In our analysis of palliative oncology literature, the studies identified in our search were subdivided based on publication date, either from 1995–2005 or 2006–2016. The 100 most-cited articles from each time frame were selected in order to limit the scope to the most impactful studies in the field. Each study was systemically examined and categorized with the intent of characterizing palliative oncology literature collectively, charting trends within the field, and elucidating new avenues for subsequent research. In such a nascent field, early studies have primarily sought to substantiate the benefits of palliative oncology care. As a result, this foundational work has contributed to an increased awareness of palliative oncology research and its application to patient care.
Across all publications included in our study, 8 articles were cited over 500 times. As expected, these predominantly occur in the 1995–2005 timeframe, which would allow each study to accumulate more citations in a time dependent manner. All but 1 of the articles were published after 1999, and the 2 overall most-cited articles by Temel J.S. et al. and Wright A.A. et al. were published in 2010 and 2008, respectively. This suggests an increased interest in palliative oncology in scientific investigation over the past decade as indicated both by their number of citations and citation rates.
In both time frames, 1995–2005 and 2006–2016, the analysed studies primarily used mixed cancer types in their inclusion criteria. Not selecting for specific cancer types facilitates a large enough patient population to generate a sufficiently powered study. This pragmatic approach to patient recruitment may reflect the general increase in clinical oncology research. Research protocols which limit participation in additional studies or trial fatigue on the part of patients may impact the type and quantity of patients available for study. Nonetheless, the underlying premise appears to be that type of cancer would have limited influence on the administration of palliative care as opposed to having cancer in general. Lung cancer, in contrast, may have been the most frequently used specific cancer type because its experiences and symptoms present a unique scenario for receiving palliative care. Although a more intuitive explanation for studying palliative care in lung cancer is simply because more patients are available for study due to overall cancer epidemiology and prevalence. [11] If principles of palliative care are held to be largely universal in their application to oncology, the mixed cancer approach is appropriate. Nonetheless, cancer, more so than many other medical problems, represents a very heterogeneous set of diseases, each with a very distinct set of palliative needs. This stems from differences in comorbidity, life style, cancer symptoms, and treatment complications, which vary widely from one cancer to the next. Therefore, future investigation of palliative care in oncology should focus on specific cancer types in order to better delineate the impact of treatment.
After classifying the topics of each study, several trends were suggested from the outcome of this analysis. Studies performed in the later time period were less likely to study the role of prognosis in palliative care. This decrease may correspond with the publication of the seminal paper by Christakis at el. in 2000 which found that only 20% of physicians demonstrated accurate prognostic capability at the end of life. Based on the conclusions of this study, many investigators may have forgone attempts at additional prognostic models and have focused their efforts on other areas. Alternatively, the benefit of early integration of palliative care in advanced disease management may be increasingly accepted, decreasing the utility of prognosis for this purpose. Pain and symptom management had numerous studies between 1995–2005. Research in this area may have waned due to a dearth of new drug development and the challenge of studying subjective criteria such as pain and symptoms, which are particularly susceptible to the placebo effect. Then in 2006–2016, an uptick in studies about religion and spirituality occurred. Although there does not appear to be a clear antecedent in the literature, there is clearly a growing awareness of and interest in understanding the role of spirituality in the mental health and physical experience of patients and families living with serious illness. The work of prolific authors, such as Prigerson H.G., on this topic may also have a disproportionate effect on shifting the body of research in the relatively small field of palliative care.
A particularly interesting topic is the example of end-of-life discussions. This exact phrase did not appear in any of the studies from 1995–2005 but was referred to in more general terms such as “communication.” This heightened emphasis and validation of end-of-life discussions contributed to the inclusion of advance care planning for the first time on the Medicare physician fee schedule in 2016. [12] The increasing acceptance of the proven benefits of palliative oncology likely contributed to the increase in studies assessing the effectiveness or limitations in providing access to its services. The topic of health care utilization was increasingly studied more recently. Emergency department visits, hospitalization, admission to the intensive care unit, and other metrics of care were often used a proxy for cost and aggressive medical intervention for patients at the end of life. Lastly, the psychosocial aspects of palliative oncology remained the consistent and most frequent study topic. These studies often reflected on the holistic experience of cancer and the ability of palliative care to alleviate the dying process. Overall, the distribution of study topics increased between 1995–2005 and 2006–2016, indicating a diversification of the research being undertaken in this field.
In order to address the aforementioned topics, investigators did not limit their studies exclusively to patients (although this represented the majority), but included studies examining caregivers and healthcare providers as well. Studies examining palliative oncology in geriatric populations are underrepresented considering the incidence and mortality rates due to cancer are highest in patients 65 years and older. [13] In 2006–2016, hospitals and countries became study populations, representing a shift in scope from patient-level to a more macroscopic, population based analysis. Very few randomized controlled trial (RCT) were used until 2006–2016. This increase may be a response to the paucity of high-quality clinical evidence due to the ethical and practical challenges of conducting RCTs in palliative care. [14, 15] Analysis of the literature reveals that palliative oncology studies consistently rely on interviews and surveys, which have the potential of introducing greater subjectivity into the data.
An ongoing challenge of this relatively young field is the concentration of highly-cited literature coming from a select number of countries. Within these countries, such as the United States, studies are originating most often from handful of institutions. This is in contrast to research in other fields of oncology, particularly in drug development or therapeutic cancer clinical trials, which have robust involvement from Europe and East Asia. While the United States led in absolute terms of publications, Switzerland, Canada, and Sweden led as a factor of their total population in 2005 during the 1995–2005 period. During 2006–2016, Canada again remained a relatively productive source of published studies for its 2015 population size along with the Netherlands and Israel. This may reflect differences on how healthcare systems or social factors influence the recognition of palliative care as a distinct specialty. Regardless, our analysis shows an influx of new investigators making significant contributions to the field since 2006. Although no author remained amongst the 5 most published between the two time frames, the top authors in 2006–2016 produced over half (n = 54) of the studies as compared to only one-third (n = 34) of the top authors in 1995–2005. Focused but high-impact journals such as Journal of Clinical Oncology are the preferred outlet for publishing their work. Since research publication is the currency of career advancement in academia and foundation for improvement in clinical practice, these investigators and journals could offer valuable resources for future collaboration and publication.
The inherent bias of this analysis is that it favours older articles and may neglect recently published studies that, while significant, may have less citations. [16] In an attempt to control for lead-time publication date, the studies have been ranked based on number of citations per year, which will limit the effect of the absolute number of citations. However, more recently published articles may still not have had adequate time for inclusion in the top 100. Recently published articles with sufficient citations may have added importance, particularly those in Table 3. Although citation analysis is a frequently employed tool in scientific literature evaluation, number of citations may not necessarily correlate with a study’s impact and is an imperfect proxy for determining significance. [17] This analysis is unable to control for disproportionate citation due to institutional, language, or self-citation biases. Of note, several studies included subjects with non-malignant disease, resulting in a mixed study population. This may limit the ability to directly infer all findings to an exclusive cancer population.
By examining the 100 most-cited palliative oncology studies in 1995–2005 and 2006–2016, we were able to identify and analyze research trends across the literature. Existing palliative care studies in oncology largely focused on multiple–as opposed to single–cancer types, addressed the impact of palliative care on communication and end-of-life decisions, and were rarely RCTs. Early questions of pain, symptoms, and survival in palliative oncology have been replaced with studies addressing access to care and healthcare utilization. The relation of religion and spirituality to the field also has recently become a frequent area of investigation. Such information may prove useful in directing future study and highlighting the ongoing need for high-quality clinically-based research.
