Pancreatic cancer is one of the most challenging types of cancer because there are no effective prevention or early detection methods and treatment options are limited. Pancreatic cancer ranks fourth as a cause of cancer deaths, with more than 40 500 estimated deaths for 2015 in the United States.1 By 2030, scientists predict that pancreatic cancer will be the second leading cause of cancer death.2 Despite significant improvement in survival rates for many types of cancer, the death rate for pancreatic cancer has slowly increased over the past decade. In fact, the overall 5-year survival rate for patients in the advanced stage is approximately only 2%.1,3
The complexity of the disease and treatment and the rapid physical deterioration pose special challenges to symptom management for patients with advanced pancreatic cancer (APC). Symptoms, which are the “perceived indicators of change in normal functioning as experienced by patients,”4(p68) may be both complex and severe and significantly impact health-related quality of life (HRQOL). For patients with APC and their caregivers, symptom management is the primary goal of care. However, although some studies have begun to focus on special symptoms or symptom clusters among different critically ill cancer populations, such as leukemia and lung and ovarian cancer,5–7 little is known about the symptom experience of patients living with APC. Emphasis has been placed on developing or evaluating treatment methods rather than symptom management.
There is a lack of comprehensive and systematic approaches to understanding symptoms and their impact in patients with APC. This knowledge gap not only contributes to poor symptom management but also ignores how symptoms interfere with patients’ survival duration, HRQOL, psychological health, communication, decision making, and preparing for death.4,8 Furthermore, because of the quick disease progression, APC is an ideal prototype to understand symptom changes and care needs in patients who face rapid transition from healthy status to terminal illness.9,10 Therefore, the purpose of this integrative review is to synthesize current evidence regarding APC patients’ symptom experiences. Findings from this review will inform future research directions and help healthcare providers design comfort measures that support patients as they manage and cope with symptoms.
This integrative review was designed to fully examine the symptoms experienced by patients with APC and used the methodological strategies proposed by Whittemore and Knafl.11 An integrative review was selected because it allowed us to include heterogeneous resources such as different research methods and varying data collection instruments. The steps of the review included (1) problem identification, (2) literature search, (3) data evaluation, (4) data analysis, and (5) presentation of findings.
Literature describing the symptom experience of patients with APC was identified by searching in 4 databases: PubMed, Cumulative Index to Nursing and Allied Health Literature (CINAHL), Embase, and PsychINFO. We used 2 medical subject heading searches to find citations in PubMed: (1) “pancreatic neoplasms” AND “symptom assessment” OR quality of life” and (2) “pancreatic neoplasms,” “signs and symptoms,” AND “terminal care.” The CINAHL headings of “pancreatic neoplasms” AND “symptoms” OR “quality of life” were used to search in the CINAHL, and the Emtree terms of “pancreas cancer,” “terminally ill patients,” AND “symptoms” OR “quality of life” were used to search in Embase. Emtree terms are hierarchically structured terminologies, which are used to index the Embase content. For PsychINFO, subject terms of “neoplasms,” “pancreas,” AND “symptoms” OR “quality of life” were used. In addition to subject terms, we also used key words (ie, “pancreatic cancer” AND “stage three” OR “stage four” OR terminal OR palliative) AND (symptoms OR signs OR “quality of life”) to search aforementioned databases. Search limitations were English language, human sample, and year published (2005–2015) because treatment protocols for APC advance quickly. Each journal article’s reference list was also carefully searched by hand to identify additional pertinent articles. The search results were imported into EndNote X7.5 and duplicates were removed. We then reviewed the titles, abstracts, and full text of the articles based on the inclusion and exclusion criteria to determine their eligibility.
INCLUSION AND EXCLUSION CRITERIA
Based on the theoretical definition of symptom experience in Armstrong’s concept analysis and Lenz’s Theory of Unpleasant Symptoms, only the patient can report on the symptom experience, including its 4 dimensions: intensity, timing, quality, and distress.4,12 Therefore, manuscripts included in this review include quantitative, qualitative, and mixed-methods studies focusing on physical or psychological symptoms experienced and reported by patients with APC. Patients with APC were defined as patients diagnosed with locally advanced or distant pancreatic cancer that was not eligible for curative surgery at diagnosis. We also included studies with heterogeneous cancer patient populations only if the results for those with APC were analyzed separately.
We excluded manuscripts that:(1) did not report on empirical studies, including opinions, case reports, or editorials; (2) were review articles; (3) did not include patient “self-report” of symptoms; or (4) addressed only symptoms related to a specific drug or procedure because the foci of these articles were on drug toxicity or safety/effectiveness of the procedure versus overall symptom experiences. Moreover, studies focused only on specific drug- or procedure-related symptoms often set inclusion criteria of particular symptom intensity (eg, patients with moderate pain).
We used an author-developed data coding sheet to conduct the 2 steps of data extraction. First, we extracted information regarding authors, year of publication, setting characteristics, participant characteristics, and study design. Second, the symptom-related variables, including type of symptom, measurement instruments, symptom profile (symptom intensity, timing, quality, and distress), and associated factors were identified. The 4 dimensions of symptom profile were defined based on the Theory of Unpleasant Symptoms.4 Specifically, symptom quality is related to characteristics of symptoms (eg, “burning” pain). Symptom intensity quantifies the degree, strength, or severity of symptoms. Timing is related to the occurring time, duration, and frequency. The distress dimension refers to the affective aspect or meaning of symptoms.4 After reading the articles, 2 of the authors (C.T. and D.V.) highlighted relevant information and organized information using the coding sheet. We further created several tables to contrast and compare variables. Tables are presented along with findings in the next paragraph.
A total of 916 articles were initially identified. After removing duplicates (n = 90), the remaining 826 articles were screened by titles, which resulted in a total of 337 articles remaining. After screening the 337 abstracts using the established criteria, 293 articles were excluded. Among the 293 articles, 44% (n = 128) did not report results specific to an APC population; 36% (n = 106) were nonempirical, non–peer-reviewed, or review articles; 16% (n = 47) did not include patient-reported symptoms; and 4% (n = 12) addressed only symptoms related to a specific drug or procedure. Among the 44 articles that were retained for full-text review, 29 were excluded because they (1) did not include patient-reported symptoms (n = 11), (2) addressed only symptoms related to a specific drug or procedure (n = 11), (3) did not report results specific to an APC population (n = 6); and/or (4) were not written in English (n = 1). A hand search of each manuscript’s reference list resulted in adding 1 more article. Thus, a total of 16 studies was included in the analysis (Figure).
All 16 studies were quantitative, with 5 descriptive studies,13–17 4 correlational studies,18–21 and 7 quasi-experimental studies.22–28 Six of the 16 studies (37.5%) explored overall symptom experiences or the relationship among symptoms in patients with APC,15,17–21 and 2 studies (12.5%) compared symptom experiences across different pancreatic cancer stages.13,16 Five studies (31.25%) focused on pain or pain management strategies for patients with APC,14,22,23,27,28 and the remaining 3 studies (18.75%) focused on interventions other than pain management.24–26 Only 2 of the 16 studies explicitly described a guiding theory or framework. The theoretical frameworks used were systematic inflammation17 and descriptions of nociceptive and neuropathic pain.14 The number of study participants ranged from 20 to 654, and the APC patients’ medium survival duration for those articles that reported on this variable (n = 8) was about 6.36 months (range, 3.5-8.9 months). About half (n = 8) of the studies were conducted in Europe15,17,18,21–24,26 and the other half in North America (n = 7).13,14,16,19,20,25,27 One study was conducted in Asia.28Table 1 displays study aims, designs, population, and symptom-related results. From our review, we organized the studies by symptom types and instruments, symptoms identified, symptom profiles, and factors associated with symptoms.
All studies used instruments to evaluate predetermined symptoms. The 9 instruments used in the 16 studies were in 2 categories: 1 focused on evaluating cancer patients’ multiple symptoms and HRQOL and the other focused solely on pain. Six instruments that focus on multiple symptoms are the European Organization for Research and Treatment of Cancer (EORCT QLQ-C30) with or without the pancreatic special module (EORCT QLQ-PAN26), the Edmonton Symptom Assessment Scale, the European Quality of Life–5 Dimensions, the Functional Assessment of Cancer Therapy general module (FACT-G) with or without the hepatobiliary module (FACT-HEP), the Linear Analog Scale Assessment, and the MD Anderson Symptom Inventory. Table 2 displays the symptom inventory captured by these 6 instruments. Three instruments focused solely on pain are the McGill Melzack Pain Questionnaire,14 the Brief Pain Inventory,22 and a single item for rating pain intensity and frequency.24 Overall, the EORTC QLQ-C30 and/or EORTC QLQ-PAN26 were the most frequently used measurement tools (n = 8),13,15,17,18,20,23,26,27 followed by the FACT-G (n = 2).16,22 Although investigators used a variety of different instruments to measure symptoms, some symptoms are included in instruments more often than others. Specifically, almost all symptom evaluation instruments measured pain and depression symptoms. However, taste change, numbness, and most psychological symptoms were addressed by only 1 or 2 instruments.
All studies identified physical symptoms, and 9 of the 16 (56.25%) studies13,15,17–19,21–23,25 also covered psychological symptoms. Table 3 shows authors, the symptoms reviewed, and measurement instruments. Importantly, Table 3 also displays the problematic symptoms identified by each study and the corresponding operational definitions of problematic symptoms. The physical symptoms identified in the APC samples were pain, fatigue/lack of energy, loss of appetite, dry mouth, taste change, digestive problems (eg, nausea, vomiting, altered bowel habits, indigestion, and flatulence), respiratory problems (eg, dyspnea), and poor sleep. The psychological symptoms were related to sense of well-being, anxiety, depression/sadness, emotional distress/mood disturbance, life enjoyment, and fear. Congruent with our previous observation that all instruments measured pain, pain was the most prevalent symptom discussed in all studies, followed by fatigue (n = 11, 68.75%), digestive symptoms (n = 9, 56.25%), and loss of appetite (n = 7, 43.75%). However, although depression was also included in most instruments used, it was only discussed in 6 (37.5%) of the studies.
Symptom Profile: Intensity, Timing, Quality, and Distress
In this section, we report APC patients’ symptom profiles using the Theory of Unpleasant Symptoms’ 4 dimensions: intensity, timing, quality, and distress. Most of the studies found that patients with APC had substantial physical and psychological symptoms, especially as related to the intensity dimension.13,15–28 Compared with the healthy population and early-stage pancreatic cancer population, patients with APC reported more total symptoms and more intense symptoms such as fatigue, appetite loss, pain, digestive symptoms (eg, indigestion), anxiety, and depression.13,15,16,25 Although the researchers used various instruments with different operational definitions to determine the level of intensity of symptoms, they reported that a considerable number (more than 25%) of patients experienced moderate to severe intensity of symptoms that included fatigue,15,18–20,26–28 loss of appetite,15,18–20,26–28 pain,13,15,19,20,24–27 insomnia,20,26–28 digestive symptoms,13,26–28 impaired sense of well-being,15,18 anxiety and depression,25 and fear.13 Fatigue, loss of appetite, and pain were the top 3 severe symptoms reported.
Eleven studies explored fatigue, and most of these reported patients’ average fatigue intensity was moderate to severe.15,18–20,26–28 In those articles that provided more specific information, 19% to 63% patients experienced moderate to severe fatigue.15,17–19 Similarly, studies examining loss of appetite (n = 7) reported that the average intensity of appetite loss was moderate to severe,15,18–20,26–28 with about 24% to 63% of patients in those articles giving that information having loss of appetite that was moderate to severe.15,18,19 With regard to pain, patients experienced moderate to severe pain on average regardless of treatment types or disease progression.13,15,20,26 Specifically, 15% to 43% of patients with APC reported moderate to severe pain.17–19,24 Symptom intensity changed along with treatment and disease progress. Although pain20,27,28 and insomnia20,27,28 improved significantly after treatments (eg, celiac plexus block surgery), the intensity of several physical symptoms including fatigue,28 digestive symptoms,15,18,26,28 dyspnea,15 and dry mouth15 worsened with general care, palliative resection, or celiac plexus block surgery. For loss of appetite, some studies found a significant improvement after celiac plexus block surgery27,28; and other studies demonstrated that the symptom got worse with general care and palliative bypass surgery.20,26
Among the studies reporting psychological symptoms (n = 9), the focus was on sense of well-being,15,18,23 depression,15,17–19,22,25 and anxiety.15,18,29 Two studies found that patients with APC experienced moderate to severe impairment in their sense of well-being, which worsened as the disease progressed.15,18 Studies presented contradictory findings regarding depression. Some showed that most patients experienced mild depression, with mean intensity scores of 2 to 3 out of 10,15,19 whereas others showed that about 40% of patients experienced moderate to severe depression.17,18 Similarly, Bye and colleagues (2013) found that 37–44% patients experienced moderate to severe intensity of anxiety, although the mean intensity score for anxiety reported by Labori et al (2006) was at a mild level. Regardless of the intensity level, Romanus et al (2012) reported that more than half of the patients experienced anxiety and depression. When the disease progressed, the intensity of anxiety and depression stayed the same or slightly increased.15,18 Most studies used EORTC QLQ-C30 to measure anxiety and depression.15,17,18
Three studies examined the timing dimension of the symptoms, including frequencies24 and possible coexisting symptoms or symptom clusters.17,19 Muller et al (2008) reported that 51% of the patients with APC had daily pain. For the coexisting symptoms, Reyes-Gibby et al (2007) reported all possible symptoms, but Laird and colleagues (2011) focused on the common symptom cluster of pain, fatigue, and depression in cancer patients. These 2 studies found that about 24% to 51% of the patients had 2 or more coexisting symptoms with moderate to severe levels of intensity. The proportion of patients with such symptoms tended to increase temporarily during chemoradiation.19 Specifically, researchers identified 2 possible symptom clusters. Laird et al reported more than double the number of patients who would have been expected to have had the symptom combination of pain, fatigue, and depression if the symptoms were to coexist by chance. Reyes-Gibby et al (2007) reported a strong relationship between fatigue and loss of appetite. Only 1 study explored how patients described their symptom quality verbally.14 With a very small sample size, Dobratz (2008) could not distinguish pain patterns (eg, nociceptive vs neuropathic pain) based on APC patients’ word choices. No study explored the distress dimension of the symptoms.
Factors Associated With Symptoms
A number of factors were noted to play into APC patients’ symptom experiences. Researchers found that fatigue, loss of appetite, pain, and mood were significantly associated with other factors such as comorbidity, mortality, function or performance level, energy intake, psychological status, HRQOL, social relationships, and survival duration. Specifically, fatigue was negatively associated with energy intake and predicted the interference levels of walking, activity, work, enjoyment of life, and survival.18,19,21 Loss of appetite was not only linked to physical function such as energy intake, walking, and activity, but it also predicted psychological function including mood and enjoyment of life.18,19 Pain was negatively related to performance, energy intake, and relationships with other people.18,19,21,22 One study further indicated that pain intensity can predict survival in patients receiving chemotherapy. In this study, researchers also found that poor performance was associated with impaired mood.21 Low energy intake and complex comorbid medical conditions were linked to higher overall symptom intensity.18,19
The purpose of this review was to synthesize current evidence regarding APC patients’ symptom experiences. Based on the 16 reviewed studies, all using a quantitative approach with a predetermined symptom inventory, our main findings were that patients with APC experienced multiple intense physical symptoms, especially fatigue, loss of appetite, and pain. With limited and inconsistent study results, APC patients’ experiences regarding psychological symptoms remain unclear. Similarly, evidence of coexisting symptoms or symptom clusters in the APC population is limited. However, current evidence suggests that coexisting symptoms exist. Although there is no qualitative study that met our inclusion criteria, qualitative evidence supported one of our main findings: Patients with APC incur a number of complex symptoms that can become debilitating. Qualitative studies exploring terminal pancreatic cancer patients’ concerns showed that patients and their caregivers experienced several symptoms and expressed their great concerns about both physical and psychological symptoms.30,31 The following paragraphs further discuss findings in depth with several identified knowledge gaps.
First, the use of various symptom measurement instruments makes it difficult to compare identified symptoms and symptom intensity across studies. Instrument variation is especially problematic when interpreting psychological symptoms because every instrument uses different terms and definitions in relation to psychological symptoms (eg, depression and sadness). Instruments such as the Linear Analog Scale Assessment measure psychological symptoms using 1 general term (ie, mood) to capture patients’ experience with regard to depression, anxiety, and stress. Furthermore, all reviewed studies focused only on intensity dimension of predetermined symptoms because of forced-choice instruments and might ignore other symptoms and other symptom dimensions such as quality and distress. Another problem with regard to the instrument is that using the instruments designed to measure HRQOL to evaluate symptoms, as most of our reviewed articles did, causes difficulties in understanding and managing nutrition-related symptoms.32
Second, although our results show that fatigue, loss of appetite, and pain were prevalent and intense physical symptoms reported by the patients across studies, these symptoms received disproportionate attention. It is not surprising that pain has been the major focus of studies because pancreatic cancer is widely known to be one of the most painful malignancies.33 All reviewed studies addressed pain, and about half of them focused on pain management strategies. In contrast, only half or fewer of the studies mentioned other problematic physical symptoms (eg, fatigue or loss of appetite) and their symptom management strategies. Our review found that fatigue is a prominent and severe problem in the APC population, which corresponds to existing assumptions in all cancer population.34 On the other hand, there is a growing recognition that loss of appetite is one of the most distressing symptoms for APC and their caregivers but is often overlooked by healthcare professionals.35–37 Although the etiology of loss of appetite is multifactorial and not fully understood, the experience and management of loss of appetite can be particularly complicated for patients with APC because it may be associated not only with treatment and physical deterioration but also with reduced pancreatic function (eg, pancreatic exocrine insufficiency) and depression,18,37 which is a prevalent symptom in this context.38 The disproportion emphasis of physical symptoms is not only obvious in research but also observable in the clinical practice. Two articles that reported the most significant problems faced by healthcare providers when caring patients with APC discussed only pain and anorexia-cachexia.39,40 Other studies showed that whereas pain management has been noted as the most frequent intervention provided in the hospice consultation for patients with APC, nutrition-related evaluation and intervention were documented in less than 15% of the charts.41,42 This ignorance of nonpain symptoms prohibits healthcare providers from understanding APC patients’ symptom profile fully and addressing their needs. A qualitative study reported that pancreatic cancer patients expressed their lack of knowledge, confidence, resource access, and effective communication with healthcare providers when managing their digestive symptoms.32 Our limited understanding of these problematic symptoms may also partly explain why there are still no effective symptom management strategies for most of the symptoms, although APC patients experienced these intense symptoms until death. For example, whereas general treatments (eg, chemotherapy) and pain management surgeries (eg, nerve block) improved pain and insomnia, fatigue and digestive symptoms did not change or even worsened. Studies pointed out that the severe symptoms continuously contribute to APC patients’ poor functional status and HRQOL, with nutrition and digestion symptoms and fatigue being the most significant symptoms affecting HRQOL.32,41,43
Third, psychological symptoms also have received insufficient attention. Only about half of the studies addressed psychological symptoms, and there was little in-depth exploration or discussion. Our findings showed different symptom profiles of psychological symptoms and, because of the limited number of studies looking at these symptoms, cannot either support or reject the mounting evidence of strikingly high psychological distress rates in pancreatic cancer population compared to other types of cancer.38,44,45 For example, although 2 reviewed studies17,18 found that depression was a severe problem, with approximately 33% to 50% of the pancreatic cancer patients experiencing depression,38 other researchers15,19 concluded that depression is mild in the APC population. These different results may be because of different measurement methods (eg, mean symptom score vs the percentage of patients with a high symptom score). However, our results do support that psychological distress is elevated when disease progresses over time.46
Despite the insufficient evidence, qualitative evidence suggested that psychological distress bothers APC patients and their caregivers. Researchers analyzing the types of questions asked by terminal pancreatic cancer patients and their caregivers online indicated that 11% to 23% of the questions were related to psychological concerns.30,47 Interestingly, although maintaining hope is one of the main themes identified with regard to pancreatic cancer patients’ experience,48 only 1 instrument was used by our sample studies that evaluates hope. None of our sample studies addressed hope in their result or discussion. Although the evidence is not enough to determine the possible cause of psychological symptoms in pancreatic cancer,49,50 it is clear that there is a complicated relationship among patients’ physical symptoms, physical symptoms, and health-related outcomes. A qualitative study demonstrated that nearly all patients expressed feelings of anger, frustration, and powerless related to the lack of knowledge of symptoms, unfamiliarity of symptom management strategies, and poor symptom control.32 Researchers suggested that the psychological distress is significantly related to poor QOL, fatigue, pain, and loss of appetite in the pancreatic cancer population.44
Fourth, with only 3 studies exploring pain frequencies and coexisting symptoms, we know little about the timing dimension of the symptoms. Although our findings suggest that symptom clusters may exist, more evidence is needed to determine if there is any unique symptom cluster that is associated with APC. Lastly, we have almost no clues regarding the quality and distress dimension of the symptoms because only 1 article discussed pain quality and no study explored symptom distress.
To our knowledge, this is the first integrative review to explore symptom experiences of patients living with APC. By synthesizing the important evidence and highlighting the knowledge gaps, this review has important implications for both clinical and research practice. For clinical practice, the review findings help to target problems for improved symptom management in APC patients. Furthermore, we have identified pressing needs to raise awareness of and design interventions for a number of poorly managed and severe symptoms. For future research, given that quantitative methodology has been the predominant approach to examine symptom experience of patients with APC to date, qualitative studies are needed to explore the multiple dimensions of symptoms. For both researchers and clinicians, it is imperative to focus on psychological symptoms, which are still underexplored yet were the main concerns mentioned by patients and caregivers during patient-healthcare provider discussions.47 Studying psychological symptoms will facilitate a deeper understanding of the high psychological distress rate and the causes so that interventions to alleviate this distress can be developed.
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