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Perceptions, expectations, and experiences of gynecological cancer patients: a pan-European ESGO-ENGAGe survey
  1. Esra Urkmez1,2,
  2. Elif Andac-Jones3,
  3. David Cibula4,
  4. Denis Querleu5,
  5. Michael J Halaska6,
  6. Daniel Driak6,
  7. Jalid Sehouli7,
  8. Jacek P Grabowski7,
  9. Gulhan Inci7,
  10. Kamil Zalewski8,9,
  11. Lucas Minig10,
  12. Cristina Zorrero11,
  13. Muzaffer Sancı12,
  14. Murat Alan12,
  15. Jonathan A Ledermann13,
  16. Christina Fotopoulou14 and
  17. Murat Gultekin15
  1. 1European Society of Gynecologic Oncology-European Network of Gynecological Cancer Advocacy Groups (ESGO ENGAGE) Chair, Geneva, Switzerland
  2. 2Kanserle Dans, Ankara, Turkey
  3. 3Sociology, Georgetown University, Washington, District of Columbia, USA
  4. 4Gynecologic Oncology Center, General University Hospital in Prague, Praha, Czech Republic
  5. 5Surgery, Institut Bergonie, Bordeaux, France
  6. 63rd Medical Faculty, Charles University, Prague, Czech Republic
  7. 7ChariteCentrum 10 Charité Comprehensive Cancer Center, Berlin, Germany
  8. 8Gynecologic Oncology, Holycross Cancer Center, Kielce, Poland
  9. 9Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology Gliwice, Gliwice, Poland
  10. 10IVO, Gynecology, Valencian Institute of Oncology Foundation, Valencia, Spain
  11. 11CEU Cardenal Herrera University, Moncada, Spain
  12. 12Izmir Tepecik Training and Research Hospital, Izmir, Turkey
  13. 13(NCRI/MRC), UCL Cancer Institute, London, UK
  14. 14Department of Surgery and Cancer, Imperial College London, London, UK
  15. 15Gyne Oncology Division, Hacettepe University, Ankara, Turkey
  1. Correspondence to Dr Murat Gultekin, Hacettepe University Faculty of Medicine, Ankara, Turkey; mrtgultekin{at}yahoo.com

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HIGHLIGHTS

  • The percentage of patients who were aware of the cancer type before their diagnosis was 70.9%.

  • Only 56.5% of patients were aware of Pap smears for diagnosis/prevention of cervical carcinoma, 30.7% of BRCA testing for ovarian cancer, and 6.3% of weight as a risk for endometrial cancer.

  • When considering time to therapy, 68% of patients waited up to 1 month for treatment, 19.2% waited 1–2 months, and 12.7% waited longer than 2 months.

Introduction

Gynecological cancers account for a significant amount of all cancers among women. In 2018, cervical-, uterine-, and ovarian- cancers accounted for 13.7% of all cancers among women worldwide,1 and it is estimated that each year gynecological cancers cause half a million deaths worldwide by an incidence of over a million new cases,2 despite the fact that a significant proportion of gynecological cancers may be preventable.3

Gynecological cancers have a significant impact on the reproductive and sexual health of affected patients.4 5 During the treatment journey, not just medical care, but also adequate supportive care including good communication with healthcare professionals,6 networking with other patients and having access to valuable information in printed and video materials,7 and support by patient advocacy groups,8 all have been shown to contribute in reducing the levels of stress and anxiety experienced by patients.

In an effort to capture the overall perception and needs of gynecological cancer patients, ESGO-Engage carried out a cross-national survey in 10 European countries. Established in 2012 by ESGO- (The European Society of Gynecological Oncology) ENGAGe (Network of Gynecological Cancer Advocacy Groups) is a network of European patient advocacy groups representing all gynecological cancers. The main goal of the research was to establish a baseline of unmet needs, attitudes, and behavioral patterns of gynecological cancer patients during treatment, identify areas of improvement relating to patient-doctor communication aspects but also the overall quality of care, so that we can help better navigate treatment pathways and advocate for patients' needs and access to a more holistic approach in Europe, especially in the area of supportive care: an approach that goes beyond medical care, with elements of psychological and social needs, sexual counseling, access to broad information and resources, including patient support and advocacy organizations, and improving of communication with healthcare professionals. Among firsts in its class in scope and outreach in a wide range of countries in Europe, it aimed to provide an overview of not one specific but all gynecological cancers with an emphasis on patients’ perceptions of quality of care and expectations.

Methods

Data collection took place between August and September of 2017 in 10 European countries comprising the Czech Republic, Denmark, Germany, the UK, Greece, Hungary, Poland, Serbia, Spain, and Turkey, collecting data from 1436 patients by ENGAGe. The country selection was based on the desire to capture the wide range of issues possibly present in vastly different healthcare systems and possible issues across Europe, as well as whether ESGO-ENGAGe had a strong and well established presence to help access respondents and collect reliable data within the aimed time framework. Ethics Committee approval was provided by Izmir Tepecik Training and Research Hospital in Izmir, Turkey. Translated into patients’ respective native languages, the survey was carried out online when possible, and as paper survey in person. A combination of nurses, project coordinators, as well as other ENGAGe organization members handed out the paper surveys to patients at collaborating hospitals. Data entry of collected responses was conducted at the ESGO-ENGAGe office into a web-based database.

There were some limitations to the study: the questionnaire used in the study was not validated, and respondents were not selected by random sampling. However, several steps were implemented to solidify the strength, validity, and reliability of the study overall. The questionnaire was developed by a team of 30 members of the organization. Emphasis was placed on capturing the expertise of gynecological oncologists, patient organizers, survey scientists, and statisticians, and there was a focus to capture the heterogeneous nature of oncological care in Europe, which might vary by infrastructure and cultural differences in different countries. An initial selection of issues deemed important by gynecological cancer survivors were collected by advocacy groups and survivors, then circulated among a group of doctors and scientists for feedback. A final list of issues was sent to a research methods expert to write formal questions for the survey, ensuring the questions were within survey questionnaire guidelines. Written questions were sent to the group of doctors, members of the advocacy organization, and other scientists in the group for feedback and final selection. A professional survey research company was hired to carry out and proof translations of the finalized questionnaire. Translated questionnaires were then circulated among professionals, non-profit organizations, and patients in each respective country of data collection for comments, and updated according to feedback. The questionnaire included a total of 35 questions: 10 demographic and 25 questions on patient awareness of their disease, diagnosis, prevention models, treatment pathways, access to clinical trials, and patient education. At each site of data collection, convenience sampling is used to reach the maximum number of responses within the specified time frame, that is, patients who fit the initial selection criteria were approached and responses from those who agreed to participate were collected. The total number of patients who accessed the survey online was high but not systematically counted. No rejection or official response rate was collected. Once the data collection window iwas closed, all surveys were transferred for data entry.

All results are presented as frequency and rate for categorical variables, compared with the Pearson chi-square test, and ordinal variables with Kendall’s tau b. Nominal two-sided P-values set to P<0.01 significance are reported. All data were analyzed using IBM SPSS Statistics release 25.0.

Results

The country distribution of total respondents was as follows: the Czech Republic=173, Denmark=125, Germany=119, the UK=231, Greece=108, Hungary=123, Poland=110, Serbia=152, Spain=113, and Turkey=182. A total of 622 (43.3%) respondents had ovarian-/fallopian tube cancer, 378 (26.3%) breast cancer, 219 (15.3%) uterine cancer, 185 (12.9%) cervical cancer, and 32 (2.2%) vulvar or vaginal cancer. A total of 739 (51.5%) respondents had completed initial treatment, 535 (37.3%) were currently under treatment for primary tumor, and 162 (11.3%) were in relapse (either under active treatment or in remission for relapsed disease).

A total of 963 (67.1%) respondents were between the ages of 41–65 years, 263 (18.3%) respondents were 66 years or older, 197 (13.7%) respondents were between ages 26–40, and 13 (0.9%) respondents were 25 years or younger. A total of 803 (55.9%) respondents had a college or higher education, 477 (33.2%) were high-school graduates, and 156 (10.9%) were primary school graduates. A total of 471 (32.8%) respondents were considered low-income earners, 540 (37.6%) average-income earners, and 422 (29.4%) high-income earners (based on Organization for Economic Co-operation and Development Net income per country). Of note, three of 1436 respondents chose not to answer the income question.

A total of 1018 patients (70.9%) stated having heard of their cancer type before. The highest ratio of people who had never heard of their particular type of cancer (68.8%) were vulvar and vaginal cancer patients, followed by uterine (29.1%) and ovarian/fallopian tube cancer patients (37.9%). When considering screening, 56.5% of patients indicated they were aware of a cervical smear test for early diagnosis/prevention of cervical carcinoma, yet that number dropped to 42.5% for HPV-/DNA-based cervical cytology, 41.2% for HPV vaccine, 30.7% for BRCA test for ovarian carcinoma, and 6.3% for weight control for endometrial carcinoma. A total of 27.6% of respondents said they had not attended any breast or cervical cancer routine screening programs before their diagnosis. Among the reasons for not complying with screening programs were: not knowing about them (n=194; 13.5%); not having access to them (n=48; 3.3%); not finding them relevant for themselves (n=100; 7%); or financial reasons (n=12; 0.8%).

As it pertained to diagnosis, 46.9% of patients said they were diagnosed as a result of continuous health problems, 30.4% with self-examination, 24.7% at regular check-up/screening, and 4% with routine blood work. As expected, there were significant variations on the diagnosis method by cancer type. The majority of cervical (89.7%) and ovarian/fallopian tube cancer patients (85.6%) were diagnosed by routine check-up and/or checkups after continuing health problems When considering treatment, a total of 977 (68%) patients stated to have waited up to 1 month for their treatment; 276 (19.2%) patients waited 1–2 months; and 183 (12.7%) patients indicated having to wait longer than 2 months. Waiting times were independent of cancer type, and more related to country-specific infrastructures and healthcare systems (Table 1).

Table 1

Treatment wait time by country (P<0.01)

The majority of patients indicated they were confident with their doctor of choice (69.4%), were well-informed about the disease and available treatment options as offered by their doctor and nurses at the hospital (70.9%), that they felt their doctor was empathetic to them and the difficulties they were going through (66.2%), that they were satisfied with the doctor-patient communication (64.1%), that they felt like all their questions and concerns were addressed (60.4%), and that their doctor explained adequately potential early- and long-term side effects of the disease and any related treatment (59.7%). Interestingly, only 48.9% of the patients stated that their doctor discussed with them possible relapse of the disease and symptoms.

Most accessible support seems to be the psychological support (52.8%), with significantly lower levels of: social support (13.6%), including the financial and home care assistance; dietician input (26.3%); sexual counseling (5.1%); access to a rehabilitation programs (12.8%); and palliative care (5.1%). Furthermore, access to information on patient organizations and support groups was at 33.2%. There is significant variation by country across all categories of cancer support services (Table 2). Only 31.1% of patients received any printed information from their healthcare providers. Of those, 91.1% of patients thought that the materials they received was helpful. Denmark (62.4%) and the UK (52.8%) ranked highest in printed information distribution, with Serbia (16.4%), Hungary (13.8%), and Greece (4.6%) ranked last.

Table 2

Level of support by country

Discussion

This survey identified key areas of unmet need in the care of gynecological cancer patients in Europe. We showed a broad variation across European countries in regards to levels of care, with most deficiencies relating to complimentary support, access to palliative care, patient support, and advocacy groups. The level of complimentary support offered to patients remained low in most areas across all 10 countries

Although there are a number of published single country-based surveys, they mostly focus on cancer risk factors,9 one aspect of cancer treatment or patient perspective or behavior.10 A number of published cross-national research focus on a specific type of cancer. Two most recent and comprehensive studies in this area, The ‘Every Woman’ study supported by the World Ovarian Cancer Coalition completed a study in 2018 by surveying 1531 women in 44 countries, and incorporated attitudes and practices in its scope;11 and Expression III: patients’ expectations and preferences regarding the physician–patient relationship and clinical management6 also reports data from 1830 patients in European countries, and both look at only ovarian cancer patients. Therefore, even though they provide an important comparison for ovarian cancer patient data, the scope of this survey extends beyond their focus covering all gynecological cancers. Many other studies conduct meta-analysis of existing publications or reports from centers and organizations.12

There have been significant achievements with this study, such as the extensive collaboration between multiple patient organizations working under the umbrella of ENGAGe and oncologists on site, number of countries covered in the survey, the total number of patients reached, and the breadth of the questionnaire. However, the data was collected in a relatively short amount of time and at a limited number of hospitals. These led to some important limitations including not being able to conduct advanced statistical analyses that are significant at the country level, and less than ideal conditions for the generalizability of the findings. Hospitals and patients included in the study were selected using convenience sampling, and cohort size at each site was not monitored nor standardized at any point. Nevertheless, the authors believe that the study provides very important insights on gynecological patient care and patient expectations, and allow new directions for supportive care in Europe.

Early detection plays a crucial role in the fight against cancer13 and it requires population-based screening programs and greater awareness of the early signs and symptoms of cancer. The findings of our study show that the percentage of the patients diagnosed as a result of routine screening is low (24.7%), confirming an area of unmet need to further encourage women to understand the importance of routine checkups in diagnosing gynecologic cancers.

Longer wait for treatments in cancer patients is known to cause a series of detrimental effects for patients.14 A broadly accepted timeline from diagnosis to treatment as published in the international literature ranges from 30 days to 8 weeks.15 16 Our study indicates that, on average, 12.7% of patients in Europe still have to wait longer than 2 months, and 21%–25% of patients in Poland, Serbia, and Hungary have waiting times exceeding 2 months for treatment, leaving much room for improvement. Longer waiting times exceeding the ideal mark of a month is still observed in around one-third of the patients. Though part of the delay in treatment wait times may be due to issues of co-morbidity and the elderly age of the patients, it may also signal issues in healthcare infrastructure such as lack of adequate supply of healthcare workers, and processing times in radiotherapy centers. Discovering the reasons and addressing the time to treatment disparities are among the first priorities for the future projects of ESGO-Engage discussing these findings with relevant national societies, governmental, and non-governmental organizations during local and global meetings in the near future. These efforts already culminated in a project under the umbrella of the European Cancer Organization with the goal of producing relevant European onco-policies, a European master cancer control program.

Coping with cancer and its treatment is a complicated process requiring the patient and its caregivers to be well educated about multiple aspects and stages of the process.17 18 A small yet crucial medium of increasing patient education is the use of printed materials since patients who receive printed information fare better in their disease management.19 Yet we found that only an average of 31.1% of patients received any printed materials from their healthcare providers. Cancer patients have high levels of unmet needs and prefer receiving more information and support for their disease6 20 21 with a strong preference in being involved in the decision-making process of their treatments.22–24 This can only be efficient by a matching increase in support and educational services.

The levels of support services available to patients show that with the exception of psychological support (52.8%), most others that can help improve the quality of life25 26 remain at critically low levels. Nutrition has been shown to be of paramount importance in oncologic outcomes, whereas extensive surgery in advanced stages often affects gastrointestinal absorption, function, and nutritional patterns, so that dietician input and support is crucially important on a long-term basis to help patients cope not only with their actual cancer diagnosis but also the long-term effects of their treatment.27 Our study demonstrated low numbers of dietary input and support with an average of only 26.3%. Similar low levels of support apply to sexual health. Female cancer patients have been repeatedly shown to ‘receive insufficient counseling, support, or treatment to preserve or regain sexual function after cancer treatment’.28 29 Our study shows sexual counseling being offered to only 5.1% of patients, hence flagging up another area urgently requiring improvement.

In 2014, the World Health Assembly Resolution on Palliative Care called for all countries to develop, strengthen, and implement, where appropriate, palliative care policies.30 For comparison, in the US, one of the pioneers in palliative care, 67 percent of hospitals with 50 or more total facility beds were reported to have a palliative care program.31 The ratio of patients who had access to palliative care in this study remained at a very low 5.1%.

Our interdisciplinary and inter-professionally designed European study is a great example that a collaborative effort of medical professionals with non-profit organizations, administered to all types of gynecological cancer patients in multiple countries can help access a high number of patients in a very limited recruiting time. This approach also allowed us to immediately start a subsequent discussion to translate the findings into the clinical day and to further explore future prospective studies. Findings of this study are already being used in two pilot studies in the Czech Republic and Poland, by making changes in the hospital environment as indicated in the survey results, that would affect patients’ access to palliative care. These 9-month long quasi-experimental pilot projects target to improve the areas of patient care where they scored especially low in the initial survey. In the Czech Republic, the focus is on offering and informing the patients about new onsite psycho-oncology support, as well as sexual counseling. In Poland, the distribution of thousands of informative pamphlets focusing on disease information, nutrition, and palliative care support is underway. In addition, weekly workshops bringing cancer patients with healthcare professionals together with the goal of better listening and learning of each other’s concerns and experiences began operation.

Acknowledgments

The authors thank the cancer patients who took the time to complete the surveys; the nurses and members of the medical teams who assisted in the project; QuintilesIMS for their work in collecting the data, and ENGAGe members in those countries and ESGO Prag team for their support in managing the project.

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Footnotes

  • Collaborators Czech Republic: NF Hippokrates, Prague; Denmark: Kræft i Underlivet (KIU); Germany: Stiftung Eierstock Krebs; Greece: K.E.F.I. of Athens; Hungary: Mallow Flower Foundation; Poland: Blue Butterfly Foundation; Serbia: Women’s Center Milica, Kraljevo Public Health Institute; Spain: ASACO Spain; Turkey: Kanserle Dans Dernegi, UK: Ovarian Cancer Action.

  • Contributors Design, concept, and conduct of the study: EU, MG. Data acqusition, data quality control: MJH, DD,JS, JPG, GI, KZ, CZ, LM, MS, MA, JAL. Data analysis, statistical analysis, and data interpretations: EU, EA-J, MG. Manuscript preparation, editing, and review: EU, EA-J, DC, DQ, CF, MG.

  • Funding Some funding was awarded by Clovis, MSD and AstraZeneca. This funding is used to pay the data collection company, data entry and analysis, printing paper copies of the survey, and shipping expenses to send surveys to ESGO office in Prague.

  • Competing interests None declared.

  • Patient consent for publication Not required.

  • Ethics approval T.C Izmir Valiligi Izmir Il Saglik Mudurlugu, SBU Izmir Tepecik Egitim ve Arastirma Hastanesi, Toplanti no:1, Karar No: 14.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Data availability statement Data are available upon reasonable request.

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