and matched controls. Next, two factors that could influence consultation rates were examined, i.e. age and the number of chronic diseases. The impact of these factors was tested using multivariate negative binomial regression analyses [22]. We chose this type of regression analysis since our outcome variable, the annual number of GP consultations, is a rate and this type of regression analysis predicts the rate of an event. For each group we built a model with cancer/control patient and age as independent variable. To assess the possible effect of age on the difference between patients and controls we added an interaction variable between both. We built similar models for number of chronic diseases. To correct for repeated measurements, we relaxed the assumption of independence of observations in calculating the variance–covariance estimate using the option vce (cluster). Analyses were performed using STATA1 SE version 12.1. A p-value <0.05 was considered statistically significant. The study was carried out according to the precepts of the Helsinki Declaration, Dutch legislation on privacy and the regulations of the Dutch Data Protection Authority. According to Dutch legislation, approval by a Medical Ethics Committee was not obligatory for this study. 3. Results In our database, 9752 patients were diagnosed with cancer between January 2002 and December 2010, of which 3875 had at least 2 years of follow-up. The others had died, moved, or their practice did not fulfil quality criteria in these years. Two years after the diagnosis of cancer 1507 of the patients with at least two years follow-up (39%) had no chronic disease, 629 (16%) had been diagnosed with DM, 425(11%) had been diagnosed with OA, 466 (12%) with CAD and 383 (10%) with COPD. Cancer patients without a chronic disease were somewhat younger than the other groups (see Table 1). Cancer patients with OA were predominantly female (64%), while those with CAD and COPD were predominantly male. The percentage of patients with breast cancer was lowest in these latter two groups, while lung cancer was much more common in those with COPD. For each of the five groups (no chronic disease/DM/OA/CAD/ COPD) we matched each cancer patient to two controls from the
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Table 1 Background characteristics. No chronic disease
Agea Sex (male)
No-cancer controls (n = 2988)
Cancer (n = 629)
67.1 (8.8) 1453 (49%)
66.8 (8.8) 738 (49%)
70.5 (8.7) 297 (47%)
2.5 (2.3) 3.8 (1.8)
2.5 (2.3) 4.2 (2.1)
2.6 (2.4) 3.8 (1.7)
– – – – –
Number of chronic diseasesb 1 – 2 – 3 – 4 – 5 – Cancer type Breast Prostate Colorectal Bladder Lung Other a b * **
OA
Cancer (n = 1507)
Follow-up (year) Before diagnosis After diagnosis Comorbidity DM CAD OA COPD Other
DM
395 274 256 80 80 422
– – – – –
629 123 89 89 432
(100%) (20%) (14%) (14%) (66%)
– – – – –
196 190 113 64 66
(31%) (30%) (18%) (10%) (11%)
160 118 118 40 34 159
(26%) (19%) (19%) (6%) (5%) (25%)
(26%) (18%) (17%) (5%) (5%) (28%)
No-cancer controls (n = 1223)
CAD
COPD
Cancer (n = 425)
No-cancer controls (n = 825)
Cancer (n = 466)
No-cancer controls (n = 893)
Cancer (n = 383)
No-cancer controls (n = 716)
70.1 (8.4) 574 (47%)
72.5 (8.6) 152 (36%)
72.2 (8.6) 284 (34%)
72.1 (8.3) 294 (63%)
71.7 (8.3) 559 (64%)
71.3 (8.1) 226 (59%)
70.8 (7.8) 432 (60%)
2.6 (2.4) 4.0 (1.8)
3.0 (2.5) 3.9 (1.6)
3.0 (2.5) 4.1 (1.8)
2.8 (2.3) 3.8 (1.5)
2.8 (2.3) 4.0 (1.7)
2.7 (2.4) 3.5 (1.4)
2.7 (2.4) 3.8 (1.5)
1223 246 203 135 807
405 361 227 136 94
(100%) (20%) (17%) (11%) (69%)
82 76 425 58 322
(19%) (18%) (100%) (14%) (76%)
164 120 825 93 604
(20%) (15%) (100%) (11%) (73%)
121 466 80 89 340
(26%) (100%) (17%) (19%) (73%)
238 893 141 135 666
(27%) (100%) (16%) (15%)* (75%)**
84 83 52 383 293
(22%) (22%) (14%) (100%) (77%)
166 141 114 716 563
(23%) (20%) (16%) (100%) (79%)
(33%) (30%) (19%) (11%) (8%)
102 138 74 51 60
(24%) (32%) (17%) (12%) (14%)
225 251 172 93 84
(27%) (30%) (21%) (11%) (10%)
100 139 101 57 69
(25%) (30%) (22%) (12%) (15%)
220 271 189 117 96
(25%) (31%) (22%) (13%) (11%)
85 101 83 56 58
(22%) (27%) (22%) (15%) (15%)
145 202 168 90 111
(20%) (28%) (23%) (13%) (16%)
130 74 74 25 22 100
(31%) (17%) (17%) (6%) (5%) (24%)
74 112 77 39 40 124
(16%) (24%) (17%) (8%) (9%) (27%)
64 68 67 29 66 89
(17%) (18%) (17%) (8%) (17%) (23%)
Age at diagnosis for cancer patients and age at inclusion for controls. Both chronic disease that were prevalent two years after diagnosis and new ones that developed between 2 and 5 years after diagnosis. p = 0.03. p = 0.046.
chronic disease (see Table 2). Patients with DM had the highest number of consultations related to their chronic disease (mean 2.7 per year) and those with OA and CAD the lowest (mean 0.3 and 0.4 per year). These numbers did not differ between cancer patients and matched controls. The number of GP consultations increased with age (Fig. 1a–d) and with the number of chronic diseases (Fig. 2a–d). Both increases were similar in cancer patients and matched controls (see Table 3). If the average number of GP consultations was stratified by the number of chronic diseases and cancer was counted as a chronic disease, no differences were found between patients with and without cancer (Fig. 2a–d). Although the figures for diabetes and CAD may indicate some differences between patients with and without cancer, these were non-significant (see Table 3).
same group, practice, age (5 years) and sex. 225 cancer patients, equally divided between the 5 groups, could not be matched to a control and 175 patients could only be matched to one control. No significant differences in baseline characteristics were found between cancer patients and controls (see Table 1), except for the fact that cancer patients with CAD were more likely also to have COPD (19% versus 15%, p = 0.03) and less likely to have another chronic disease (73% versus 75%, p = 0.046). Cancer patients without a chronic disease had the lowest number of GP consultations in the period of 2–5 years after diagnosis; on average 6.4 per year. For cancer patients with a comorbid disorder this number ranged from a mean of 10.1 consultations per year for those with OA to 12.3 for those with COPD. In all five groups, cancer patients had significantly more GP contacts (p < 0.001) than the matched controls. The difference between those with and without cancer was somewhat higher in those with CAD or COPD than in those with DM or OA (see Table 2). The number of consultations specifically related to cancer was on average one per year, both in patients with and without a
4. Discussion We studied the combined effect of cancer and chronic diseases (i.e. diabetes mellitus, osteoarthritis, coronary artery disease and
Table 2 Mean number (standard deviation) of GP consultations (total number/consultations for chronic disease and for cancer) per year in the period of 2–5 years after diagnosis/ inclusion for patients with a chronic disease and cancer. Chronic diseasea
Cancer
Non-cancer controls
Cancer patients
Non-cancer controls
Cancer patients
Non-cancer controls
Cancer patients
Non-cancer controls
4.0 10.0 8.7 8.4 9.7
– 2.7 0.3 0.4 1.3
– 2.9 0.2 0.4 1.3
0.9 0.9 0.8 0.9 1.1
– – – – –
5.6 8.3 9.0 10.0 9.8
4.0 7.1 8.5 8.1 8.4
Total Cancer patients No chronic disease DM OA CAD COPD a *
6.4 11.9 10.1 11.2 12.3
(9.3)* (12.5)* (11.1)* (11.9)* (13.7)*
(4.9) (8.9) (8.3) (8.0) (9.1)
(3.7) (1.1) (1.0) (3.7)
Consultations related to specific chronic disease (DM/OA/CAD/COPD). p < 0.005.
(3.7) (0.9) (1.1) (4.2)
(5.0) (5.6) (3.6) (3.6) (5.7)
Other
(6.7) (9.4) (9.8) (10.7) (10.3)
(4.9) (7.4) (8.2) (7.9) (7.6)
M.J.M. Heins et al. / Cancer Epidemiology 39 (2015) 109–114
15 10 5 0
55-64
65-69
70-74
75-79
>=80
Age (years)
CAD
20 15 10 5 0
55-64
65-69
70-74
75-79
>=80
Age (years)
DM
20 15 10 5 0
55-64
65-69
70-74
75-79
>=80
Age (years)
Number of GP consultaons per year
No comorbidity Number of GP consultaons per year
20
Number of GP consultaons per year
Number of GP consultaons per year
Number of GP consultaons per year
112
OA
20 15 10 5 0
55-64
65-69
70-74
75-79
>=80
Age (years)
COPD
20 15 10
Cancer
5 0
Controls 55-64
65-69
70-74
75-79
>=80
Age (years)
Fig. 1. Mean number of GP consultations per year in the period of 2–5 years after diagnosis of cancer with and without comorbid chronic diseases by age.
Number of GP consultaons per year
DM
20 15 10 5 0
1
2
3
4
5
Number of chronic condions (pre-exisng & new)
CAD
20
20
15
15
10
10
5 0
our sample size was relatively large, it did not allow us to study the combined effects of cancer with less common chronic diseases. Data were derived from EMRs, which could be incomplete, but (1) practices used these files for reimbursement claims with insurance companies, (2) it is unlikely that EMRs of cancer patients were more incomplete than those of non-cancer patients, especially as cancer patients and controls were matched on practice, (3) we applied recording quality criteria for practices (more than 50% valid ICPC codes, data available for at least 48 weeks per year). In the
Number of GP consultaons per year
Number of GP consultaons per year
Number of GP consultaons per year
COPD). We found that two to five years after diagnosis, cancer leads to an increase in GP contacts, both in patients with and without a chronic disease. Cancer does not seem to affect the impact of chronic diseases and does not affect the impact of age or the number of chronic diseases on health care use. Using a large primary care registry with routinely recorded data, we could include a large number of cancer patients. This enabled us to study the effect of individual chronic diseases and several determinants of GP consultation rates of cancer patients. Although
5 1
30
OA
20 15 10 5 0
1
2
3
4
20
COPD
15 10 5 0
1 2 3 4 4 Number of chronic 5 1 2 3 condions (pre-exisng & new) Number of chronic condions (pre-exisng & new) Number of chronic condions (pre-exisng & new) 2
4
5
Cancer
5
Number of chronic condions (pre-exisng & new)
5
Controls
Fig. 2. Mean number of GP consultations per year in the period of 2–5 years after diagnosis of cancer for patients with different comorbid chronic diseases by number of chronic conditions (cancer counted as a chronic condition).
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Table 3 p-Values of regression models examining the effects of age sex and comorbidity. Model
1. Age
Cancer Age (years)
Cancer Age
2. Comorbidity
Cancer No. of chronic diseases (cancer included)
Cancer No. of chronic diseases
55–64 (ref) 65–69 70–74 75–79 80 Cancer 65–69 Cancer 70–74 Cancer 75–79 Cancer 80 1 2 (ref) 3 4 5 Cancer 3 Cancer 4 Cancer 5
No. chronic disease
Diabetes
Arthritis
CAD
COPD
p-Value
p-Value
p-Value
p-Value
p-Value
<0.001 – 0.02 <0.001 <0.001 <0.001 0.99 0.84 0.83 0.85
<0.001 – 0.72 0.008 0.002 <0.001 0.74 0.46 0.74 0.43
0.03 – 0.26 <0.001 <0.001 <0.001 0.92 0.51 0.89 0.85
0.007 – 0.13 0.01 0.001 <0.001 0.20 0.65 0.98 0.77
0.003 – 0.06 0.008 0.001 <0.001 0.29 0.24 0.76 0.66
0.20 0.008 – 0.001 <0.001 <0.001 0.50 0.28 0.15
0.90 <0.001 – <0.001 <0.001 <0.001 0.50 0.81 0.89
0.14 0.004 – 0.027 <0.001 <0.001 0.76 0.93 0.56
0.06 0.146 – 0.055 0.001 <0.001 0.69 0.43 0.37
– – – – – – – – –
Netherlands, disease management programmes for diabetes have been widely implemented within primary care since 2010. Consultations related to these programmes are missing in our data, but mean number of GP consultations in diabetes patients was only slightly lower when excluding data from 2010 to 2011 (11.4 instead of 11.9 consultations per year for cancer patients and 9.7 instead of 9.8 for controls). Previous studies have also found that several years after diagnosis, cancer patients with chronic diseases have increased GP consultation rates, when compared to those without chronic disease [17,18]. These studies were also based on data from the NIVEL Primary Care Database. However, in the paper of Jabaaij et al. repeat prescriptions were included and in the paper of Heins et al. effects of individual chronic diseases were not examined so results cannot be directly compared. Heins et al. did find that in patients with colorectal cancer and matched non-cancer controls with a chronic disease, the difference between both groups increased with age [17]. This was not found in patients with breast or prostate cancer, so the effect of chronic diseases may differ between cancer types. In the current study, the difference between cancer patients and controls did not decrease with age, which may be because in the current study we included all cancer types. Although we used a large primary care registry, we could only study the impact of relatively common chronic diseases. We therefore do not know whether our results apply to other, less common chronic diseases. Besides, effects of chronic diseases may also differ by cancer type. This question can only be answered by studying a very large cohort of cancer patients. Another limitation is that we could not determine the exact date of diagnosis of the chronic disease if this was long before the cancer diagnosis. We therefore could not take this variable into account in our analyses. It would also be interesting to see whether GP contact rates increase when cancer patients develop more chronic diseases. Future research could also focus on designing and implementing primary care programmes for cancer. We found that two to five years after diagnosis, cancer leads to an increase in GP consultations, both in those with and without a chronic disease. The increase is similar to that caused by having a chronic disease. As many cancer patients have one or more chronic diseases, their care is complex. Specialists and GPs should therefore collaborate in the care for these patients. It is necessary that GPs adapt their way of treating patients with cancer, which is
currently often reactive [23]. They could learn from the approach with which they are treating patients with chronic diseases and develop care programmes for cancer patients, based on principles derived from the Chronic Care Model, i.e. proactive, patientcentred care that meets the needs of cancer patients with or without co-morbidity [24]. GPs may be trained and reassured in their capability of offering aftercare to cancer patients in the period 2–5 years after diagnosis Conflict of interest The authors have no conflict of interest to declare. Funding This study was financially supported by Alpe d’HuZes/Dutch Cancer Society, grant no. 4870. The sponsor did not have any role in study design; in the collection, analysis and interpretation of data; in the writing of the report; or in the decision to submit the article for publication Authorship contribution Study concepts: all authors Study design: all authors Data acquisition: JK Quality control of data and algorithms: MH Data analysis and interpretation: all authors Statistical analysis: MH, JK Manuscript preparation: MH Manuscript editing: JK, GD, MR, FS Manuscript review: all authors. References [1] Ferlay J, Parkin DM, Steliarova-Foucher E. Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer 2010;46(March (4)):765–81. [2] van Oostrom SH, Picavet HS, van Gelder BM, Lemmens LC, Hoeymans N, van Dijk CE, et al. Multimorbidity and comorbidity in the Dutch population – data from general practices. BMC Public Health 2012;12:715. [3] Ogle KS, Swanson GM, Woods N, Azzouz F. Cancer and comorbidity: redefining chronic diseases. Cancer 2000;88(February (3)):653–63.
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