Patient-reported patterns of follow-up care in the ‘Aftercare in Blood Cancer Survivors’ (ABC) study

One out of three individuals will be affected by cancer during their lifetime (Jemal et al. 2011). Due to improvements in diagnosis and treatment, the proportion of cancer survivors is continuously increasing. At present, about half of cancer patients will survive for 10 years or more (Allemani et al. 2018; Lagergren et al. 2019). From a patient’s perspective, cancer survivorship has been divided into three phases: acute defined as cancer diagnosis and treatment; extended defined as the period following treatment; and permanent equivalent to long-term control or cure (Mullan 1985; Mayer et al. 2017).

Because cancer survivors are at increased risk for adverse physical, mental and social consequences, follow-up care is an important component of long-term support (Jacobs and Shulman 2017). How best to provide this support is a matter of debate (Jefford et al. 2022). While comparative studies have been conducted for the most common types of cancer, such as breast, prostate, gynecological, or colorectal (Jacobs and Shulman 2017), little is known about follow-up care for hematologic malignancies (Laidsaar-Powell et al. 2019). Collectively, they are the fourth most frequent type of cancer comprising 9% of all cancer diagnoses (Smith et al. 2011) and 8% of all cancer survivors (Parry et al. 2011).

Blood cancer differs from solid tumors in various ways. First, owing to the hematopoietic system’s complex structure, an unusually large number of subtypes have been defined (Khoury et al. 2022; Alaggio et al. 2022). Second, because of its disseminated nature, systemic drug- or cell-based therapies prevail over local procedures. Radiotherapy is used with decreasing frequency and surgery is not part of the therapeutic armamentarium (Izar et al. 2016; Rezvani et al. 2016; Specht 2016; Slaney et al. 2018). Third, compared to other cancer types, chemotherapy tends to be more intense with more severe and longer lasting side effects (Hodgson 2015). Fourth, the proportion of long-term survivors is high. Despite dissemination, aggressive forms of blood cancer can often be cured and indolent forms can be controlled over prolonged periods of time or may not require treatment at all.

To gather information about the follow-up care received by blood cancer survivors from the University Hospital of Essen, the oldest and one of the largest comprehensive cancer centers in Germany, and to identify and compare patterns of care, we performed a questionnaire-based observational study consisting of two parts. The ‘Aftercare in Blood Cancer Survivors’ (ABC) study included blood cancer survivors who had been diagnosed at our institution before 2010, with an interval from the last intense treatment of at least three years. The retrospective part of the study was based on information provided by the survivors. Its major goal was to identify patterns in follow-up care and characterize the institutions that provide it. In the ensuing prospective part of the study, we compared these institutions with respect to health-related outcomes and resource use.

This report summarizes recruitment of blood cancer survivors and patterns of follow-up care identified in the retrospective part of the ABC study.

The most important findings from the retrospective part of the ABC study are the following: first, the survivors’ willingness to engage in the study was high; second, almost all participants received follow-up care; and third, there were significant differences between follow-up institutions.

Using a ‘repeated reminding’ approach successfully employed before (Stang et al. 2005), almost two-third of eligible patients consented to participate, which is within the range of other large questionnaire-based blood cancer follow-up studies (participation rate 37–78%) (Oerlemans et al. 2012; Parry et al. 2012; Hall et al. 2014; Korszun et al. 2014; Pophali et al. 2020; Armenian et al. 2022; Bhatia et al. 2023). Participation was particularly high in survivors with a long interval from primary diagnosis. Almost half of the participants were beyond year 10 of follow-up care. Thus, the ABC study contributes to filling the knowledge gap in late periods of cancer survivorship (Gallicchio et al. 2021).

More than 95% of blood cancer survivors received follow-up care. This is unlikely to represent the real-world situation. The study design did not allow us to quantify follow-up care utilization among survivors not participating in the study. However, even if none of the non-participants received follow-up care, its overall use would still exceed 60%. As expected, most participants had been diagnosed with curable types of blood cancer (aNHL/HL and AML/ALL), had received curative treatments (AlloTx), or suffered from incurable diseases with good prognosis (MGUS, iNHL/CLL, and MPN/CML). Prognostically unfavorable diseases such as MM or MDS (Khoury et al. 2022; Alaggio et al. 2022) were underrepresented.

Even after years or decades, more than two-third of survivors still came to the university hospital for follow-up care. This may in part be explained by the fact that the transfer of patients to the follow-up program at their own institution is a reflex action for many university hospital physicians. In addition, both patients and oncologists tend to have little confidence in general practitioners to provide follow-up care (Potosky et al. 2011; Jefford et al. 2022).

The large number of patients taking part in the ABC study allowed us to identify two other important care providers. About one-sixth of the survivors were seen by non-university oncologists, and the same percentage by non-oncological internists/practitioners. Most of these worked in private practice. The disease spectrum differed at the three institutions. Patients with a history of allogeneic transplantation were overrepresented at the university hospital. Patients with incurable diseases requiring continuous monitoring (MDS, MGUS, MM, MPN/CML, and iNHL/CLL) were disproportionately often seen by non-university oncologists. By contrast, survivors with curable diseases in stable remission (AML/ALL and aNHL/HL) were frequently followed up by internists/practitioners. Although the patterns of follow-up care observed in the ABC study evolved naturally, they resemble published care models: long-term follow-up clinics (e.g., university hospitals) for survivors with complex needs and a high risk of late effects, specialist-led care for unstable disease states, and general practitioner-led care for stable conditions (Jefford et al. 2022). With increasing follow-up time, an increasing proportion of survivors moved to internist/practitioner-led care. This has also been observed for solid tumor survivors (Pollack et al. 2009), possibly reflecting the assurance that the disease is cured (Oeffinger and McCabe 2006).

In the majority of survivors, follow-up intervals were described as regular, with increasing intervals corresponding to increasing time from treatment. In essence, they reflected expert opinion-based published recommendations (Majhail et al. 2012; Cheson et al. 2014). The follow-up visits were dominated by conversations, physical examination, and blood sampling. While ultrasonography was the most common imaging method in all three follow-up institutions, computed tomography and magnetic resonance imaging were strikingly overrepresented outside the university hospital. Apart from differences in the disease spectrum, dissimilar work environments may explain this observation. Physicians working in a large institution surrounded by specialists from diverse disciplines may tolerate diagnostic uncertainty better than physicians working in private practice, who may try to attain certainty using the most sensitive methods (Simpkin and Schwartzstein 2016).

About half of the survivors were completely satisfied with the follow-up care received. Better psychological support, more medical information, better management of late effects, and help with work-related issues were identified as fields requiring improvement. Similar unmet needs were reported in a systematic review of 18 previous follow-up studies in patients with hematologic malignancies (Swash et al. 2014). Psychological support for cancer patients was in its infancy when the majority of ABC study participants were diagnosed. Meanwhile, its importance has been well recognized and psychosocial care ranks among the top priorities to improve follow-up care in Europe and North America (Lagergren et al. 2019; Gallicchio et al. 2021). The same is true for late effects, whose spectrum will change with changing treatments. Expert knowledge about side effects of novel treatments may argue in favor of follow-up care by cancer specialists (Jacobs and Shulman 2017; Jefford et al. 2022).

High levels of satisfaction with follow-up care have also been reported from the Netherlands (67% of 1135 survivors with a history of a hematologic malignancy [Oerlemans et al. 2012]) and Australia (75% of 696 survivors [Hall et al. 2014]; 49% of 311 survivors [Boyes et al. 2015]). In a study from Colorado restricted to the first 4 years of follow-up care, blood cancer survivors appeared to be less satisfied, with at least one in four reporting considerable unmet needs (Parry et al. 2012). Similar to the ABC study, dissatisfaction was mostly related to deficits in psychological support and information about the disease in general and late treatment effects in particular. In some studies, physical aspects of daily living (Hall et al. 2014; Boyes et al. 2015), sexuality, and financial or employment issues also ranked high (Parry et al. 2012). Comparisons must be done with caution. While the ABC study started in year 4 of follow-up care, the other studies included the transition period immediately after chemotherapy, with no or only a minority of survivors receiving care beyond year 10.

In addition to follow-up visits, a substantial proportion of survivors sought help from family, friends, and other sources. This was particularly evident in bone marrow transplant recipients. Surprisingly, less than 5% had contacts with advocacy groups, and even fewer thought that access to such groups would improve care. This is at variance with a study from California where blood cancer survivors were more likely to make use of support groups than other cancer survivors (41% versus 1–25%). In that study, participation in group activities was perceived as a benefit by most blood cancer survivors (Owen et al. 2007). The discrepant results may be related to differences in sociocultural factors, availability of and information about support groups, patient selection, and sample size.

Not unexpectedly, quality of life was the best among patients not undergoing follow-up care. Such patients are likely a selection of favorable cases such as survivors with MGUS or a history of curable diseases, such as leukemia or lymphoma. At least with regard to the broad categories investigated, quality of life did not differ among follow-up institutions. Our study did not include a non-cancer control group matched for other factors. Therefore, we were unable to compare the blood cancer survivors with the general population.

Limitations of the ABC study’s retrospective part are its reliance on patient reporting, which is subject to participation and recall biases, and the exclusion of patients who died before the study was conducted (prevalence-incidence bias). Patients alive at the time of the survey are a selection of individuals with a favorable disease course. Whether the information provided by them is representative of the entire population remains uncertain. A further limitation is the fact that any comparison of institutions is confounded by differences in disease spectrum and follow-up duration. A strength of our study is its large size with a high proportion of participants in late periods of follow-up care.

Almost all blood cancer survivors participating in the ABC study received follow-up care. There were three major follow-up institutions that exhibited significant differences with respect to disease groups and diagnostic procedures. The naturally evolved patterns observed in the study resemble published care models: follow-up clinics for complex needs, specialist-led care for unstable disease states, and general practitioner-led care for stable conditions. Irrespective of institution, the survivors’ satisfaction with follow-up care was high, but there was room for improvement in psychosocial support and information about late effects.