Detection of Colon Cancer Recurrences During Follow-up Care by General Practitioners vs Surgeons

Julien A. M. Vos, MD; Edanur Sert, MSc; Wim B. Busschers, MSc; Laura A. M. Duineveld, MD, PhD; Thijs Wieldraaijer, MD, PhD; Jan Wind, MD, PhD; Sandra C. Donkervoort, MD, PhD; Marc. J. P. M. Govaert, MD; Frédérique H. Beverdam, MD; Anke B. Smits, MD, PhD; Willem A. Bemelman, MD, PhD; Gijsbert Heuff, MD, PhD; Henk C. P. M. van Weert, MD, PhD; Kristel M. van Asselt, MD, PhD

Disclosures

J Natl Cancer Inst. 2023;115(5):523-529.

Abstract and Introduction

Abstract

Background: In the I CARE study, colon cancer patients were randomly assigned to receive follow-up care from either a general practitioner (GP) or a surgeon. Here, we address a secondary outcome, namely, detection of recurrences and effect on time to detection of transferring care from surgeon to GP.

Methods: Pattern, stage, and treatment of recurrences were described after 3 years. Time to event was defined as date of surgery, until date of recurrence or last follow-up, with death as competing event. Effects on time to recurrence and death were estimated as hazard ratios (HRs) using Cox regression. Restricted mean survival times were estimated.

Results: Of 303 patients, 141 were randomly assigned to the GP and 162 to the surgeon. Patients were male (67%) with a mean age of 68.0 (8.4) years. During follow-up, 46 recurrences were detected; 18 (13%) in the GP vs 28 (17%) in the surgeon group. Most recurrences were detected via abnormal follow-up tests (74%) and treated with curative intent (59%). Hazard ratio for recurrence was 0.75 (95% confidence interval [CI] = 0.41 to 1.36) in GP vs surgeon group. Patients in the GP group remained in the disease-free state slightly longer (2.76 vs 2.71 years). Of the patients, 38 died during follow-up; 15 (11%) in the GP vs 23 (14%) in the surgeon group. Of these, 21 (55%) deaths were related to colon cancer. There were no differences in overall deaths between the groups (HR = 0.76, 95% CI = 0.39 to 1.46).

Conclusion: Follow-up provided by GPs vs surgeons leads to similar detection of recurrences. Also, no differences in mortality were found.

Introduction

Colon cancer is a common disease worldwide.^[1] In 2021, there were more than 9000 patients diagnosed with colon cancer in the Netherlands.^[2] In turn, this is leading to a large number of patients who require survivorship care after they have been treated with curative intent. Survivorship care consists of several components, including follow-up (monitoring and detection of recurrences) and aftercare and rehabilitation.^[3]

In the Netherlands, survivorship care is provided by a surgeon, whereas general practitioners (GPs) do not play a formal role. However, in practice, GPs often provide support to patients in terms of aftercare and rehabilitation.^[4] It has therefore been suggested that GPs could play a greater role in survivorship care.^[5,6] GPs are familiar not only with patients' medical history but also with their social context, which may help personalize care to the individual needs.^[7] This has led to the initiation of the Improving Care After colon canceR treatment in the Netherlands, personalized care to Enhance quality of life (I CARE) study in 2015.^[8] In this randomized study, colon cancer patients were allocated to receive survivorship care by a GP vs care by a surgeon. Within the first year after surgery, care by the GP did not improve quality of life recovery, the primary outcome of the study.^[9] Other outcomes are therefore important to consider.

Follow-up is aimed at the surveillance of recurrences, either locally recurrent disease, and also metastases and new colorectal malignancies. Follow-up of colon cancer consists of routine check-ups for 5 years after treatment, including blood tests, imaging, and colonoscopy.^[10] To date, limited studies have looked at the effects of follow-up provided by a GP on outcomes such as the detection of recurrences and mortality.^[11] The effects on these outcomes remain uncertain and highlight the need for larger, randomized trials.^[12,13] Here, we report a secondary outcome of the I CARE study. We assessed the detection of recurrences and the effect on time to detection of recurrences and overall death of transferring follow-up care from surgeon to GP.

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Next Section

Abstract and Introduction
Methods
Results
Discussion
References

Table 1. Baseline characteristics of the participants ^a
Characteristics	Care by a general practitioner (n = 141)	Care by a surgeon (n = 162)	P
Sociodemographic
Age, mean (SD), y	67.9 (8.3)	68.2 (8.4)	.83
Sex, No. (%)
Females	43 (30)	57 (35)
Male	98 (70)	105 (65)	.39
Living situation, together, No. (%)	107 (76)	120 (74)	.89
Educational attainment, No. (%)			.17
Primary or non	14 (10)	13 (8)
Secondary	28 (20)	40 (25)
Vocational education	75 (53)	71 (44)
University	12 (9)	24 (15)
Missing	12 (9)	14 (9)
Randomly assigned to Oncokompas, No. (%)	68 (48)	83 (51)	.60
Clinical and pathological
Comorbidities, No. (%)			.21
0–1	63 (45)	84 (52)
≥2	78 (55)	78 (48)
Cancer diagnosis via, No. (%)			.45
Population screening	74 (53)	78 (48)
Clinical course	67 (48)	84 (52)
Tumor stage, No. (%);			.10
I	59 (42)	54 (33)
II	50 (36)	54 (33)
III	32 (23)	54 (33)
Stoma, No. (%)	6 (4)	7 (4)	.98
Chemotherapy, No. (%)	27 (19)	41 (25)	.26
Time to inclusion, median (IQR), mo	3.6 (1.8–5.9)	3.5 (1.8–6.1)	.97

^aIQR = interquartile range.

Table 2. Recurrences and deaths
Outcome	Care by a general practitioner (n = 141)	Care by a surgeon (n = 162)	Total participants (n = 303)
Recurrences, No. (%)	18 (13)	28 (17)	46 (15)
Diagnosis via abnormal follow-up test results, No.	14	20	34
Imaging	8	13	21
Carcinoembryonic antigen	5	7	12
Colonoscopy	1	NA	1
Diagnosis via symptoms, No.	4	6	10
(Abdominal) pain	2	3	5
Weight loss	1	1	2
Changes in stool	1	NA	1
Other^a	2	3	5
Diagnosis via other route, No.^b	NA	2	2
Localization of recurrence, No.
Liver	8	7	15
Gastrointestinal tract and/or peritoneum	3	7	10
Lungs	2	4	6
Lymph nodes	1	2	3
Multiple sites (stage IV)	3	7	10
Other ^c	1	1	2
Treatment of recurrence, No.
With curative intent	12	15	27
Palliative (or no treatment)	6	13	19
Deaths, No. (%)	15 (11)	23 (14)	38 (13)
Reason of death, No.
Related to colon cancer	7	14	21
Unrelated^d	8	9	17

^aPatients may experience multiple symptoms. Other symptoms include coughing (n = 2), dyspnea (n = 1), clavicle lump (n = 1), and symptomatic abdominal wall hernia (n = 1).
^bRecurrence was found after a positive fecal occult blood test (n = 1) and as an incidental finding on a chest computed tomography after trauma (n = 1).
^cOther localizations include bone metastases (n = 1) and abdominal wall (n = 1).
^dUnrelated causes of death include second primary cancers (n = 11), cardiac failure (n = 2), stroke (n = 1), complications after trauma (n = 1), progressive parkinsonism (n = 1), and COVID-19 (n = 1).

Table 3. Survival analysis
Outcome	Care by a general practitioner vs surgeon HR (95% CI)
Recurrences
Intention-to-treat
Univariable	0.75 (0.41 to 1.36)
Multivariable^a	0.78 (0.43 to 1.43)
Per-protocol
Univariable	0.68 (0.36 to 1.26)
Multivariable^a	0.71 (0.38 to 1.34)
Deaths
Intention-to-treat
Univariable	0.76 (0.39 to 1.46)
Multivariable^a	0.70 (0.36 to 1.35)
Per-protocol
Univariable	0.53 (0.25 to 1.12)
Multivariable^a	0.49 (0.23 to 1.04)
Restricted mean survival time in each health state, y
Disease-free	2.76 (2.68 to 2.85) vs 2.71 (2.62 to 2.83)
Recurrence	0.21 (0.13 to 0.29) vs 0.25 (0.13 to 0.33)
Death	0.03 (0.00 to 0.04) vs 0.04 (0.00 to 0.07)

^aThe following variables were included in multivariable analyses treatment with adjuvant chemotherapy and presence of comorbidities. CI = confidence interval; HR = hazard ratio.

Authors and Disclosures

Julien A. M. Vos, MD^1,2,*, Edanur Sert, MSc¹, Wim B. Busschers, MSc¹, Laura A. M. Duineveld, MD, PhD¹, Thijs Wieldraaijer, MD, PhD¹, Jan Wind, MD, PhD¹, Sandra C. Donkervoort, MD, PhD³, Marc. J. P. M. Govaert, MD⁴, Frédérique H. Beverdam, MD⁵, Anke B. Smits, MD, PhD⁶, Willem A. Bemelman, MD, PhD⁷, Gijsbert Heuff, MD, PhD⁸, Henk C. P. M. van Weert, MD, PhD^1,2 and Kristel M. van Asselt, MD, PhD^1,2, on behalf of the I CARE study Group^†

¹Department of General Practice, Amsterdam UMC, Location University of Amsterdam, Amsterdam, the Netherlands
²Amsterdam Public Health, Research Programme Quality of Care, and Personalized Medicine, Amsterdam, the Netherlands
³Department of Surgery, Onze Lieve Vrouwe Gasthuis, Amsterdam, the Netherlands
⁴Department of Surgery, Dijklander Hospital, Hoorn, the Netherlands
⁵Department of Surgery, Franciscus Gasthuis & Vlietland Hospital, Schiedam, the Netherlands
⁶Department of Surgery, St. Antonius Hospital, Nieuwegein, the Netherlands
⁷Department of Surgery, Amsterdam UMC, Location University of Amsterdam, Amsterdam, the Netherlands
⁸Department of Surgery, Spaarne Gasthuis, Hoofddorp, the Netherlands

*Correspondence to
Julien A. M. Vos, MD, Department of General Practice, Amsterdam UMC, Location University of Amsterdam, Post-Box 22660, 1100 DD Amsterdam, the Netherlands (e-mail: j.a.m.vos@amsterdamumc.nl).

^†A. A. W. van Geloven and A. W. H. van de Ven.

Disclosures
The authors declare that they have no competing interests.

Authors contribution
Anke B. Smits, MD, PhD (Conceptualization; Data curation; Writing – review & editing), Frédérique H. Beverdam, MD (Conceptualization; Data curation; Writing – review & editing), Marc. J.P.M. Govaert, MD (Conceptualization; Data curation; Writing – review & editing), Willem A. Bemelman, MD, PhD (Conceptualization; Data curation; Writing – review & editing), Kristel M. van Asselt, MD, PhD (Conceptualization; Supervision; Writing – review & editing), Henk C.P.M. van Weert, MD, PhD (Conceptualization; Supervision; Writing – review & editing), Gijsbert Heuff, MD, PhD (Conceptualization; Data curation; Writing – review & editing), Wim B. Busschers, MSc (Conceptualization; Formal analysis; Visualization; Writing – review & editing), Edanur Sert, MSc (Data curation; Project administration; Validation; Writing – review & editing), Julien Vos, MD (Conceptualization; Data curation; Formal analysis; Project administration; Validation; Visualization; Writing – original draft; Writing – review & editing), Laura A.M. Duineveld, MD, PhD (Conceptualization; Data curation; Project administration; Validation; Writing – review & editing), Sandra C. Donkervoort, MD, PhD (Conceptualization; Data curation; Writing – review & editing), Jan Wind, MD, PhD (Conceptualization; Funding acquisition; Project administration; Supervision; Writing – review & editing), Thijs Wieldraaijer, MD, PhD (Conceptualization; Data curation; Project administration; Validation; Writing – review & editing).