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Patient-Reported Experience of Diagnosis, Management, and Burden of Neuroendocrine Tumors

Patient-Reported Experience of Diagnosis, Management, and Burden of Neuroendocrine Tumors ORIGINAL ARTICLE Patient-Reported Experience of Diagnosis, Management, and Burden of Neuroendocrine Tumors Results From a Large Patient Survey in the United States Edward M. Wolin, MD,* John Leyden, MD,† Grace Goldstein, MA,‡ Teodora Kolarova, MA,§ Ron Hollander, MS,|| and Richard R.P. Warner, MD¶ (Pancreas 2017;46: 639–647) Objectives: The aim of this survey was to examine the experience of pa- tients with neuroendocrine tumors (NETs) to raise awareness of the NET- related burden and identify unmet needs. Here, we report data from patients in the United States. euroendocrine tumors (NETs) are a diverse group of malig- Methods: Patients with NETs participated in a 25-minute anonymous N nancies that originate in neuroendocrine cells throughout survey, conducted primarily online from February to May 2014. Survey the body, including the gastrointestinal tract, pancreas, and questions captured information on sociodemographics, clinical characteris- 1 lungs. Neuroendocrine tumors are rare, although incidence rates tics, NET diagnostic experience, disease impact/management, interaction have risen substantially in the United States (partly in response to with medical teams, and NETs knowledge/awareness. improvements in diagnosis and increased awareness), with an age- Results: Of 1928 patients who participated globally, the largest percent- adjusted incidence of 5.25/100,000 people in 2004. Neuroendo- age was from the United States (39%). Approximately 50% of US patients crine tumors can be clinically symptomatic because of the secretion reported being diagnosed with other conditions before receiving their NET of hormones (termed functional tumors) or silent/nonsecretory tu- diagnosis, which for 34% took 5 years or more. Patients experienced many mors, which are generally symptom free (nonfunctional). Lack symptoms on a daily basis as a result of NETs, which had a substantial neg- of clear symptoms associated with NETs leads to delays in diag- ative impact on their work and daily lives. Numerous improvements were nosis, often until advanced stages of the disease when symptoms suggested by patients, including better access to NET-specific treatments 2,3 become more pronounced. and medical teams/centers and better education for the management of Several types of medical specialists and health care profes- disease-related and treatment-related symptoms. sionals may be involved in the diagnosis and staging of NETs, re- Conclusions: This survey demonstrated the significant burden of NETs quiring patients to undergo potentially repetitive and extensive on patients' lives and identified key areas for improvement in diagnosis and examinations. The wide array of imaging techniques, biochemical long-term management, including better access to NET-specific treatments testing, and expertise that are required to characterize the location and specialist medical teams/centers. and grade of the primary tumor and the extent of metastatic dis- Key Words: burden of illness, neuroendocrine tumors, ease could possibly lead to patients receiving conflicting treatment 4,5 patient-centered care, quality of life, surveys, rare diseases plans and misdiagnoses. A large number of health care re- sources are also required for the long-term management of 6,7 From the *Neuroendocrine Program, Montefiore M-E Center for Cancer Care, NETs, with qualitative studies highlighting the lack of a clear 8,9 Bronx, NY; †The Unicorn Foundation, Mosman, New South Wales, Australia; pathway of care for patients with NETs. Neuroendocrine tumor ‡The Carcinoid Cancer Foundation, Inc., White Plains, NY; §APOZ & Friends, management should be highly individualized based on the burden Sofia, Bulgaria; ||Neuroendocrine Tumor (NET) Research Foundation, Boston, and symptoms associated with the tumor and whether the aim of MA; and ¶Mount Sinai School of Medicine, New York, NY. Received for publication June 21, 2016; accepted December 15, 2016. treatment is to ameliorate symptoms or prevent tumor growth. Address correspondence to: Edward M. Wolin, MD, Neuroendocrine Tumor Difficulty in achieving an accurate diagnosis, limited access to Program, Montefiore M-E Center for Cancer Care, 1521 Jarrett Pl, Bronx, NET-specific treatment centers or information about NETs, and NY 10461 (e‐mail: ewolin@montefiore.org). inadequate support as part of ongoing care have been highlighted This study was supported by Novartis Pharmaceuticals Corporation. 8,9 Edward Wolin: honoraria and consultant/advisor: Novartis, Ipsen, Celgene, and in previous studies as issues. A multidisciplinary approach has Advanced Accelerator Applications; John Leyden: travel/accommodations/ been proposed to streamline the care of patients with NETs, in- expenses: The Unicorn Foundation Australia; Grace Goldstein: COO of volving the collaboration of diverse medical disciplines to optimize The Carcinoid Cancer Foundation, Inc.; reports that the foundation has diagnosis, staging, and management, with the aim of enhancing received grants from Novartis, Ipsen, Advanced Accelerator Applications, and Lexicon Pharmaceuticals; travel/accommodations/expenses: Novartis; clinical outcomes and improving patient satisfaction. Teodora Kolarova: travel/accommodations/expenses and honoraria: The impact of NETs on reducing health-related quality of life Novartis; reports that INCA has received grants from Novartis; Ron 11–13 (HRQOL) has been demonstrated using standardized testing. Hollander: executive director of the Neuroendocrine Tumor Research For the United States, Beaumont et al reported significantly Foundation; Richard Warner: honoraria and consultant: Novartis, Pfizer, and Lexicon Pharmaceuticals; research funding: Lexicon Pharmaceuticals. worse HRQOL outcomes on all subscales of the 36-item Short Supplemental digital contents are available for this article. Direct URL citations Form Health Survey and 29-item Patient-Reported Outcome Mea- appear in the printed text and are provided in the HTML and PDF versions surement Information System in patients with NET compared of this article on the journal’s Web site (www.pancreasjournal.com). with the general population. Furthermore, a qualitative study in Copyright © 2017 The Author(s). Published by Wolters Kluwer Health, Inc. This is an open-access article distributed under the terms of the Creative Canadian patients with NET reported negative physical and psy- Commons Attribution-Non Commercial-No Derivatives License 4.0 chological long-term effects, with many experiencing feelings (CCBY-NC-ND), where it is permissible to download and share the work of anxiety and struggling to cope with the chronic and unpredict- provided it is properly cited. The work cannot be changed in any way or able nature of their disease. A substantial financial burden has used commercially without permission from the journal. DOI: 10.1097/MPA.0000000000000818 also been demonstrated in NET patients in the United States, Pancreas � Volume 46, Number 5, May/June 2017 www.pancreasjournal.com 639 Wolin et al Pancreas Volume 46, Number 5, May/June 2017 particularly in the first year after receipt of the diagnosis and re- The survey was deliberately designed to be self-reporting to gardless of whether the patients received surgery or medical ther- appropriately capture patient opinion. Question categories in- apy. Although NETs have been shown to have a clear impact on cluded (1) initial screening; (2) patient's current status; (3) diagno- patients' lives in North America, the patient perspective is not well sis; (4) QOL; (5) NET management; (6) NET treatment; (7) NET documented, and the use of disease-specific quantitative surveys education; and (8) demographics. The majority of survey ques- may provide further insight into the individual symptoms and con- tions were closed ended (ie, participants were provided options 13,14 cerns associated with NETs. from which to choose). The only exceptions were open-ended The International Neuroendocrine Cancer Alliance (INCA) questions related to the collection of numerical data (eg, age, num- consists of 18 independent charitable organizations and patient ber of visits per year to a NET specialist center, etc.). Patients were groups from 15 countries, and aims to be the global advocate for asked to rate certain parameters; responses included “not at all,” patients with NETs. In collaboration with Novartis Pharmaceuti- “somewhat,”“very,” and “extremely” as graded descriptors, and cals Corporation, INCA conducted the first global patient survey when asked the degree to which they (dis)agreed with a particular to gather data about the experience of patients with NETs. This statement, the descriptors “strongly” and “somewhat” were used. survey was designed to increase knowledge regarding NETs from a patient perspective. The main goals were to increase understand- Data Analyses ing of patient needs and challenges with regard to diagnosis, inter- Data from patients in the United States were analyzed using actions with health care professionals, knowledge and awareness the MERLIN (Merlinco, London, United Kingdom) survey soft- levels of NETs, information sources, and long-term management ware. Subgroup analyses were also performed based on the time of the disease. Results of the global survey have been published since diagnosis (<5 or ≥5 years) and if the patient had visited a elsewhere ; this publication presents data analyzed from patients NET specialist center at least once a year. Responses were summa- in the United States with NETs. Results relevant to diagnosis and rized using descriptive statistics, including percentages, means, and the impact that NETs have on patients' daily lives and the US medians. Statistical significance is shown at a 95% confidence in- health care system are highlighted. terval level (P < 0.05). Some responses are presented as a combina- tion of the top 2 responses (eg, somewhat agree/strongly agree; a moderateamount/alot). MATERIALS AND METHODS RESULTS Study Design and Participants Recruitment of patients was conducted primarily online via Patient-Reported Sociodemographics the use of Web site postings, e-mails, flyers, and social media channels of the INCA member organizations/patient advocacy Participants with NETs from the United States represented groups. The global survey was conducted between February and 39% (758/1928) of the total number of patients in the global sur- May 2014. vey and were the largest number of respondents of any participat- ing country. Patients were broadly distributed across the country, with 49 of 50 states represented (North Dakota was the only excep- Survey Details tion). The largest number of respondents were from California The survey was designed and conducted as an equal collab- (87/758; 11%), followed by Pennsylvania (48/758; 6%), and Texas oration between INCA and Novartis Pharmaceuticals. The survey (48/758; 6%). The average patient age was 57 years, with only domains and key questions were originally developed based on 7% (52/758) of patients younger than 40 years, and the majority discussions at the roundtable INCA meeting in March 2013, held of respondents (546/758; 72%) were women (Table 1). Patients during the time of the 10th annual European Neuroendocrine Tu- were well-educated, with 51% (389/758) of patients having at mor Society conference in Barcelona, Spain. Hall & Partners were least a bachelor's degree. At the time of the survey, 42% commissioned to construct and professionally develop the ques- (316/758) of patients stated that they were employed at least part tions; 14 NET patient health consumer groups within INCA had time (including self-employment), 28% (209/758) stated they direct input into question development, and the final questionnaire were retired, and 20% (154/758) had a self-reported medical dis- was reviewed and edited by all members of INCA and Novartis ability. A considerable number of patients required help with between May and October 2013. For transparency, the Novartis day-to-day activities; 59% (449/758) of patients had a close family logo was clearly displayed on all materials, and patients were no- member or friend who acted as a caregiver. At the time of the sur- tified that the INCA patient group partners or Novartis may use vey, the patients who participated had received their NET diagno- the data for disease awareness purposes. Hall & Partners facili- sis a mean of 5.3 years ago. tated conduction of the survey from February to May 2014 and an- alyzed the results. This anonymous survey was designed to be Patient-Reported Clinical Characteristics predominantly completed online, with an estimated duration to completion of 25 minutes. For patients taking the survey in the The most common site that patients reported for primary United States, the survey was available in English and simplified tumors was the gastrointestinal tract (444/758; 59%), followed by Chinese. The English version of the survey used in the United the lung (112/758; 15%), and pancreas (111/758; 15%). The major- States is included as Supplemental Digital Content 1, http:// ity of patients reported having low-grade NETs: 35% (264/758) links.lww.com/MPA/A587. were grade 1 (low) and 17% (127/758) were grade 2 (intermediate). Sociodemographic information, including sex, age, employ- However, 29% (219/758) of patients reported that their physician ment status, and education level, was collected in addition to did not give their NET a grade, and an additional 11% (82/758) patient-reported clinical characteristics such as type, functional stated that their physician did not give or discuss a grade for their status, and grade of NETs. Furthermore, information on desired NET. Almost half of patients (363/758; 48%) had a functional NET, improvements, the burden of NETs on daily life and work, interac- 33% (248/758) had a nonfunctional or asymptomatic NET, and tions with medical teams, and sources of information on NETs 19% (147/758) said that their physician did not discuss the func- were also captured. tional status of their NETwith them or that they did not remember. 640 www.pancreasjournal.com © 2017 Wolters Kluwer Health, Inc. All rights reserved. Pancreas Volume 46, Number 5, May/June 2017 US Patient-Reported Experience of NETs Delays in the Diagnosis of NETs TABLE 1. Patient Sociodemographics and Clinical Characteristics Few patients (131/758; 17%) suspected that the symptoms they were experiencing could be the result of a cancer. The mean Patients (N = 758) patient-reported time from first symptom onset to clinical diagno- Patient-reported sociodemographics sis was 59 months; 34% (259/758) of patients required 5 years or Age, mean, y 57 more for a NET diagnosis, and at diagnosis 57% (434/758) had Age distribution, % metastatic disease. Patients saw a mean of 5.7 health care profes- <40 y 7 sionals before their NET diagnosis, across a mean of 12.7 doctor 40–49 y 15 visits, and only 9% (69/758) of patients were diagnosed at a NET 50–59 y 33 specialist center. The likelihood of being diagnosed at a NET spe- cialist center has increased in recent years; diagnosis occurred at a 60–69 y 33 NET specialist center in 11% (49/438) of patients diagnosed less ≥70 y 11 than 5 years ago versus only 6% (20/320) of patients diagnosed Sex, female, % 72 5 or more years ago. After initial symptoms and tests, 49% Educational level, % (368/758) of patients were initially diagnosed with another condi- Bachelor degree or higher 51 tion before receiving a NET diagnosis, with the most common other Not completed university education 49 diagnoses received including irritable bowel syndrome (182/368; Work status, % 49%), gastritis or another gastric disorder (169/368; 46%), and anx- Employed iety or a psychosomatic-type condition (97/368; 26%) (Fig. 1). Full-time 31 Twenty-two percent (168/758) of respondents received a NET diag- Part-time 6 nosis as an incidental finding while being tested for another con- Self-employed 5 dition, and this occurrence has increased significantly in recent Retired 28 years, with 27% (117/438) of patients being diagnosed with Medical disability 20 NET in this manner in the last 5 years compared with only 16% Not employed/homemaker/student 10 (51/320) of patients who were diagnosed 5 or more years ago. Patient-reported clinical characteristics NET type, % Patient-Reported Diagnostic Experiences Gastrointestinal 59 In total, 57% (435/758) of patients agreed that they were able Lung 15 to get answers to their questions about NETs. The results for this Pancreas 15 were significantly different for patients diagnosed recently com- Thymus 1 pared with those diagnosed 5 or more years ago, with 61% Other 6 (267/438) of patients diagnosed less than 5 years ago agreeing that Site unknown 6 they were able to get answers to their questions about NETs versus I don't know 2 53% (168/320) of patients diagnosed 5 or more years ago. Fewer Tumor grade, %* than half (338/758; 45%) of patients agreed that they had suffi- 135 cient information about NETs after being diagnosed. Only 39% 217 (293/758) of patients “strongly” agreed that they had received com- 36 prehensive medical care after diagnosis, while 32% (239/758) disagreed or “strongly” disagreed. A statistically significant dif- Unknown/don't remember 43 ference in patient response was observed for the time since diag- Functional status, % nosis subgroup analysis: 71% (313/438) of patients diagnosed Functional 48 less than 5 years ago agreed that they had received comprehensive Nonfunctional 12 medical care after diagnosis, compared with 63% (203/320) of pa- Asymptomatic 21 tients diagnosed 5 or more years ago. However, nearly all patients Unknown/don't remember 19 (702/758; 93%) felt that there was a lot of room for improvement Time since diagnosis, mean, y 5.3 in the process of diagnosing NETs. The most commonly desired Time since diagnosis, % improvements were clearer information on the long-term impact <5 y 58 of NETs (504/758; 66%), increased access to NET specialist health 5–9y 28 care professionals (481/758; 63%), better direction on where to find 10–14 y 8 useful NET information (436/758; 58%), and more knowledge- ≥15 y 6 able health care professionals (436/758; 58%) (Fig. 2). Metastatic disease at time of diagnosis, % 57 Surgical removal of primary tumor since diagnosis, % 72 Burden of NETs on Patients' Lives *Grade 1: Neuroendocrine tumors are relatively slow growing, Ki-67 in- Approximately one third of patients reported poor or fair dex of 2% or less; grade 2: NETs have a less predictable, moderately aggres- overall health (251/758; 33%). A majority of patients reported sive course, Ki-67 index 3% to 20%; grade 3: NETs can be highly symptoms as a result of their NET, which were often experienced aggressive, Ki-67 index greater than 20%. on a constant or daily basis (Fig. 3). Overall, the most com- Functional NETs: produce symptoms caused by the secretions of hor- monly reported symptoms were general fatigue/muscle weakness mones (eg, flushing, diarrhea, wheezing, cramping); nonfunctional NETs: (463/758; 61%), diarrhea (416/758; 55%), abdominal pain/cramping do not secrete hormones, but they may cause symptoms caused by the (359/758; 47%), and skin reactions (eg, flushing) (353/758; tumors' growth (eg, pain, intestinal blockage, bleeding). 47%). Patients experienced a number of other conditions as a re- sult of their NET, including poor or abnormal absorption of nutri- ents (207/758; 27%), vitamin deficiency disease (129/758; 17%), and hyperglycemia (121/758; 16%). © 2017 Wolters Kluwer Health, Inc. All rights reserved. www.pancreasjournal.com 641 Wolin et al Pancreas Volume 46, Number 5, May/June 2017 Neuroendocrine tumors were reported by nearly three quar- 43% (172/403) saw a surgeon and 40% (160/403) of patients saw ters of patients to have had at least a moderate negative impact a gastrointestinal specialist compared with 30% (106/355) and on their lives. Thirty-nine percent (293/758) of patients felt that their 26% (94/355) of nonvisiting patients, respectively. Those patients NET had a large negative impact on their lives, 35% (263/758) stated who reported having nurses (204/758; 27%) and physician assis- that they felt a moderate negative impact, and only 27% (201/758) tants (114/758; 15%) as part of their medical team saw them the of patients felt their NET had little-to-no negative impact on most frequently, at intervals of 1 and 2 months, respectively. their lives. The most commonly reported negative impacts on pa- A total of 750 patients indicated that they had received a tients' lives were overall energy levels (540/758; 71%), finances NET-related test; the vast majority of these patients (511/750; (451/758; 59%), and emotional health (441/758; 58%) (Fig. 4A). 68%) reported having had up to 5 NET-related tests per year. How- Patients reported making several lifestyle changes because of ever, 29% (220/750) of patients reported having tests 6 or more their NET. Just 6% (45/758) felt that they made no lifestyle changes times a year; of these, 16% (118/750) had more than 10. The most as a result of their NET. Dietary changes (487/758; 64%), increased common tests performed on patients with NET were medical im- spending on travel (458/758; 60%), and cutting back on physical aging tests (715/758; 94%) (Table 2). activities (435/758; 57%) were the most commonly reported life- Long distances were traveled by NET patients to see their style changes indicated by patients in the survey. medical team. In total, 22% (168/758) of patients traveled more than Many patients also reported a negative impact on their work 125 miles (200 km) to their medical provider; 23% (173/758) trav- life (Fig. 4B). Only patients who were currently working (316/758; elled 13–31 miles (21–50 km), and 27% (204/758) of patients 42% of respondents) answered questions relating to their work only had to travel up to 12 miles (20 km). The median distance life. Many patients (196/316; 62%) stated that they needed to traveled by all US NET patients in the survey was 30 miles take days off work. Furthermore, 30% (94/316) reported asking (48 km). Patients who visited a specialist center at least once a their employer to make accommodations. Other work impacts year traveled more than twice the distance of nonvisiting patients, commonly conveyed by patients were working reduced hours with a median of 50 miles (80 km) traveled for specialist center (65/316; 21%) and stopping work altogether for a time (51/316; visitors compared with 20 miles (32 km) for nonvisiting patients. 16%). Patients who stated that they were not employed or able to work because of medical disability at the time of the sur- Perceptions of Care and Desired Improvements vey (192/758; 25% of total respondents) were asked if their More than half of patients (391/758; 52%) felt that the overall NET was the reason they had to stop working, to which 79% quality of NET treatments available today were good or very good; (151/192) said yes. Patients who were retired at the time of the sur- however, approximately a third of patients (258/758; 34%) felt that vey (209/758; 28% of respondents) were asked about the previous NET treatments available today were poor or very poor. Patients impact NETs had on their work life. Thirty-one percent (65/209) who visited specialist centers felt significantly more satisfied with stated they had to retire earlier than planned, 14% (29/209) had treatment than nonvisiting patients, with 57% (230/403) of pa- to take days off work, and 11% (22/209) had to stop working alto- tients rating treatment quality as good or very good compared gether for a time, whereas 22% (45/209) said their NET had not with 45% (161/355) of nonvisiting patients. affected their work life. Generally, patients felt that they did not have access to treat- ments of which they had heard. The most common treatments patients Management of NETs had heard of were surgery, chemotherapy, and nonchemotherapy-based In the ongoing management of NETs, patients had an average drug therapies (Table 3). Nearly all (718/758; 95%) patients had of 3 health care professionals who were involved in their NET heard of surgery, 82% (618/758) said they had access to surgery, medical team. The health care professionals most commonly seen and 72% (546/758) said they had received or were receiving sur- by patients were oncologists/hematologists (659/758; 87%), gen- gical treatment. Large differences were observed for chemother- eral practitioners/primary care physicians (400/758; 53%), and sur- apy and nonchemotherapy-based drug therapies in terms of geons (278/758; 37%). Patients who visited a specialist center at treatments patients had heard of and treatments patients had ac- least once a year were more likely to see a wider range of specialists; cess to: 80% (603/758) of patients had heard of chemotherapy, FIGURE 1. Diagnoses received before a NET diagnosis. Only includes conditions mentioned by more than 5% of patients. Base: all US respondents who were diagnosed with other conditions (n = 368). Question: Which of the following conditions were you initially diagnosed with before receiving a NET diagnosis? 642 www.pancreasjournal.com © 2017 Wolters Kluwer Health, Inc. All rights reserved. Pancreas Volume 46, Number 5, May/June 2017 US Patient-Reported Experience of NETs FIGURE 2. Desired improvements to the diagnosis of NETs. Base: all US respondents (N = 758). Question: Which of the following, if any, would have helped you have a better experience with your NET diagnosis? dx, diagnosis; HCPs, health care professionals. but only 41% (310/758) said they had access to chemotherapy, significantly higher than nonvisiting patients (243/355; 68%). and 22% (165/758) were currently receiving or had received che- Overall, 76% (579/758) of patients felt they were very knowledge- motherapy. Although 83% (632/758) of patients had heard of able about treatment options. nonchemotherapy-based drug therapies, only 58% (442/758) said Generally, patients felt that improvements could be made by they had access to and 49% (371/758) said they were currently re- health care professionals in terms of understanding and support. ceiving or had received such therapies. Most patients felt that health care professionals in general were ei- Overall, almost all patients (688/758; 91%) felt that more ther somewhat or not at all understanding (380/758; 50%: 121/ treatment options were needed for the ongoing management of 758; 16%) or supportive (336/758; 44%: 58/758; 8%). Of those NETs. A majority of patients (597/758; 79%) believed that there patients who reported seeing specific health care professionals, is room for improvement in the management of NETs. Eighty- oncologists/hematologists (492/659; 75%), nurses (151/204; three percent (336/403) of patients who visit a NET specialist cen- 74%), and surgeons (192/278; 69%) were felt to be the most ter at least once a year felt that they were very knowledgeable understanding health care professionals. The same health about the treatment options available to them, which was care professionals were considered to be the most supportive: FIGURE 3. Symptoms experienced by patients as a result of NETs, often on a constant or daily basis. Within each subgroup of patients who experienced a particular symptom, the percentage that experienced that symptom on a constant or daily basis is provided. Base: all US respondents (N = 758). Questions: Which of the following symptoms, if any, do you suffer from as a result of your NET? Select all that apply. How frequently do you suffer from each of the following symptoms as a result of your NET? © 2017 Wolters Kluwer Health, Inc. All rights reserved. www.pancreasjournal.com 643 Wolin et al Pancreas Volume 46, Number 5, May/June 2017 FIGURE 4. Negative impact of NETs on patients' daily lives (A) and work life (B). A, Base: all US respondents (N = 758). Question: How much has each of the following areas of your life been negatively affected, if at all, by your NET? Top 2 responses shown (a moderate amount/a lot). B, *Accommodations include flexible work schedule, work from home, adaptive devices, opportunities for rest, etc. Base: US respondents who are working full time/part time or self-employed (n = 316). Question: Has your NET impacted you at work in any of the following ways? Please select all that apply. 81% (225/278) of surgeons, 79% (162/204) of nurses, and 77% Patients believed that better access to NET-specific treatments (509/659) of oncologists/hematologists were viewed as extremely/ and doctors would be beneficial in their NET care and help them very supportive. However, only 57% (228/400) of patients viewed to live better with NETs (Fig. 5B). Access to NET-specific medi- general practitioners/primary care physicians as extremely/very cal treatments (385/758; 51%) and NET medical teams (344/758; understanding, whereas 70% (278/400) viewed them as extremely/ 45%) were the most common responses by patients. Patients also very supportive. reported wanting a better understanding of steps that could be taken to help manage disease-related (336/758; 44%) or treatment- The most frequently desired improvements for ongoing NET related symptoms (304/758; 40%) and more awareness of the management were a wider range of treatment options (518/758; condition in general (318/758; 42%). Patients who visited NET 68%), better access to NET experts (471/758; 62%), and more specialist centers felt they did not need as many improvements treatments available “in my country that I see in other countries” to NET care as nonvisitors. (453/758; 60%) (Fig. 5A). Significant differences were observed between specialist center visitors and nonvisitors. Patients who DISCUSSION were diagnosed less than 5 years ago were more likely to want more information about participating in NET clinical trials than those di- The use of social media and other online sources allowed the agnosed 5 or more years ago (54% [235/438] vs 46% [147/320]). recruitment of a large number of patients for this survey, despite 644 www.pancreasjournal.com © 2017 Wolters Kluwer Health, Inc. All rights reserved. Pancreas Volume 46, Number 5, May/June 2017 US Patient-Reported Experience of NETs TABLE 2. Tests Received for Ongoing NET Management Patients Who Receive Each Test for Ongoing NET Management, % Patients Visiting Specialist Patients Not Visiting Specialist All Patients Centers at Least Once/Year Centers at Least Once/Year (N = 758) (n = 403) (n = 355) Imaging or enhanced imaging* 94 97 91 CgA 79 84 73 Urinary 5-HIAA 72 74 68 Other blood tests (eg, fasting serum glucose, 67 75 59 fasting gastrin, glucagon, VIP, somatostatin) Endoscopic procedures (eg, gastroscopy, 62 64 59 colonoscopy, capsule endoscopy) Serum 5-HIAA 38 42 34 I am not sure what tests I had 1 1 1 Other/none of the above 10 11 10 Base: all US respondents (N = 758). Question: Which of the following tests, if any, have you received for the ongoing management of your NET? *CT, MRI, PET, SRS (Octreoscan, PET/CTwith Ga, F-DOPA scan, FDG PET/CT, MIBG scan). †P <0.05. 5-HIAA indicates 5-hydroxyindoleacetic acid; CgA, chromogranin A; CT, computed tomography; MRI, magnetic resonance imaging; PET, positron emission tomography; SRS, somatostatin receptor scintigraphy; VIP, vasoactive intestinal peptide. the fact that NETs are a rare disease. Findings from this survey of US incidence, the average time to NET diagnosis reported by a patients with NETs in the United States provide valuable informa- third of patients in this survey was more than 5 years, with more tion on the experience of NETs from a patient perspective. There than half of the patients having metastatic disease at the time of di- is a paucity of relevant disease-specific quantitative data regarding agnosis. This highlights the need for further improvements in this the NET patient experience and QOL. Although this NET pa- area. Multidisciplinary teams within an institution may create a tient survey is not a validated survey of HRQOL, reporting more streamlined procedure and allow a consensus on NET diag- patient-centered data, in addition to targeting improvements in nosis to be reached earlier. As this survey showed, patients primary care and patient experience, is beneficial to health care attended doctor appointments on approximately 13 occasions systems, and these data are becoming increasingly important and were seen by a mean of 6 different health care professionals endpoints in oncology clinical trials. (including all doctors, specialists, and nurses) before receiving A delay in NET diagnosis increases the probability of meta- their diagnosis. Effective multidisciplinary teams at specialist 10 1 static disease, which is associated with poor survival. Early and NET centers offer the best opportunity to improve outcomes for accurate diagnosis of NETs is therefore an essential element in im- patients with NETs. proving patient outcomes. Although the diagnosis of NETs has This survey characterized the significant burden of NETs on improved in recent years, reflected in part by an increase in the patients' lives, with 73% of patients reporting that NETs had at TABLE 3. Availability of NET Treatments Treatments I Have Treatments I Have Treatments I Have Received/Am Heard Of, % (*) Access To, % (†) Currently Receiving, % (‡) †‡ ‡ Surgery 95 82 72 †‡ ‡ Chemotherapy 80 41 22 †‡ ‡ Drug therapy other than chemotherapy 83 58 49 § †‡ ‡ PRRT 78 20 10 †‡ ‡ Interventional radiology 74 39 21 †‡ ‡ Observation 86 61 52 †‡ Other/none of the above 14 75 Superscripted symbols appearing next to a given value indicate significant differences (P < 0.05) between the patient group specified in that column com- pared with those specified in the other columns. Base: all US respondents (N = 758). Question: This is a list of available NET treatments. Please select those you have heard of, those you have access to (meaning they are available to you), and those you have received/are currently receiving for the treatment of your NET. §In the United States, PRRT is only available in clinical trials. PRRT, peptide receptor radionuclide therapy. © 2017 Wolters Kluwer Health, Inc. All rights reserved. www.pancreasjournal.com 645 Wolin et al Pancreas Volume 46, Number 5, May/June 2017 least a moderate negative impact on their life and only 5% from $2547.90 to $8810.40 in the 6 months before and 12 months reporting no negative impact at all. The reduced QOL experienced after the diagnosis, respectively. by patients in this survey is supported by findings from standard- The results from this survey highlight several unmet needs by ized HRQOL testing in previous studies of patients from Europe patients, including better access to NET-specific medical treat- 11–13 and the United States. This disease-specific survey further ments and specialist NET centers, as well as access to a NET med- elucidated this multidimensional concept of QOL, representing ical team. The diagnosis, management, and treatment of NETs is perceptions of health and well-being and how patients coped with highly specialized, and health care professionals at a single institu- their disease, demonstrating that several lifestyle changes were re- tion will generally encounter a limited number of NET patients, quired, including making dietary changes and stopping or cutting making it difficult to maintain this specialized expertise. NET spe- back on physical activities. Patients also reported a negative im- cialist centers have been proposed to facilitate the diagnostic pro- 5,9 pact on their work life, with many forced to reduce working hours, cess and reduce the burden on patients and health care systems. stop working altogether for a time, or retire early. This adds to the Overall, 53% of patients visited a NET specialist center at least already considerable financial burden associated with surgical or once a year, which were located a median of 50 miles from a pa- medical therapy for NET management. A retrospective study re- tient's residence, compared with 20 miles for nonspecialist cen- ported that monthly total health care costs of NET patients in the ters. Many patients believed that access to NET specialist United States who were treated with medical therapy increased facilities and NET experts would be beneficial, and patients who from $5629.70 in the 6 months preceding the diagnosis to visited NET centers felt that they received better care, which $9093.30 in the 12 months following (an increase of more than was reflected in the proportions of patients receiving specialized 60%). For those receiving surgical therapy, the costs increased imaging and biochemical testing for NETs at these centers. Other FIGURE 5. Desired improvements in NET patient care. A, Bold numbers indicate statistical significance between patients visiting specialist centers versus those who do not. Base: All US respondents (N = 758). Question: Which of the following would help with the ongoing management of your NET? B, Bold numbers indicate statistical significance between patients visiting specialist centers versus those who do not. Base: all US respondents (N = 758). Question: Which of the following, if any, would help you living with a NET? 646 www.pancreasjournal.com © 2017 Wolters Kluwer Health, Inc. All rights reserved. Pancreas Volume 46, Number 5, May/June 2017 US Patient-Reported Experience of NETs unmet needs identified by patients in this large survey were REFERENCES improving management of NETs, including education on disease 1. Yao JC, Hassan M, Phan A, et al. One hundred years after "carcinoid": and treatment-related symptom management, and improving epidemiology of and prognostic factors for neuroendocrine tumors in awareness of the condition to assist in communicating with others. 35,825 cases in the United States. JClin Oncol. 2008;26:3063–3072. Although the results from this survey are informative, it is 2. Vinik AI, Woltering EA, Warner RR, et al. NANETS consensus guidelines important to note that the survey itself has several limitations. for the diagnosis of neuroendocrine tumor. Pancreas. 2010;39:713–734. First, it did not use standardized and validated assessments of 3. Boudreaux JP, Klimstra DS, Hassan MM, et al. The NANETS consensus HRQOL. In addition, biased results could have been reported be- guideline for the diagnosis and management of neuroendocrine tumors: cause recruitment for this survey was primarily online (Web sites, well-differentiated neuroendocrine tumors of the jejunum, ileum, appendix, 41%; social media, 32%) or through patient advocacy groups (20%), and cecum. Pancreas. 2010;39:753–766. and a long time had passed since the initial NET diagnosis was made 4. Metz DC, Choi J, Strosberg J, et al. A rationale for multidisciplinary care in (42% were diagnosed ≥5 years ago). The sociodemographics of treating neuroendocrine tumours. Curr Opin Endocrinol Diabetes Obes. the patients recruited were not fully representative of a heteroge- 2012;19:306–313. neous NET population because respondents were more likely to 5. Modlin IM, Moss SF, Chung DC, et al. Priorities for improving the be women (72% of respondents). Recruitment through advocacy management of gastroenteropancreatic neuroendocrine tumors. JNatl groups might have enrolled more highly engaged, motivated care Cancer Inst. 2008;100:1282–1289. seekers who may have had a poorer prognosis. Moreover, details regarding experience at the time of diagnosis are more likely to 6. Chuang CC, Bhurke S, Chen SY, et al. Clinical characteristics, treatment be inaccurately recalled by those patients who had been diagnosed patterns, and economic burden in patients treated for neuroendocrine tumors in the United States: a retrospective cohort study. J Med Econ.2015; several years before participating in the survey. Nevertheless, the results from this survey are informative and 18:126–136. reflect the patient perspective. Validated patient-reported out- 7. Strosberg J, Casciano R, Stern L, et al. United States-based practice patterns comes are becoming more prevalent endpoints in clinical studies and resource utilization in advanced neuroendocrine tumor treatment. because it is important to gain a true understanding of how pa- World J Gastroenterol. 2013;19:2348–2354. tients experience their disease. Taken together, clinical outcomes 8. Griffiths J, Willard C, Burgess A, et al. Meeting the ongoing needs of and patient perspectives will aid in continuing to improve patient survivors of rarer cancer. Eur J Oncol Nurs. 2007;11:434–441. care and disease management. Although patient-reported surveys 9. Feinberg Y, Law C, Singh S, et al. Patient experiences of having a can be used to identify areas that require improvement as well as neuroendocrine tumour: a qualitative study. Eur J Oncol Nurs. 2013;17: areas for further research, changes must be implemented by health 541–545. care professionals for progress to be made. 10. Modlin IM, Oberg K, Chung DC, et al. Gastroenteropancreatic This survey demonstrates the significant burden of NETs on neuroendocrine tumours. Lancet Oncol.2008;9:61–72. patients' lives and has identified key areas for advancement in the 11. Fröjd C, Larsson G, Lampic C, et al. Health related quality of life and diagnosis and long-term management of NETs. The use of NET psychosocial function among patients with carcinoid tumours. A specialist centers and health care professionals who specialize in longitudinal, prospective, and comparative study. Health Qual Life NETs have been highlighted as areas in which patients would like Outcomes.2007;5:18. to see further development in the future. Access to NET specialist facilities should lead to faster diagnoses and better management of 12. Haugland T, Vatn MH, Veenstra M, et al. Health related quality of life in patients with neuroendocrine tumors compared with the general Norwegian NETs, which in turn should help to reduce the burden on both pa- population. Qual Life Res. 2009;18:719–726. tients and health care systems. 13. Beaumont JL, Cella D, Phan AT, et al. Comparison of health-related quality of life in patients with neuroendocrine tumors with quality of life in the general US population. Pancreas. 2012;41:461–466. ACKNOWLEDGMENTS 14. Chau I, Casciano R, Willet J, et al. Quality of life, resource The authors thank the patients who participated in this sur- utilisation and health economics assessment in advanced neuroendocrine vey and their patient advocacy partners in the United States tumours: a systematic review. Eur J Cancer Care (Engl).2013;22: who contributed to this project, The Carcinoid Cancer Foundation 714–725. and NET Research Foundation. Hall & Partners, a research 15. Singh S, Granberg D, Wolin E, et al. Patient-reported burden of a organization, fielded the survey and analyzed the results. neuroendocrine tumor (NET) diagnosis: results from the first global This survey was funded by Novartis Pharmaceuticals Corpo- survey of patients with NETs. JGlobal Oncol. 2017;1:43–53. ration and conducted as an equal collaboration between the Inter- national Neuroendocrine Cancer Alliance (INCA) and Novartis. 16. Browne K, Roseman D, Shaller D, et al. Analysis & commentary. Medical editorial writing assistance was provided by ApotheCom Measuring patient experience as a strategy for improving primary care. (Yardley, Pa) and funded by Novartis. Health Aff (Millwood). 2010;29:921–925. © 2017 Wolters Kluwer Health, Inc. All rights reserved. www.pancreasjournal.com 647 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Pancreas Pubmed Central

Patient-Reported Experience of Diagnosis, Management, and Burden of Neuroendocrine Tumors

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Pubmed Central
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Copyright © 2017 The Author(s). Published by Wolters Kluwer Health, Inc.
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0885-3177
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10.1097/MPA.0000000000000818
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Abstract

ORIGINAL ARTICLE Patient-Reported Experience of Diagnosis, Management, and Burden of Neuroendocrine Tumors Results From a Large Patient Survey in the United States Edward M. Wolin, MD,* John Leyden, MD,† Grace Goldstein, MA,‡ Teodora Kolarova, MA,§ Ron Hollander, MS,|| and Richard R.P. Warner, MD¶ (Pancreas 2017;46: 639–647) Objectives: The aim of this survey was to examine the experience of pa- tients with neuroendocrine tumors (NETs) to raise awareness of the NET- related burden and identify unmet needs. Here, we report data from patients in the United States. euroendocrine tumors (NETs) are a diverse group of malig- Methods: Patients with NETs participated in a 25-minute anonymous N nancies that originate in neuroendocrine cells throughout survey, conducted primarily online from February to May 2014. Survey the body, including the gastrointestinal tract, pancreas, and questions captured information on sociodemographics, clinical characteris- 1 lungs. Neuroendocrine tumors are rare, although incidence rates tics, NET diagnostic experience, disease impact/management, interaction have risen substantially in the United States (partly in response to with medical teams, and NETs knowledge/awareness. improvements in diagnosis and increased awareness), with an age- Results: Of 1928 patients who participated globally, the largest percent- adjusted incidence of 5.25/100,000 people in 2004. Neuroendo- age was from the United States (39%). Approximately 50% of US patients crine tumors can be clinically symptomatic because of the secretion reported being diagnosed with other conditions before receiving their NET of hormones (termed functional tumors) or silent/nonsecretory tu- diagnosis, which for 34% took 5 years or more. Patients experienced many mors, which are generally symptom free (nonfunctional). Lack symptoms on a daily basis as a result of NETs, which had a substantial neg- of clear symptoms associated with NETs leads to delays in diag- ative impact on their work and daily lives. Numerous improvements were nosis, often until advanced stages of the disease when symptoms suggested by patients, including better access to NET-specific treatments 2,3 become more pronounced. and medical teams/centers and better education for the management of Several types of medical specialists and health care profes- disease-related and treatment-related symptoms. sionals may be involved in the diagnosis and staging of NETs, re- Conclusions: This survey demonstrated the significant burden of NETs quiring patients to undergo potentially repetitive and extensive on patients' lives and identified key areas for improvement in diagnosis and examinations. The wide array of imaging techniques, biochemical long-term management, including better access to NET-specific treatments testing, and expertise that are required to characterize the location and specialist medical teams/centers. and grade of the primary tumor and the extent of metastatic dis- Key Words: burden of illness, neuroendocrine tumors, ease could possibly lead to patients receiving conflicting treatment 4,5 patient-centered care, quality of life, surveys, rare diseases plans and misdiagnoses. A large number of health care re- sources are also required for the long-term management of 6,7 From the *Neuroendocrine Program, Montefiore M-E Center for Cancer Care, NETs, with qualitative studies highlighting the lack of a clear 8,9 Bronx, NY; †The Unicorn Foundation, Mosman, New South Wales, Australia; pathway of care for patients with NETs. Neuroendocrine tumor ‡The Carcinoid Cancer Foundation, Inc., White Plains, NY; §APOZ & Friends, management should be highly individualized based on the burden Sofia, Bulgaria; ||Neuroendocrine Tumor (NET) Research Foundation, Boston, and symptoms associated with the tumor and whether the aim of MA; and ¶Mount Sinai School of Medicine, New York, NY. Received for publication June 21, 2016; accepted December 15, 2016. treatment is to ameliorate symptoms or prevent tumor growth. Address correspondence to: Edward M. Wolin, MD, Neuroendocrine Tumor Difficulty in achieving an accurate diagnosis, limited access to Program, Montefiore M-E Center for Cancer Care, 1521 Jarrett Pl, Bronx, NET-specific treatment centers or information about NETs, and NY 10461 (e‐mail: ewolin@montefiore.org). inadequate support as part of ongoing care have been highlighted This study was supported by Novartis Pharmaceuticals Corporation. 8,9 Edward Wolin: honoraria and consultant/advisor: Novartis, Ipsen, Celgene, and in previous studies as issues. A multidisciplinary approach has Advanced Accelerator Applications; John Leyden: travel/accommodations/ been proposed to streamline the care of patients with NETs, in- expenses: The Unicorn Foundation Australia; Grace Goldstein: COO of volving the collaboration of diverse medical disciplines to optimize The Carcinoid Cancer Foundation, Inc.; reports that the foundation has diagnosis, staging, and management, with the aim of enhancing received grants from Novartis, Ipsen, Advanced Accelerator Applications, and Lexicon Pharmaceuticals; travel/accommodations/expenses: Novartis; clinical outcomes and improving patient satisfaction. Teodora Kolarova: travel/accommodations/expenses and honoraria: The impact of NETs on reducing health-related quality of life Novartis; reports that INCA has received grants from Novartis; Ron 11–13 (HRQOL) has been demonstrated using standardized testing. Hollander: executive director of the Neuroendocrine Tumor Research For the United States, Beaumont et al reported significantly Foundation; Richard Warner: honoraria and consultant: Novartis, Pfizer, and Lexicon Pharmaceuticals; research funding: Lexicon Pharmaceuticals. worse HRQOL outcomes on all subscales of the 36-item Short Supplemental digital contents are available for this article. Direct URL citations Form Health Survey and 29-item Patient-Reported Outcome Mea- appear in the printed text and are provided in the HTML and PDF versions surement Information System in patients with NET compared of this article on the journal’s Web site (www.pancreasjournal.com). with the general population. Furthermore, a qualitative study in Copyright © 2017 The Author(s). Published by Wolters Kluwer Health, Inc. This is an open-access article distributed under the terms of the Creative Canadian patients with NET reported negative physical and psy- Commons Attribution-Non Commercial-No Derivatives License 4.0 chological long-term effects, with many experiencing feelings (CCBY-NC-ND), where it is permissible to download and share the work of anxiety and struggling to cope with the chronic and unpredict- provided it is properly cited. The work cannot be changed in any way or able nature of their disease. A substantial financial burden has used commercially without permission from the journal. DOI: 10.1097/MPA.0000000000000818 also been demonstrated in NET patients in the United States, Pancreas � Volume 46, Number 5, May/June 2017 www.pancreasjournal.com 639 Wolin et al Pancreas Volume 46, Number 5, May/June 2017 particularly in the first year after receipt of the diagnosis and re- The survey was deliberately designed to be self-reporting to gardless of whether the patients received surgery or medical ther- appropriately capture patient opinion. Question categories in- apy. Although NETs have been shown to have a clear impact on cluded (1) initial screening; (2) patient's current status; (3) diagno- patients' lives in North America, the patient perspective is not well sis; (4) QOL; (5) NET management; (6) NET treatment; (7) NET documented, and the use of disease-specific quantitative surveys education; and (8) demographics. The majority of survey ques- may provide further insight into the individual symptoms and con- tions were closed ended (ie, participants were provided options 13,14 cerns associated with NETs. from which to choose). The only exceptions were open-ended The International Neuroendocrine Cancer Alliance (INCA) questions related to the collection of numerical data (eg, age, num- consists of 18 independent charitable organizations and patient ber of visits per year to a NET specialist center, etc.). Patients were groups from 15 countries, and aims to be the global advocate for asked to rate certain parameters; responses included “not at all,” patients with NETs. In collaboration with Novartis Pharmaceuti- “somewhat,”“very,” and “extremely” as graded descriptors, and cals Corporation, INCA conducted the first global patient survey when asked the degree to which they (dis)agreed with a particular to gather data about the experience of patients with NETs. This statement, the descriptors “strongly” and “somewhat” were used. survey was designed to increase knowledge regarding NETs from a patient perspective. The main goals were to increase understand- Data Analyses ing of patient needs and challenges with regard to diagnosis, inter- Data from patients in the United States were analyzed using actions with health care professionals, knowledge and awareness the MERLIN (Merlinco, London, United Kingdom) survey soft- levels of NETs, information sources, and long-term management ware. Subgroup analyses were also performed based on the time of the disease. Results of the global survey have been published since diagnosis (<5 or ≥5 years) and if the patient had visited a elsewhere ; this publication presents data analyzed from patients NET specialist center at least once a year. Responses were summa- in the United States with NETs. Results relevant to diagnosis and rized using descriptive statistics, including percentages, means, and the impact that NETs have on patients' daily lives and the US medians. Statistical significance is shown at a 95% confidence in- health care system are highlighted. terval level (P < 0.05). Some responses are presented as a combina- tion of the top 2 responses (eg, somewhat agree/strongly agree; a moderateamount/alot). MATERIALS AND METHODS RESULTS Study Design and Participants Recruitment of patients was conducted primarily online via Patient-Reported Sociodemographics the use of Web site postings, e-mails, flyers, and social media channels of the INCA member organizations/patient advocacy Participants with NETs from the United States represented groups. The global survey was conducted between February and 39% (758/1928) of the total number of patients in the global sur- May 2014. vey and were the largest number of respondents of any participat- ing country. Patients were broadly distributed across the country, with 49 of 50 states represented (North Dakota was the only excep- Survey Details tion). The largest number of respondents were from California The survey was designed and conducted as an equal collab- (87/758; 11%), followed by Pennsylvania (48/758; 6%), and Texas oration between INCA and Novartis Pharmaceuticals. The survey (48/758; 6%). The average patient age was 57 years, with only domains and key questions were originally developed based on 7% (52/758) of patients younger than 40 years, and the majority discussions at the roundtable INCA meeting in March 2013, held of respondents (546/758; 72%) were women (Table 1). Patients during the time of the 10th annual European Neuroendocrine Tu- were well-educated, with 51% (389/758) of patients having at mor Society conference in Barcelona, Spain. Hall & Partners were least a bachelor's degree. At the time of the survey, 42% commissioned to construct and professionally develop the ques- (316/758) of patients stated that they were employed at least part tions; 14 NET patient health consumer groups within INCA had time (including self-employment), 28% (209/758) stated they direct input into question development, and the final questionnaire were retired, and 20% (154/758) had a self-reported medical dis- was reviewed and edited by all members of INCA and Novartis ability. A considerable number of patients required help with between May and October 2013. For transparency, the Novartis day-to-day activities; 59% (449/758) of patients had a close family logo was clearly displayed on all materials, and patients were no- member or friend who acted as a caregiver. At the time of the sur- tified that the INCA patient group partners or Novartis may use vey, the patients who participated had received their NET diagno- the data for disease awareness purposes. Hall & Partners facili- sis a mean of 5.3 years ago. tated conduction of the survey from February to May 2014 and an- alyzed the results. This anonymous survey was designed to be Patient-Reported Clinical Characteristics predominantly completed online, with an estimated duration to completion of 25 minutes. For patients taking the survey in the The most common site that patients reported for primary United States, the survey was available in English and simplified tumors was the gastrointestinal tract (444/758; 59%), followed by Chinese. The English version of the survey used in the United the lung (112/758; 15%), and pancreas (111/758; 15%). The major- States is included as Supplemental Digital Content 1, http:// ity of patients reported having low-grade NETs: 35% (264/758) links.lww.com/MPA/A587. were grade 1 (low) and 17% (127/758) were grade 2 (intermediate). Sociodemographic information, including sex, age, employ- However, 29% (219/758) of patients reported that their physician ment status, and education level, was collected in addition to did not give their NET a grade, and an additional 11% (82/758) patient-reported clinical characteristics such as type, functional stated that their physician did not give or discuss a grade for their status, and grade of NETs. Furthermore, information on desired NET. Almost half of patients (363/758; 48%) had a functional NET, improvements, the burden of NETs on daily life and work, interac- 33% (248/758) had a nonfunctional or asymptomatic NET, and tions with medical teams, and sources of information on NETs 19% (147/758) said that their physician did not discuss the func- were also captured. tional status of their NETwith them or that they did not remember. 640 www.pancreasjournal.com © 2017 Wolters Kluwer Health, Inc. All rights reserved. Pancreas Volume 46, Number 5, May/June 2017 US Patient-Reported Experience of NETs Delays in the Diagnosis of NETs TABLE 1. Patient Sociodemographics and Clinical Characteristics Few patients (131/758; 17%) suspected that the symptoms they were experiencing could be the result of a cancer. The mean Patients (N = 758) patient-reported time from first symptom onset to clinical diagno- Patient-reported sociodemographics sis was 59 months; 34% (259/758) of patients required 5 years or Age, mean, y 57 more for a NET diagnosis, and at diagnosis 57% (434/758) had Age distribution, % metastatic disease. Patients saw a mean of 5.7 health care profes- <40 y 7 sionals before their NET diagnosis, across a mean of 12.7 doctor 40–49 y 15 visits, and only 9% (69/758) of patients were diagnosed at a NET 50–59 y 33 specialist center. The likelihood of being diagnosed at a NET spe- cialist center has increased in recent years; diagnosis occurred at a 60–69 y 33 NET specialist center in 11% (49/438) of patients diagnosed less ≥70 y 11 than 5 years ago versus only 6% (20/320) of patients diagnosed Sex, female, % 72 5 or more years ago. After initial symptoms and tests, 49% Educational level, % (368/758) of patients were initially diagnosed with another condi- Bachelor degree or higher 51 tion before receiving a NET diagnosis, with the most common other Not completed university education 49 diagnoses received including irritable bowel syndrome (182/368; Work status, % 49%), gastritis or another gastric disorder (169/368; 46%), and anx- Employed iety or a psychosomatic-type condition (97/368; 26%) (Fig. 1). Full-time 31 Twenty-two percent (168/758) of respondents received a NET diag- Part-time 6 nosis as an incidental finding while being tested for another con- Self-employed 5 dition, and this occurrence has increased significantly in recent Retired 28 years, with 27% (117/438) of patients being diagnosed with Medical disability 20 NET in this manner in the last 5 years compared with only 16% Not employed/homemaker/student 10 (51/320) of patients who were diagnosed 5 or more years ago. Patient-reported clinical characteristics NET type, % Patient-Reported Diagnostic Experiences Gastrointestinal 59 In total, 57% (435/758) of patients agreed that they were able Lung 15 to get answers to their questions about NETs. The results for this Pancreas 15 were significantly different for patients diagnosed recently com- Thymus 1 pared with those diagnosed 5 or more years ago, with 61% Other 6 (267/438) of patients diagnosed less than 5 years ago agreeing that Site unknown 6 they were able to get answers to their questions about NETs versus I don't know 2 53% (168/320) of patients diagnosed 5 or more years ago. Fewer Tumor grade, %* than half (338/758; 45%) of patients agreed that they had suffi- 135 cient information about NETs after being diagnosed. Only 39% 217 (293/758) of patients “strongly” agreed that they had received com- 36 prehensive medical care after diagnosis, while 32% (239/758) disagreed or “strongly” disagreed. A statistically significant dif- Unknown/don't remember 43 ference in patient response was observed for the time since diag- Functional status, % nosis subgroup analysis: 71% (313/438) of patients diagnosed Functional 48 less than 5 years ago agreed that they had received comprehensive Nonfunctional 12 medical care after diagnosis, compared with 63% (203/320) of pa- Asymptomatic 21 tients diagnosed 5 or more years ago. However, nearly all patients Unknown/don't remember 19 (702/758; 93%) felt that there was a lot of room for improvement Time since diagnosis, mean, y 5.3 in the process of diagnosing NETs. The most commonly desired Time since diagnosis, % improvements were clearer information on the long-term impact <5 y 58 of NETs (504/758; 66%), increased access to NET specialist health 5–9y 28 care professionals (481/758; 63%), better direction on where to find 10–14 y 8 useful NET information (436/758; 58%), and more knowledge- ≥15 y 6 able health care professionals (436/758; 58%) (Fig. 2). Metastatic disease at time of diagnosis, % 57 Surgical removal of primary tumor since diagnosis, % 72 Burden of NETs on Patients' Lives *Grade 1: Neuroendocrine tumors are relatively slow growing, Ki-67 in- Approximately one third of patients reported poor or fair dex of 2% or less; grade 2: NETs have a less predictable, moderately aggres- overall health (251/758; 33%). A majority of patients reported sive course, Ki-67 index 3% to 20%; grade 3: NETs can be highly symptoms as a result of their NET, which were often experienced aggressive, Ki-67 index greater than 20%. on a constant or daily basis (Fig. 3). Overall, the most com- Functional NETs: produce symptoms caused by the secretions of hor- monly reported symptoms were general fatigue/muscle weakness mones (eg, flushing, diarrhea, wheezing, cramping); nonfunctional NETs: (463/758; 61%), diarrhea (416/758; 55%), abdominal pain/cramping do not secrete hormones, but they may cause symptoms caused by the (359/758; 47%), and skin reactions (eg, flushing) (353/758; tumors' growth (eg, pain, intestinal blockage, bleeding). 47%). Patients experienced a number of other conditions as a re- sult of their NET, including poor or abnormal absorption of nutri- ents (207/758; 27%), vitamin deficiency disease (129/758; 17%), and hyperglycemia (121/758; 16%). © 2017 Wolters Kluwer Health, Inc. All rights reserved. www.pancreasjournal.com 641 Wolin et al Pancreas Volume 46, Number 5, May/June 2017 Neuroendocrine tumors were reported by nearly three quar- 43% (172/403) saw a surgeon and 40% (160/403) of patients saw ters of patients to have had at least a moderate negative impact a gastrointestinal specialist compared with 30% (106/355) and on their lives. Thirty-nine percent (293/758) of patients felt that their 26% (94/355) of nonvisiting patients, respectively. Those patients NET had a large negative impact on their lives, 35% (263/758) stated who reported having nurses (204/758; 27%) and physician assis- that they felt a moderate negative impact, and only 27% (201/758) tants (114/758; 15%) as part of their medical team saw them the of patients felt their NET had little-to-no negative impact on most frequently, at intervals of 1 and 2 months, respectively. their lives. The most commonly reported negative impacts on pa- A total of 750 patients indicated that they had received a tients' lives were overall energy levels (540/758; 71%), finances NET-related test; the vast majority of these patients (511/750; (451/758; 59%), and emotional health (441/758; 58%) (Fig. 4A). 68%) reported having had up to 5 NET-related tests per year. How- Patients reported making several lifestyle changes because of ever, 29% (220/750) of patients reported having tests 6 or more their NET. Just 6% (45/758) felt that they made no lifestyle changes times a year; of these, 16% (118/750) had more than 10. The most as a result of their NET. Dietary changes (487/758; 64%), increased common tests performed on patients with NET were medical im- spending on travel (458/758; 60%), and cutting back on physical aging tests (715/758; 94%) (Table 2). activities (435/758; 57%) were the most commonly reported life- Long distances were traveled by NET patients to see their style changes indicated by patients in the survey. medical team. In total, 22% (168/758) of patients traveled more than Many patients also reported a negative impact on their work 125 miles (200 km) to their medical provider; 23% (173/758) trav- life (Fig. 4B). Only patients who were currently working (316/758; elled 13–31 miles (21–50 km), and 27% (204/758) of patients 42% of respondents) answered questions relating to their work only had to travel up to 12 miles (20 km). The median distance life. Many patients (196/316; 62%) stated that they needed to traveled by all US NET patients in the survey was 30 miles take days off work. Furthermore, 30% (94/316) reported asking (48 km). Patients who visited a specialist center at least once a their employer to make accommodations. Other work impacts year traveled more than twice the distance of nonvisiting patients, commonly conveyed by patients were working reduced hours with a median of 50 miles (80 km) traveled for specialist center (65/316; 21%) and stopping work altogether for a time (51/316; visitors compared with 20 miles (32 km) for nonvisiting patients. 16%). Patients who stated that they were not employed or able to work because of medical disability at the time of the sur- Perceptions of Care and Desired Improvements vey (192/758; 25% of total respondents) were asked if their More than half of patients (391/758; 52%) felt that the overall NET was the reason they had to stop working, to which 79% quality of NET treatments available today were good or very good; (151/192) said yes. Patients who were retired at the time of the sur- however, approximately a third of patients (258/758; 34%) felt that vey (209/758; 28% of respondents) were asked about the previous NET treatments available today were poor or very poor. Patients impact NETs had on their work life. Thirty-one percent (65/209) who visited specialist centers felt significantly more satisfied with stated they had to retire earlier than planned, 14% (29/209) had treatment than nonvisiting patients, with 57% (230/403) of pa- to take days off work, and 11% (22/209) had to stop working alto- tients rating treatment quality as good or very good compared gether for a time, whereas 22% (45/209) said their NET had not with 45% (161/355) of nonvisiting patients. affected their work life. Generally, patients felt that they did not have access to treat- ments of which they had heard. The most common treatments patients Management of NETs had heard of were surgery, chemotherapy, and nonchemotherapy-based In the ongoing management of NETs, patients had an average drug therapies (Table 3). Nearly all (718/758; 95%) patients had of 3 health care professionals who were involved in their NET heard of surgery, 82% (618/758) said they had access to surgery, medical team. The health care professionals most commonly seen and 72% (546/758) said they had received or were receiving sur- by patients were oncologists/hematologists (659/758; 87%), gen- gical treatment. Large differences were observed for chemother- eral practitioners/primary care physicians (400/758; 53%), and sur- apy and nonchemotherapy-based drug therapies in terms of geons (278/758; 37%). Patients who visited a specialist center at treatments patients had heard of and treatments patients had ac- least once a year were more likely to see a wider range of specialists; cess to: 80% (603/758) of patients had heard of chemotherapy, FIGURE 1. Diagnoses received before a NET diagnosis. Only includes conditions mentioned by more than 5% of patients. Base: all US respondents who were diagnosed with other conditions (n = 368). Question: Which of the following conditions were you initially diagnosed with before receiving a NET diagnosis? 642 www.pancreasjournal.com © 2017 Wolters Kluwer Health, Inc. All rights reserved. Pancreas Volume 46, Number 5, May/June 2017 US Patient-Reported Experience of NETs FIGURE 2. Desired improvements to the diagnosis of NETs. Base: all US respondents (N = 758). Question: Which of the following, if any, would have helped you have a better experience with your NET diagnosis? dx, diagnosis; HCPs, health care professionals. but only 41% (310/758) said they had access to chemotherapy, significantly higher than nonvisiting patients (243/355; 68%). and 22% (165/758) were currently receiving or had received che- Overall, 76% (579/758) of patients felt they were very knowledge- motherapy. Although 83% (632/758) of patients had heard of able about treatment options. nonchemotherapy-based drug therapies, only 58% (442/758) said Generally, patients felt that improvements could be made by they had access to and 49% (371/758) said they were currently re- health care professionals in terms of understanding and support. ceiving or had received such therapies. Most patients felt that health care professionals in general were ei- Overall, almost all patients (688/758; 91%) felt that more ther somewhat or not at all understanding (380/758; 50%: 121/ treatment options were needed for the ongoing management of 758; 16%) or supportive (336/758; 44%: 58/758; 8%). Of those NETs. A majority of patients (597/758; 79%) believed that there patients who reported seeing specific health care professionals, is room for improvement in the management of NETs. Eighty- oncologists/hematologists (492/659; 75%), nurses (151/204; three percent (336/403) of patients who visit a NET specialist cen- 74%), and surgeons (192/278; 69%) were felt to be the most ter at least once a year felt that they were very knowledgeable understanding health care professionals. The same health about the treatment options available to them, which was care professionals were considered to be the most supportive: FIGURE 3. Symptoms experienced by patients as a result of NETs, often on a constant or daily basis. Within each subgroup of patients who experienced a particular symptom, the percentage that experienced that symptom on a constant or daily basis is provided. Base: all US respondents (N = 758). Questions: Which of the following symptoms, if any, do you suffer from as a result of your NET? Select all that apply. How frequently do you suffer from each of the following symptoms as a result of your NET? © 2017 Wolters Kluwer Health, Inc. All rights reserved. www.pancreasjournal.com 643 Wolin et al Pancreas Volume 46, Number 5, May/June 2017 FIGURE 4. Negative impact of NETs on patients' daily lives (A) and work life (B). A, Base: all US respondents (N = 758). Question: How much has each of the following areas of your life been negatively affected, if at all, by your NET? Top 2 responses shown (a moderate amount/a lot). B, *Accommodations include flexible work schedule, work from home, adaptive devices, opportunities for rest, etc. Base: US respondents who are working full time/part time or self-employed (n = 316). Question: Has your NET impacted you at work in any of the following ways? Please select all that apply. 81% (225/278) of surgeons, 79% (162/204) of nurses, and 77% Patients believed that better access to NET-specific treatments (509/659) of oncologists/hematologists were viewed as extremely/ and doctors would be beneficial in their NET care and help them very supportive. However, only 57% (228/400) of patients viewed to live better with NETs (Fig. 5B). Access to NET-specific medi- general practitioners/primary care physicians as extremely/very cal treatments (385/758; 51%) and NET medical teams (344/758; understanding, whereas 70% (278/400) viewed them as extremely/ 45%) were the most common responses by patients. Patients also very supportive. reported wanting a better understanding of steps that could be taken to help manage disease-related (336/758; 44%) or treatment- The most frequently desired improvements for ongoing NET related symptoms (304/758; 40%) and more awareness of the management were a wider range of treatment options (518/758; condition in general (318/758; 42%). Patients who visited NET 68%), better access to NET experts (471/758; 62%), and more specialist centers felt they did not need as many improvements treatments available “in my country that I see in other countries” to NET care as nonvisitors. (453/758; 60%) (Fig. 5A). Significant differences were observed between specialist center visitors and nonvisitors. Patients who DISCUSSION were diagnosed less than 5 years ago were more likely to want more information about participating in NET clinical trials than those di- The use of social media and other online sources allowed the agnosed 5 or more years ago (54% [235/438] vs 46% [147/320]). recruitment of a large number of patients for this survey, despite 644 www.pancreasjournal.com © 2017 Wolters Kluwer Health, Inc. All rights reserved. Pancreas Volume 46, Number 5, May/June 2017 US Patient-Reported Experience of NETs TABLE 2. Tests Received for Ongoing NET Management Patients Who Receive Each Test for Ongoing NET Management, % Patients Visiting Specialist Patients Not Visiting Specialist All Patients Centers at Least Once/Year Centers at Least Once/Year (N = 758) (n = 403) (n = 355) Imaging or enhanced imaging* 94 97 91 CgA 79 84 73 Urinary 5-HIAA 72 74 68 Other blood tests (eg, fasting serum glucose, 67 75 59 fasting gastrin, glucagon, VIP, somatostatin) Endoscopic procedures (eg, gastroscopy, 62 64 59 colonoscopy, capsule endoscopy) Serum 5-HIAA 38 42 34 I am not sure what tests I had 1 1 1 Other/none of the above 10 11 10 Base: all US respondents (N = 758). Question: Which of the following tests, if any, have you received for the ongoing management of your NET? *CT, MRI, PET, SRS (Octreoscan, PET/CTwith Ga, F-DOPA scan, FDG PET/CT, MIBG scan). †P <0.05. 5-HIAA indicates 5-hydroxyindoleacetic acid; CgA, chromogranin A; CT, computed tomography; MRI, magnetic resonance imaging; PET, positron emission tomography; SRS, somatostatin receptor scintigraphy; VIP, vasoactive intestinal peptide. the fact that NETs are a rare disease. Findings from this survey of US incidence, the average time to NET diagnosis reported by a patients with NETs in the United States provide valuable informa- third of patients in this survey was more than 5 years, with more tion on the experience of NETs from a patient perspective. There than half of the patients having metastatic disease at the time of di- is a paucity of relevant disease-specific quantitative data regarding agnosis. This highlights the need for further improvements in this the NET patient experience and QOL. Although this NET pa- area. Multidisciplinary teams within an institution may create a tient survey is not a validated survey of HRQOL, reporting more streamlined procedure and allow a consensus on NET diag- patient-centered data, in addition to targeting improvements in nosis to be reached earlier. As this survey showed, patients primary care and patient experience, is beneficial to health care attended doctor appointments on approximately 13 occasions systems, and these data are becoming increasingly important and were seen by a mean of 6 different health care professionals endpoints in oncology clinical trials. (including all doctors, specialists, and nurses) before receiving A delay in NET diagnosis increases the probability of meta- their diagnosis. Effective multidisciplinary teams at specialist 10 1 static disease, which is associated with poor survival. Early and NET centers offer the best opportunity to improve outcomes for accurate diagnosis of NETs is therefore an essential element in im- patients with NETs. proving patient outcomes. Although the diagnosis of NETs has This survey characterized the significant burden of NETs on improved in recent years, reflected in part by an increase in the patients' lives, with 73% of patients reporting that NETs had at TABLE 3. Availability of NET Treatments Treatments I Have Treatments I Have Treatments I Have Received/Am Heard Of, % (*) Access To, % (†) Currently Receiving, % (‡) †‡ ‡ Surgery 95 82 72 †‡ ‡ Chemotherapy 80 41 22 †‡ ‡ Drug therapy other than chemotherapy 83 58 49 § †‡ ‡ PRRT 78 20 10 †‡ ‡ Interventional radiology 74 39 21 †‡ ‡ Observation 86 61 52 †‡ Other/none of the above 14 75 Superscripted symbols appearing next to a given value indicate significant differences (P < 0.05) between the patient group specified in that column com- pared with those specified in the other columns. Base: all US respondents (N = 758). Question: This is a list of available NET treatments. Please select those you have heard of, those you have access to (meaning they are available to you), and those you have received/are currently receiving for the treatment of your NET. §In the United States, PRRT is only available in clinical trials. PRRT, peptide receptor radionuclide therapy. © 2017 Wolters Kluwer Health, Inc. All rights reserved. www.pancreasjournal.com 645 Wolin et al Pancreas Volume 46, Number 5, May/June 2017 least a moderate negative impact on their life and only 5% from $2547.90 to $8810.40 in the 6 months before and 12 months reporting no negative impact at all. The reduced QOL experienced after the diagnosis, respectively. by patients in this survey is supported by findings from standard- The results from this survey highlight several unmet needs by ized HRQOL testing in previous studies of patients from Europe patients, including better access to NET-specific medical treat- 11–13 and the United States. This disease-specific survey further ments and specialist NET centers, as well as access to a NET med- elucidated this multidimensional concept of QOL, representing ical team. The diagnosis, management, and treatment of NETs is perceptions of health and well-being and how patients coped with highly specialized, and health care professionals at a single institu- their disease, demonstrating that several lifestyle changes were re- tion will generally encounter a limited number of NET patients, quired, including making dietary changes and stopping or cutting making it difficult to maintain this specialized expertise. NET spe- back on physical activities. Patients also reported a negative im- cialist centers have been proposed to facilitate the diagnostic pro- 5,9 pact on their work life, with many forced to reduce working hours, cess and reduce the burden on patients and health care systems. stop working altogether for a time, or retire early. This adds to the Overall, 53% of patients visited a NET specialist center at least already considerable financial burden associated with surgical or once a year, which were located a median of 50 miles from a pa- medical therapy for NET management. A retrospective study re- tient's residence, compared with 20 miles for nonspecialist cen- ported that monthly total health care costs of NET patients in the ters. Many patients believed that access to NET specialist United States who were treated with medical therapy increased facilities and NET experts would be beneficial, and patients who from $5629.70 in the 6 months preceding the diagnosis to visited NET centers felt that they received better care, which $9093.30 in the 12 months following (an increase of more than was reflected in the proportions of patients receiving specialized 60%). For those receiving surgical therapy, the costs increased imaging and biochemical testing for NETs at these centers. Other FIGURE 5. Desired improvements in NET patient care. A, Bold numbers indicate statistical significance between patients visiting specialist centers versus those who do not. Base: All US respondents (N = 758). Question: Which of the following would help with the ongoing management of your NET? B, Bold numbers indicate statistical significance between patients visiting specialist centers versus those who do not. Base: all US respondents (N = 758). Question: Which of the following, if any, would help you living with a NET? 646 www.pancreasjournal.com © 2017 Wolters Kluwer Health, Inc. All rights reserved. Pancreas Volume 46, Number 5, May/June 2017 US Patient-Reported Experience of NETs unmet needs identified by patients in this large survey were REFERENCES improving management of NETs, including education on disease 1. Yao JC, Hassan M, Phan A, et al. 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PancreasPubmed Central

Published: Mar 21, 2017

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