Follow-up cancer care in Danish general practice: a questionnaire study

Background The number of patients who have survived cancer has increased substantially owing to improved cancer treatment. This has reinforced the need for effective strategies for follow-up cancer care in general practice. Aim To investigate the organisation of follow-up cancer care in Danish general practice and to analyse GPs’ self-assessment of competences regarding patients who have survived cancer and late effects. Design & setting A total of 500 Danish general practices were invited to a web-based survey. Method Questions comprised organisation of follow-up cancer care, and GPs’ self-assessment of their competences in follow-up care and evaluation of late effects. Covariates considered included sex, age, seniority, and practice type. Analyses were conducted using descriptive statistics and multivariable logistic regression models. Results Some 28% of the GPs reported systematic organisation of follow-up cancer care in their clinic. More than half of the GPs assessed themselves as competent in evaluating mental sequelae, existential considerations, and the impact on comorbidities. In contrast, only 19% and 33% of GPs reported competences in sexual and physical sequelae, respectively. Female GPs were less likely to report competences regarding physical and mental sequelae as well as sexual disturbances, and GPs from partnership practices were more likely to report competence in assessing mental sequelae. Conclusion Fewer than one in three general practices have organised systematic follow-up cancer care and GPs assess their competence as low with respect to physical sequelae and sexual challenges. This emphasises the need for more systematic organisation and focus on knowledge of late effects in general practice.


Introduction
Cancer remains a major cause of disease worldwide with almost 20 million new cases in 2020 (1).
The combination of an aging population, improvements in cancer treatment and survival has led to a growing population of cancer survivors worldwide including Denmark (2).Many cancer survivors face late effects for years after end of cancer treatment and often even lifelong (3).
Hence the need for follow-up care is increasing significantly, prompting researchers, healthcare organizers and patient organizations to suggest expanding and reorganising the follow-up cancer care (4).The main part of the follow-up cancer care has traditionally been dealt with by the hospitals in Denmark, though have recent updates of the follow-up programs for cancer by the Danish Health Authority involved task delegation to general practice for the follow-up of prostate, bladder, and kidney cancer.
Due to the expanding needs of e.g., accessibility and individualisation alongside with organizational changes in the healthcare sector as a whole, the importance of general practice' role has been highlighted both nationally and internationally (2).
A recent review concludes that quality of care for cancer patients increases when General Practitioners (GPs) have a proactive approach to the patients, act as interpreters of the cancer diagnosis, assess treatment options, and its consequences, and engage in care coordination with specialists in secondary care while keeping the patients' resources and wishes in mind (5).
Likewise, the Danish Health Authority highlights the GPs´ important role as coordinator throughout the entire course of diagnostics, treatment, and long-term care (6,7).
The guidelines for follow-up cancer care from the Danish College of General Practitioners recommend implementing systematic efforts in general practice to ensure that all cancer patients are offered the necessary follow-up, e.g., by a systematic proactive approach, regular controls, and assessment of the potential late effects.Most cancer patients have at least one comorbidity in addition to their cancer disease, which enhances the risk of physical and psychological distress (8).This emphasizes the need for patient-centred and persistent follow-up care after cancer.
Knowledge on how follow-up cancer care is organized in general practice in Denmark and whether the GPs feel competent to assess e.g., the patients' late effects, is however sparse.To ensure the possibilities of a well-structured and well-organized follow-up cancer care in general practice, knowledge about the current organization and the GPs' qualifications is needed.Thus, the aim of this questionnaire study is to investigate the organisation of follow-up cancer care in Danish general practice and analyse the GPs' self-assessment of competence in addressing late effects, along with the impact on comorbidities and lifestyle.

Setting and design
This study is based on a survey conducted in Danish general practices from September to November 2021.
The GPs play a pivotal role as gatekeepers and care coordinators, collaborating with both primary and secondary healthcare providers in Denmark.Danish GPs are remunerated through taxes in a mixed capitation and fee-for service system, and nearly all medical services are provided to the patients free of charge.Regarding cancer patients, the hospitals possess specialized knowledge about the patient's cancer treatments, late effects and prognosis, and the department provides a discharge summery.The GPs follow the patient throughout their life and manage both acute and chronic conditions.Moreover, they provide continuity of care for the patients and have the opportunity to address the psychological, social, and existential consequences of cancer, including concerns about recurrence.

Subjects and sampling
The study population comprised 500 general practices, 250 from the Capital Region of Denmark and 250 from the Region of Southern Denmark, randomly selected by the unique company registration number (CVR number) and invited to participate in a web-based survey about followup and end-of-life care of cancer patients in general practice.The Capital Region of Denmark was selected due to its status as the largest region in Denmark, boasting the highest number of citizens and GPs.The Region of Southern Denmark was chosen as it mirrors the general population's composition in Denmark.
The invitation to the survey was sent to a digital mailbox linked to the CVR number in September 2021.A reminder letter was sent to the digital mailbox encouraging the GPs to participate after two and four weeks, respectively.Participation was voluntary and an economic compensation corresponding to 20 minutes (approximately 37 €) was offered to each participating GP.

Questionnaire development
The conceptual framework and constructs in the questionnaire were developed based on existing literature and guidelines regarding follow-up cancer care for cancer patients in general practice (5,6).The definition of follow-up cancer aligns with the definition in the guideline for follow-up cancer care in general practice from the Danish College of General Practitioners; Cancer follow-up encompasses processes where the active treatment of cancers patients has concluded or where the patient has transitioned to medical aftercare.We framed it as followed in the questionnaire: "Follow-up care for cancer patients, who has undergone treatment for cancer includes both follow-up care after the active treatment has ended, and the patient is cancer-free, and follow-up care for patients who receive long-term aftercare for their cancer" (6).The definition therefore both include patients who has completed their treatment and patients who receive adjuvant, palliative or no treatment.
Based on the conceptual framework four domains were included in the questionnaire: I) The organisation of follow-up cancer care in general practice, II) Professional efforts and competences in general practice, III) Interdisciplinary and cross-sectorial cooperation and IV) Coordination and coherent processes.For each domain, several items were generated.The questionnaire was assessed and discussed in a multidisciplinary group consisting of a nurse, younger doctors, GPs, and representatives from a patient organisation.
Prior to the distribution of the questionnaire, two pilot tests were conducted to ensure the content validity.In the first pilot test, the questionnaire was sent to GPs associated with the research environment.This test resulted in reduction of questions and clarifications of the definitions of follow-up cancer care.In the second pilot test, the questionnaire was sent to selected general practices in the two regions, resulting in rewordings and comprehension changes.
The final questionnaire included 18 questions.Five questions regarding GP characteristics and 13 questions covering the four domains.
In this paper, we included questions from the first two domains, which relate to the GPs' management and self-assessment of competences in follow-up cancer care.Management included systematic efforts and contacts.GPs answering that they had implemented systematic efforts for follow-up cancer care, had the opportunity to describe their effort in free text boxes.
Self-assessment of competences in follow-up cancer care were related to comorbidities (other somatic diseases and treatments), physical sequelae, sexual sequalae (challenges and problems related to sexuality and intimacy), mental sequelae, social sequelae, existential considerations, and lifestyle challenges.The GPs´ perception of follow-up cancer care and self-assessment of competences in late effects were reported on a five-point Likert scale.

Covariates and statistical analyses
Due to the risk of ambiguous information on practice characteristics and organization of follow-up cancer care, GPs with more than one provider number were excluded prior to invitation.GPs employed in a regional owned practice and GPs with incomplete answers to the questionnaire were excluded from analyses.
The GPs´ ratings for management of follow-up cancer care were categorised as follows; very rarely/rarely, sometimes, and often/very often, and GPs self-assessment of qualifications as; not at all/to a very low degree/to a low degree, somewhat and to a high degree/to a very high degree.
The proportion of answers within each category was calculated by using descriptive statistics, and χ2 test were used to test for differences between groups.
The associations between GP-, and practice characteristics and having implemented systematic efforts (yes/no) were analysed by multivariable logistic regression models.The GPs´ selfassessment of competences were analysed in multivariable ordered logistic regression models including all outcome variable (not at all, to a very low degree, to a low degree, somewhat, to a high degree, and to a very high degree).
The covariates included in the analyses were categorized as followed: Sex: men or women,

Results
From the 500 invited general practices some 173 GPs completed the entire questionnaire (35%), Figure 1.
[Figure 1] The distribution of GP-, and practice characteristics appear from Table 1.

[Table 1]
The GPs most often received information about patients' need for follow-up through discharge letters from the hospital (49%) or from the patients or relatives (47%).Some 41% of the GPs contacted the patients in writing or by telephone encouraging them to contact the practice, if necessary, Table 2.
More than half of the GPs assessed they were qualified to assess mental sequalae (70%), existential considerations (51%), impact on lifestyle (63%), and co-morbidities (59%).Contrary, only 19% and 33% of the GPs, respectively, reported competences regarding sexual and physical sequalae, Table 2. Some 65% of the GPs assessed that the written information from hospital departments met their need for knowledge about the patient's cancer diagnoses, while only 8% had sufficient knowledge about possible side effects and long-term effects of their patient's cancer treatment, Table 2.
[ Table 3] In total 28% of the GPs reported that they had implemented a systematic organisation of followup cancer care in their clinic.Examples of the systematic efforts from the free text boxes appears in Table 4.
[Table 4] Most GPs described efforts to get in contact with the patients and invite them to a consultation.
No associations between GP-, and practice characteristics and having implemented a systematic effort were found in the adjusted analyses, Table 5.

Summary:
We explored the organisation of follow-up cancer care in Danish general practice and analysed the GPs´ self-assessment of competences in addressing late effects.Less than one of three general practices have implemented systematic follow-up cancer care in their clinic.Most GPs assess their own competence high with respect to assess late effects in terms of mental sequalae, existential considerations and impact on co-morbidities and lifestyle.However, the GPs assess their competences lower with respect to physical and sexual sequalae.Female GPs more often report high competences regarding co-morbidities than male GPs, while they rate their competences lower regarding physical-, sexual and mental sequalae.Competences related to assessment of mental sequelae are higher among partnership practices compared to single-handed practices.

Strengths and limitations
The random sample representative of Danish GPs is a strength of the study, yet the participation rate of 35% is lower than desired, but in line with previous survey studies among Danish GPs (9).
Although the respondents were fairly comparable to Danish GPs regarding both gender, age and practice type (9, 10), we cannot rule out non-responder bias.The responding GPs may be more engaged and interested in the topic of follow-up cancer care and palliative care which could lead to an overestimation of the self-assessment of competences and systematic follow-up.Though, this possible overestimation even emphasizes the need for more focus on the knowledge and management of late effects in general practice.Further, the predefined closed answer categories may be a limitation of the study.Therefore, we offered the possibility of elaborating on the organisation of follow-up strategies in free text boxes.A thorough qualitative thematizing and analyses of the text boxes are beyond the scope of this study, but we believe the presented statements provide valuable insights and nuances.
We chose an ordered logistic regression model, as it allows us to include all categories for the outcome variable in an ordered manner, under the assumption that the "distance" between the categories is equal across the range, i.e., fulfilling the proportional odds assumption.

Comparison with existing literature
Previous studies have targeted patients' need of attention to follow-up cancer care, and potential lack of professional awareness from their GPs (11,12,13,14,15).Cancer patients suffer from both specific late effects, which are related to individual cancer sites and treatments, and more general late effect including depression, fear of recurrence, cognitive impairment, sleep disturbances, fatigue, and pain issues (3).Compared to the specific late effects, these general symptoms and diseases are prevalent across all cancer survivors and influence many patients in their daily life.Furthermore, the general late effects are often related, and patients rarely experience only one (3).According to an Australian review, a substantial number of cancer survivors experience unmet needs, particularly in relation to psychosocial challenges (16), which are not adequately dealt with in the existing healthcare system (4).Moreover, many cancer survivors are more likely to die from chronic, often preventable non-communicable disease, rather than from their malignancy (17).
Therefore, lifestyle interventions targeted to each patient's risk profile and personal preferences should also be prioritized, which is a task the GPs are already familiar with.
A prerequisite for the GPs to play a sufficient role in the follow-up care is insight into the patient's course of disease.Many patients have sparse contact with their GPs during their treatment at the hospitals, and the contact need to be reestablished after the end of treatment (18,19).
Participating GPs in the present study reported to receive most information regarding patients in need of follow-up care from the hospital discharge cards or from the patients.However, less than two of three GPs reported that the written information from the hospital met need for knowledge about the patient's cancer diagnoses, and less than ten percent had sufficient knowledge about possible side effects and late effects of their patient's cancer treatment.Being a patient can be a daunting and overwhelming experience, particularly for those who are less familiar with the organisation of the healthcare system or who may have had negative experiences in the past.Far from all patients seek help themselves (19), and some of these people may benefit from systematic follow-up from their GP.The literature points to the fact that health literacy challenges may lead to misinterpretation of symptoms and postponing or omitting relevant healthcare-seeking (20,21), and individuals with health literacy challenges may therefore benefit more from continuity and easy access to consults with the same doctor or nurse every time they contact general practice.

Implications for Research and/or practice
Increasing prevalence of cancer survivors has reinforced the need for strategies for follow-up cancer care, also in general practice.We investigated the organisation of follow-up cancer care in Danish general practice and analysed the GPs´ self-assessment of competences regarding cancer survivors and late effects.Less than one of three Danish general practices have organised systematic follow-up cancer care, and GPs assess their competences as low with respect to physical sequelae and sexual challenges.This emphasises the need for more systematic organisation and focus on management of late effects in general practice, to ensure cancer patients a more coherent and comprehensive follow-up in primary care.
Health systems are continually looking for ways of optimizing resource usage, while maintaining quality of treatment and care (22).Future studies should address the transition from hospital treatment to follow-up in primary care, the importance of collaboration between healthcare seniority in practice: <10 years, 10-19 years, > 20 years, practice type: partnership practice or single-handed practice, and region: Capital Region of Denmark and Region of Southern Denmark.The models were adjusted for sex, seniority, practice type, and region.Data analyses were conducted using Stata statistical software 17 (StataCorp.2021.Stata Statistical Software: Release 17. College Station, TX: StataCorp LLC).All tests used a significance level of pvalue less than 0.05.