Any child with cancer is a childhood cancer survivor (CCS) from the time of diagnosis, and will continue to be one for the rest of his or her life.1 In Spain, approximately 950 children less than 15 years of age are diagnosed with cancer each year.2 In recent decades, their survival rate has increased spectacularly thanks to the progressive improvement in the available treatments, the creation of referral units in hospitals and international cooperation studies.3 The overall five-year survival rate for childhood cancer in the autonomous community of the Region of Murcia is approximately 80%, very similar to the rates for the whole of Spain (77% in the 2000–2003 period) and Western Europe (81% from 1995 to 2003).4,5 This increase in survival has brought forth the need to monitor for possible late relapses and the risk to develop subsequent neoplasms,6–8 chronic diseases and dysfunctions that affect quality of life at earlier ages than the general population.4,9,10 By the second decade of life, more than 60% of CCSs will suffer from at least one chronic disease related to the treatment they have received and/or associated environmental risk factors.11 This trend continues to rise during the life of the survivor, and by around 50 years of age more than 50% of CCSs will have experienced a severe or disabling life-threatening or fatal disease.12 National and international agencies recommend a structured and if possible lifelong follow-up of CCSs.4,13–15 Different models to guarantee the adequate follow-up of survivors are being considered. In the Region of Murcia, which has an established public primary care (PC) health system, we have developed a shared-care model for the transition from hospital care (long-term follow-up unit) to primary care (PC) that is tailored to the specific needs of each CCS. Most adult and some adolescent CCSs are followed-up by their primary care physicians (PCPs),15–17 and an appropriate transition from hospital to primary care is essential to guarantee the adequate long-term follow-up of CCSs. In Spain, the transition to PC is still performed in a mostly unstructured manner.18 The aims of this study were to: (a) assess the beliefs, attitudes and preferences of PC physicians regarding the follow-up of CCSs, and (b) explain the basic structure of the Childhood Cancer Survivor Long-Term Follow-up Programme of the Region of Murcia (Programa de Largo Seguimiento de Supervivientes de Cáncer Pediátrico en la Región de Murcia [PLASESCAP-MUR]).

We conducted the study in Health Area 1 (Murcia/Oeste) of the Region of Murcia, which has a total population of 256725 inhabitants and a population under 15 years of age of 45302. Health Area 1 comprises 14 basic health zones (BHZs) each of which has a designated primary care centre. It has 38 paediatric clinics and 127 family medicine clinics. Table 1 shows the distribution of childhood cancer in Area 1 Murcia/Oeste over the 1998–2014 period. The PLASESCAP-MUR programme includes individuals diagnosed with cancer at ages less than 15 years since 1998.19 A total of 113 children were diagnosed with cancer in Area 1 during this period. In 2014, 32 (28%) of CCSs were older than 18 years of age. Inclusion in the long-term follow-up programme is granted to all patients that received a cancer diagnosis during childhood if three or more years have elapsed since the end of treatment and they have remained disease-free. Table 2 shows the structure and questionnaires of the PLASESCAP-MUR.20–27 Prior to implementing the PLASESCAP-MUR training activities in the PC setting, questionnaires were sent to the medical coordinator of each of the 14 BHZs for their distribution to the 172 physicians. Of these physicians, 71% were family physicians, 22% paediatricians and 7% resident physicians. The self-administered questionnaire had a structured format and assessed the attitudes, preferences and beliefs of PC family physicians and paediatricians concerning the follow-up of CCSs.28–30 The questionnaire, which is available on the PLASESCAP-MUR website,20 consists of 13 questions about the follow-up of CCSs: demographic characteristics, medical training and professional characteristics of the providers. Physicians were asked whether they had cared for any CCSs in the past five years and how often they had been given a detailed report or personalised long-term follow-up plan (diagnosis, types of treatment and dosages, identified risks, late effects), measured on a 5-point Likert scale ranging from 1 (never) to 5 (always). A similar scale was used to measure their level of comfort in caring for CCSs, from 1 (very uncomfortable) to 5 (very comfortable) and their familiarity with the existing guidelines for the long-term follow-up of CCSs, ranging from 1 (not at all familiar) to 5 (very familiar). Physicians were also asked about their preferences for the care of CCSs (referral to a different level of care, independent care offered by the physician, or shared care with the long-term follow-up clinic). They were asked about the usefulness of four tools that may improve the care of CCSs (detailed report, long-term follow-up guidelines, continued education and communication by telephone or electronic mail with the long-term follow-up clinic), using the same type of scale ranging from 1 (not at all useful) to 5 (very useful). Finally, they were asked whether improvements in environmental quality would reduce morbidity and mortality in CCSs on a scale from 1 (strongly disagree) to 5 (strongly agree) and to rate how different environmental risks can affect CCSs on a scale from 1 (very little) to 4 (to a great extent). We performed descriptive and regression analyses to assess the possible correlation between qualitative variables and the number of years the physician had been practising medicine. The confounding variables selected a priori were sex and the number of patients seen per week. We performed all the statistical analyses with the SPSS software version 15.0 (SPSS Inc., Chicago, USA).

All the BHZs agreed to participate in the study. We received 100 questionnaires out of the 172 that had been sent out (response rate, 58.1%). The response rate was slightly higher among paediatricians than among family physicians (60.5% vs. 55.1%; P=.9). Of all respondents, 49.4% reported having seen at least 1 CCS in the 5 years preceding completion of the questionnaire. Table 3 summarises the demographic and professional characteristics of the participating physicians. Eighty-four percent reported that they had never or rarely (Likert scale score ≤2) received a detailed report or personalised long-term follow-up plan (diagnosis, type and dosage of treatments, identified risks, late effects) for CCSs. Only 34.0% of the surveyed physicians reported feeling “comfortable” or “very comfortable” (Likert scale score ≥4) providing care for CCSs. Ninety-five percent preferred to care for CCSs in collaboration with the long-term follow-up clinic, while none of the respondents preferred being solely responsible for their follow-up.

Of all respondents, 37.1% was familiar with the long-term follow-up guidelines for CCSs (Likert scale score, 1.5). Table 4 shows the perception of clinicians regarding the usefulness of different tools used in the follow-up of CCSs. More than 80% of the surveyed PC physicians considered that generally speaking, the different resources used to improve the quality of the follow-up of CCS (detailed report, long-term follow-up guidelines, continuing education and direct contact with the long-term follow-up clinic) were quite or very useful (Likert score ≥4).

Of all respondents, 80.2% strongly agreed or agreed (Likert scale score ≥5) that improving environmental quality could reduce the morbidity and mortality of CCSs. They expressed that the environmental risks that affect CCSs most often are (Table 5): exposure to pesticides (mean, 3.74), environmental smoke (mean, 3.67), ionising radiation (mean, 3.62), outdoor air pollution (mean, 3.62) and legal or illegal drug use (mean, 3.53). We found a significant association between the number of years physicians had been practising medicine and the importance they attributed to the impact of environmental factors on CCSs, such as a lack of contact with nature, the state of the living setting, the use of legal and illegal drugs, exposure to second-hand smoke and sedentary lifestyles.

To our knowledge, this is the first study conducted in Spain that analyses the attitudes, knowledge and preferences of PC physicians concerning the follow-up of CCSs. Furthermore, we asked PC physicians about the association between environmental risks and the morbidity and mortality of CCSs. Most of the physicians (80%) strongly agreed or agreed that improving environmental quality would succeed in reducing the morbidity and mortality of CCSs, and identified the environmental risks that affect them most: exposure to pesticides, exposure to environmental tobacco smoke, ionising radiation, outdoor air pollution and use of legal/illegal drugs. Several studies have emphasised the need for lifestyle changes and reducing or eliminating the environmental risks as being among the most important goals in the long-term follow-up of CCSs.3,31,32 Chief among the findings in our study was that 84% of the surveyed physicians stated that they had never or rarely received a detailed report from the oncology centre presenting not only the diagnosis and general aspects of the treatment, but also a personalised risk assessment and long-term follow-up plan. We believe that this report or survivorship care plan constitutes a fundamental pillar around which to build a quality long-term follow-up,3,33 and so do physicians, of whom 91% considered that it was quite useful or very useful. The basic elements of such a plan include a summary of the treatments received, information on the potential late effects that may develop, and recommendations for follow-up.34,35 Having a personalised care plan increases the probability of patients receiving adequate follow-up care and does not increase their worry about cancer.30,33 These data are similar to those of other studies conducted in the United States, where the use of care plans for CCSs was low (<20%) but PC physicians considered them very useful (>90%).29

Another salient finding is that 66% of physicians reported feeling somewhat uncomfortable or uncomfortable treating CCSs and 95% preferred to care for them in collaboration with a specialised long-term follow-up unit. Their discomfort in treating CCSs could be related to a lack of experience in the follow-up of survivors by professionals in the PC setting. Nathan et al.28 found similar results in their study, in which 85% of respondents preferred caring for CCSs in collaboration with oncologists or in the context of a long-term follow-up programme.

Previous studies have shown that CCSs are at greater risk of morbidity and mortality during childhood, adolescence and adulthood, usually due to late relapses, secondary tumours and an increased susceptibility to the early development of chronic diseases of adulthood.36,37 This makes CCSs a particularly vulnerable group, and consequently it is very important to ensure an adequate long-term follow-up of these patients, preferably for life.4,13–15 Ideally, follow-up would extend to the children and grandchildren of CCSs. In Spain, as in most western countries, long-term follow-up programmes for CCSs are being set up.38 Patients are mostly followed-up by oncologists and haematologists that treat the primary disease and perform the follow-up for a variable and increasingly long period of time. Sooner or later, patients are discharged from these services and transferred to PC, where paediatricians or family physicians will be their primary care providers and be responsible for their follow-up.3,15–17 The province-based organisation of care provision and the prior experience of two referral units, the Unidad de Salud Medioambiental Pediátrica of Murcia (Unit of Paediatric Environmental Health [PEHSU]) and the Unidad de Oncología y Hematología Pediátricas (Paediatric Oncology and Haematology Unit) of the Hospital Clínico Universitario Virgen de la Arrixaca, has allowed the launching of an integrated long-term follow-up programme. In the PLASESCAP-MUR programme, patient care and follow-up are based on the individual needs of each patient. The programme is carried out by the long-term follow-up clinic and PC services in a shared care model.39 Thus, as the programme continues to develop, PC paediatricians, family physicians and nurses will be increasingly engaged in the follow-up of CCSs. One of the goals of the PLASESCAP is education in, and the promotion of, healthier environments and lifestyles for the survivor, his or her family and the community, in order to improve their environmental quality and quality of life. Another goal is the performance of screenings for the early detection and appropriate management of late effects of the disease and the treatments received by the patient.20 The PLASESCAP will address a good portion of the needs identified through the questionnaire, promoting access to quality reports for the long-term follow-up of each CCS and increasing the skills of PC healthcare professionals in the management of CCSs. One of the limitations of this study is the low response rate (58.1%), although it was higher than response rates in similar studies in PC settings (which range between 23% and 45%)28,29 and similar to the 61% response rate for questionnaires administered to hospitalists.30 The low response rate may have been due to the lack of knowledge on this topic of providers in this BHZ. The questionnaires were collected prior to a clinical training session on CCSs and a second round could not be administered, as we believed that the responses could have been biased after the session, and we were unable to analyse the characteristics of nonrespondents. On the other hand, while the sample was small, it was representative of the Health Area, as it included all of its physicians. Last of all, since our findings are based on the perceptions of PC physicians, they may not reflect what actually occurs in clinical practice.

Using the resources available through the national health system of Spain, with its high coverage, quality, and focus on prevention through PC, to develop long-term follow-up programmes, could offer better health options to this subset of the population.

This study was funded partially by the Plan de Formación Continuada (Continuing Education Programme) of the Health Area 1 of Murcia Oeste, Servicio Murciano de Salud (Murcia Health Service), training action n. I-14-10184-14, and the grant MD 001452 IP: Dr. Luz Claudio, National Center on Minority Health and Health Disparities of the National Institutes of Health.

The authors have no conflicts of interest to declare.