Research Methods for Health Sciences 2

206 April 2015 • Volume 19, Number 2 • Clinical Journal of Oncology Nursing

Carol L. Goldstein, PhD, RN, Ellen P. Susman, PhD, Suzy Lockwood, PhD, RN, OCN®, FAAN, Erin E. Medlin, MD, and Kian Behbakht, MD

Background: Awareness of ovarian cancer among women and healthcare providers is under- studied. An early awareness of ovarian cancer may lead to early detection and treatment of ovarian cancer. Objectives: The purpose of this study was to determine the level of that awareness among a sample of women and providers. Methods: Written surveys were developed by the authors based on available literature and were administered to women (n = 857) and healthcare providers (n = 188) attending or vol-

unteering at a community health fair. Chi-square tests for independence and z tests were used for analysis. Findings: Healthcare providers were significantly more likely to identify the symptoms and risk factors for ovarian cancer. Forty percent of women reported being at least slightly familiar with the symptoms of ovarian cancer. Women who were familiar with symptoms were significantly more likely to identify symptoms and risk factors correctly and to report symptoms immediately to a provider. Identification of symptoms among healthcare providers ranged from 59%–93%. Identification of ovarian cancer symptoms and risk factors is poor among women, and knowledge deficits are present in providers. Increasing familiarity and awareness could lead to improvements in early diagnosis.

Carol L. Goldstein, PhD, RN, is an affiliate nursing faculty in the Loretto Heights School of Nursing at Regis University in Denver, CO; Ellen P. Susman, PhD, is a professor emeritus in the Department of Psychology at the Metropolitan State University of Denver in Colorado; Suzy Lockwood, PhD, RN, OCN®, FAAN, is a director of the Division of Undergraduate Nursing Studies and a professor in the Harris College of Nursing and Health Sciences, both at Texas Christian University in Fort Worth; Erin E. Medlin, MD, is a clinical instructor in the University of Wisconsin Hospital and Clinics in Madison; and Kian Behbakht, MD, is a professor in the School of Medicine at the University of Colorado Denver Anschutz Medical Campus in Aurora. The authors take full responsibility for the content of the article. This study was supported, in part, by the Colorado Ovarian Cancer Alliance. The content of this article has been reviewed by independent peer reviewers to ensure that it is balanced, objective, and free from commercial bias. No financial relationships relevant to the content of this article have been disclosed by the independent peer reviewers or editorial staff. Medlin can be reached at [email protected], with copy to editor at [email protected]. (Submitted May 2014. Revision submitted July 2014. Accepted for publication July 27, 2014.)

Key words: ovarian cancer; awareness; symptoms; gynecology; oncology

Digital Object Identifier: 10.1188/15.CJON.206-212

n Article

Awareness of Symptoms and Risk Factors of Ovarian Cancer in a Population of Women and Healthcare Providers

© Raycat/iStock

O varian cancer is responsible for more deaths per year than all other gynecologic cancers combined. The American Cancer Society (2015) estimated that 21,290 women will be diagnosed with ovarian cancer, and 14,180 women are expected to die from

ovarian cancer in 2015. In the United States, the average five-year survival rate is 35% when diagnosed at stage IIIC, which accounts for 75% of initial diagnoses (American Cancer Society, 2015). Women diagnosed at an early stage have a higher five-year survival rate; however, no accepted, reliable screening test exists, and only

15% of women with ovarian cancer are diagnosed at an early stage (Gajjar, Ogden, Mujahid, & Razvi, 2012; Jayde & Boughton, 2012).

Ovarian cancer has an insidious onset, and signs and symp- toms are vague and nonspecific. Symptoms include bloating, pelvic or abdominal pain, frequent urination, and early satiation or difficulty eating (Goff, Mandel, Melancon, & Muntz, 2004). Women associate these symptoms with a variety of every- day conditions and often do not seek medical care (Cooper, Polonec, Stewart, & Gelb, 2013). This results in the delay of diagnosis, and most patients present with advanced disease (Luce,

Clinical Journal of Oncology Nursing • Volume 19, Number 2 • Ovarian Cancer Symptom and Risk Factor Awareness 207

Dow, & Holcomb, 2003). Most women recall having symptoms before diagnosis (Goff et al., 2004). Women have reported be- ing prescribed medication for abdominal discomfort without thorough investigation of all complaints after consulting their healthcare providers (Goff, Mandel, Muntz, & Melancon, 2000; Goff et al., 2004).

Numerous national ovarian cancer organizations note in their mission statements that raising awareness is essential. However, few studies have been completed on the level of awareness among women. Those that have been conducted have shown that women in the general population are not aware of, or have low awareness of, the symptoms of ovarian cancer ( Jayde & Boughton, 2012; Jones et al., 2010; Koldjeski, Kirkpatrick, Ever- ett, Brown, & Swanson, 2004; Lockwood-Rayermann, Donovan, Rambo, & Kuo, 2009). Evidence exists that many primary care providers do not follow up with patients who complain of these symptoms (Evans, Ziebland, & McPherson, 2007; Jayde & Bough- ton, 2012; Koldjeski et al., 2004; Seibaek, Petersen, Blaakaer, & Hounsgaard, 2011). Therefore, the importance of raising awareness and increasing knowledge of these symptoms among women and primary care providers cannot be overstated.

The primary purpose of this study was to establish and com- pare the current level of awareness of ovarian cancer symptoms and risk factors among a population of women seeking healthcare screening and healthcare providers. The authors hypothesized that, despite numerous efforts, women and healthcare providers continue to have knowledge deficits about the signs and symp- toms of ovarian cancer.

Methods Survey Development

Surveys were developed for women and healthcare providers. A survey was developed by the authors based on available literature related to ovarian cancer (Goff et al., 2004; Lockwood-Rayermann et al., 2009). The surveys were piloted among healthcare provid- ers and patients at the study institution, but they were not vali- dated. Questions regarding symptoms of ovarian cancer required a response of “yes” or “no” about whether the respondent thought it was a symptom of ovarian cancer; a “don’t know” response was permitted. All “don’t know” responses were included in the “no” responses. Missing data were excluded. Three incorrect symp- toms were added to examine possible response bias. Surveys were administered in English and Spanish. Spanish interpretation was provided by a certified Spanish interpreter. The survey for health- care providers was similar to the one distributed to women and contained questions regarding their knowledge about the symp- toms and risk factors for ovarian cancer. General demographic information was collected from all participants.

Recruitment

The 9Health Fair, a not-for-profit organization in Colorado, performs free health screenings annually. These events take place at more than 140 sites in rural and urban areas, with an average of 87,000 attendees and 14,000 volunteers. About one-half of the volunteers are healthcare professionals. Of those seeking screening in 2013, about 59% were women (C. Belz, personal communication, January 24, 2013). Eleven sites were selected

based on projected high attendance and a representative sample of counties across Colorado. The first 200 women and all health- care providers presenting at each selected site were personally approached by volunteers from the 9Health Fair and asked to participate in a study about cancer. Respondents were asked to return completed surveys to a designated collection box located at the entrance of the health fair. In addition, three additional healthcare clinics’ providers affiliated with the sponsoring insti- tution were surveyed. This was done to more accurately sample healthcare providers across primary health care disciplines. The 9Health Fair Medical Advisory Board and the institutional review board at the University of Colorado approved the study. Informed consent was implied based on participation.

Statistical Analysis

The data were analyzed using SPSS®, version 21. Chi-square tests for independence were performed on speed of report- ing symptoms by the presence or absence of having a regular healthcare provider. Z tests were performed for comparisons of women’s awareness of symptoms to healthcare providers’ knowledge and for the comparison of women’s knowledge of risk factors in those familiar with symptoms compared to those who were not. Ninety-five percent confidence intervals

TABLE 1. Women and Healthcare Provider Participant Demographics (N = 1,045)

Healthcare Providers (n = 188)

Women (n = 857)

Characteristic n % n %

Age (years) Younger than 40 60 32 145 17 40–59 44 23 417 49 50–59 48 26 – – 60 and older 31 16 261 30 Missing data 5 3 34 4

Race Caucasian – – 649 76 Latino or Hispanic – – 121 14 African American – – 18 2 Other – – 26 3 Missing data – – 43 5

Education High school or less – – 128 15 College or postgraduate – – 439 51 Some college – – 234 27 Missing data – – 56 7

Familiarity with ovarian cancer Knew someone – – 309 36 Did not know someone – – 518 60 Missing data – – 30 4

Specialty Family practitioner 40 21 – – Nurse or nurse practitioner 86 46 – – Obstetrician or gynecologist 6 3 – – Other 46 24 – – Missing data 10 5 – –

Note. Because of rounding, not all percentages total 100.

208 April 2015 • Volume 19, Number 2 • Clinical Journal of Oncology Nursing

were computed for each difference between the women’s and healthcare providers’ proportions. Significance was determined by a two-sided alpha level of 0.05. A power analysis was not performed because of the exploratory nature of this study.

Results Demographics

In all, 857 women completed the survey. However, two ques- tions were inadvertently omitted on 256 surveys. Therefore, the results for these two questions are reported for 601 women. Based on attendance, about 2,200 women received the survey with a response rate of about 39%. Survey distribution was initi- ated on April 6, 2013, and completed on June 15, 2013.

The women’s demographic information is presented in Table 1. Most women were aged 40–59 years (49%), self-identified as Caucasian and non-Hispanic (76%), and were college educated (51%). Thirty-six percent of respondents said they knew some- one with ovarian cancer, and 1% reported being diagnosed with ovarian cancer.

A total of 252 healthcare providers were given the survey, and 188 completed it. Forty respondents self-identified as family practice physicians, 52 as nurses, 34 as nurse practitioners, and

6 as obstetricians or gynecologists. The largest group (32%) of healthcare providers was younger than age 40 years.

Comparison of Awareness of Symptoms and Risk Factors

The ability to recognize the signs and symptoms of ovarian cancer for healthcare providers and women is presented in Table 2. For each symptom presented, healthcare providers were signifi- cantly more knowledgeable than the women. Pelvic or abdominal pain, as well as bloating or abdominal swelling, was recognized as indicative of ovarian cancer more than any other symptoms. No significant difference was found between the two groups for the symptoms of frequent headaches and continuous fever. Healthcare providers were more accurate in indicating that an abnormal Papanicolaou (Pap) test was not a symptom of ovarian cancer compared to the women (p < 0.001).

Identification of risk factors is listed in Table 3. Five of the six factors are known risk factors for ovarian cancer (Engeland, Tretli, & Bjorge, 2003; Heintz et al., 2006; King, Marks, & Mandell, 2003; Lynch, Cavalieri, Lynch, & Casey, 1992; Negri et al., 1991), with the effect of high-dose estrogen without progesterone on ovarian cancer unknown (Beral, Bull, Green, & Reeves, 2007). Personal or family history of ovarian, breast, or colon cancer was identified as a risk factor more than any other

for both groups, with 91% of healthcare providers and 84% of women correctly identifying this risk factor. Healthcare pro- viders were significantly more knowledgeable compared to the women for each risk factor, with the exception of high-dose estrogen.

Women’s Knowledge of Symptoms

A total of 303 (40%) women were at least slightly familiar with the symptoms of ovarian cancer. Women who self-re- ported as familiar with ovarian cancer symptoms were signifi- cantly more accurate with the identification of symptoms for ovarian cancer compared to women unfamiliar with ovari- an cancer symptoms (see Table 4). For the three non-ovarian cancer symptoms, no signifi- cant difference was noted be- tween groups.

Women’s Timeliness of Reporting Symptoms

To ascertain whether famil- iarity with ovarian cancer symp- toms translated into earlier re- porting of suspicious symptoms

TABLE 2. Identification of Symptoms of Ovarian Cancer

HCPs (N = 188)a

Women (N = 857)a

Percent Difference

Two- Sided

pSymptom n % n % 95% CI

Frequent or urgent need to urinate

112 65 194 23 37.6 [29.8, 44.9] < 0.001

Bloating; pelvic or abdominal swelling

170 90 613 72 18.2 [12.5, 22.9] < 0.001

Unexplained weight gain or loss

166 88 467 54 33.7 [27.6, 38.8] < 0.001

Difficulty eating or feeling full quickly

116 62 275 32 31.1 [23.2, 38.4] < 0.001

Vague or persistent stomach discomfort such as gas, nausea, or indigestion

149 79 442 52 28 [20.8, 34.1] < 0.001

Unexplained changes in bowel habits

135 72 350 41 31.4 [23.8, 38.1] < 0.001

Ongoing unusual tiredness 150 80 403 47 32.7 [25.6, 38.7] < 0.001

Pelvic or abdominal pain 117 62 429b 71b 22.7 [17.3, 32.2] < 0.001

Frequent headachesc 25 13 124 14 –1.1 [–5.1, 6.1] 0.704

Continuous feverc 54 29 182 21 7 [0, 14.4] 0.041

Abnormal Papanicolaou testc 61 32 490 57 –25.1 [–32.2, 17.3] < 0.001

a Differences in total number occur because of missing data. b This question was unintentionally left off 256 surveys (N = 601). c Not a symptom of ovarian cancer CI—confidence interval; HCP—healthcare provider

Clinical Journal of Oncology Nursing • Volume 19, Number 2 • Ovarian Cancer Symptom and Risk Factor Awareness 209

to a doctor, women reporting each symptom immediately were compared by familiarity level. When women were asked which symptoms they would re- port to their doctor immediately, no difference was found between women who described themselves as familiar and those who were not familiar with ovarian cancer for every symptom, with the exception of pelvic or abdominal pain. For that symptom, the proportion of those who were familiar with ovarian cancer reporting the symptom imme- diately was significantly greater than those who were not familiar (z = 2.55, p = 0.0108).

In the current study, 663 women (81%) reported having a regular health- care provider. The reporting of several symptoms of ovarian cancer was found to be significantly related to the pres- ence or absence of having a healthcare provider. An unexplained weight gain or loss (p = 0.006), difficulty eating or feeling full quickly (p = 0.026), unexplained changes in bowel habits (p = 0.022), continu- ous fever (p = 0.004), and ongoing unusual tiredness (p < 0.001) were more quickly reported for those women who had a regular healthcare provider. No significant associations were noted between speed of reporting and having a regular healthcare provider for all other listed symptoms and tests.

Women’s Knowledge of Risk Factors

Women’s knowledge of ovarian cancer risk factors separated by familiarity with ovarian cancer symptoms is presented in Table 5. Women familiar with symptoms of ovarian cancer were significantly more likely to identify risk factors correctly except for the unknown factor of high-dose estrogen. For both groups, personal or family history of cancer was identified as an ovarian cancer risk factor more often than the other listed factors; 90% of familiar women and 80% of unfamiliar women were able to identify this risk factor.

Discussion This study showed that more than half of the women sampled

were unfamiliar with the symptoms of ovarian cancer. Health- care providers, although more familiar, were unable to identify all symptoms of ovarian cancer or all risk factors correctly. The current study is one of the largest surveys to measure the level of awareness of ovarian cancer symptoms in a sample of women compared to healthcare providers.

The authors found familiarity with the symptoms of ovarian cancer to be low, with only 14% of women reporting being very familiar or familiar with the symptoms. Forty percent of women reported being at least slightly familiar with the symptoms of ovarian cancer. Similar findings have been reported elsewhere (Andersen, Bowen, Yasui, & McTiernan, 2003; Cooper, Polonec, & Gelb, 2011; Lockwood-Rayermann et al., 2009; Robb et al.,

2009). Lockwood-Rayermann et al. (2009) conducted a national mailed survey of women and found the level of awareness of ovarian cancer symptoms to be 15%, which is low considering that 52% of the sample previously had breast cancer and would be expected to have heightened awareness of other potential cancers. Even among an at-risk population, Andersen et al. (2003) reported a low level of awareness (24%) of ovarian cancer symp- toms. Although symptom identification was relatively poor over- all among the women sampled, pelvic discomfort or pain was correctly identified by 70% of women, but gastrointestinal and genitourinary symptoms were poorly identified. In a telephone survey of women in the United Kingdom, Low et al. (2013) found poor recognition of difficulty eating or feeling full as symptoms of ovarian cancer. Pap test abnormalities are frequently wrongly identified as a sign of ovarian cancer, as noted by Jones et al. (2010) and Hawkins, Cooper, Saraiya, Gelb, and Polonec (2011). In the current study, the Pap test was misidentified by 58% of the women.

Although healthcare providers were able to identify symp- toms more accurately than women, knowledge deficits were still found. The inability to finish a meal and early satiety were only identified by 59% and 64%, respectively. Misconceptions about the Pap test persisted within this group as well, with 33% of healthcare providers incorrectly identifying an abnormal Pap test as a symptom of ovarian cancer. Gajjar et al. (2012) previ- ously addressed the general lack of awareness among primary care physicians, showing that physicians poorly identified gas- trointestinal symptoms as alerts to ovarian cancer.

Identification of risk factors was high among healthcare providers, with more than 80% identifying family history and genetic disposition as risk factors. Despite this and the moder- ate knowledge of the symptoms of ovarian cancer, delays in diagnosis occur frequently (Cooper et al., 2013; Evans et al., 2007; Koldjeski et al., 2004; Seibaek et al., 2011).

The population in the current study did not report a significant barrier to care because 81% reported having a regular primary

TABLE 3. Identification of Risk Factors for Ovarian Cancer

HCPs (N = 188)a

Women (N = 857)a

Percent Difference

Two- Sided

pRisk Factor n % n % 95% CI

Personal or family history of ovarian, breast, or colon cancer

170 90 707 82 7 [1.9, 11.7] 0.011

Genetic predisposition 156 83 628 73 10 [3.5, 15.4] 0.004

Increasing age 132 70 368 43 27 [19.5, 34.1] < 0.001

Use of high-dose estrogen without progesteroneb

92 49 380 44 5 [–3.2, 12.6] 0.25

Obesity 114 61 291 34 27 [18.8, 34] < 0.001

Undesired infertility 78 41 216 25 16 [8.7, 24] < 0.001

a Differences in total number occur because of missing data. b Unknown effect on risk of ovarian cancer CI—confidence interval; HCP—healthcare provider

210 April 2015 • Volume 19, Number 2 • Clinical Journal of Oncology Nursing

care physician. Symptoms are frequently reported to healthcare providers many months before women are diagnosed with ovar- ian cancer, with as many as 93% of women reporting symptoms prior to diagnosis. Therefore, the notion of ovarian cancer as a “silent killer” undervalues the known presence of symptoms. Primary care providers are often the first medical contact point for women with symptoms of ovarian cancer, and they represent an important population in the effort to raise awareness of these symptoms. The current study showed that the presence of a pri- mary care physician improved recognition of symptoms and early reporting of some symptoms.

Strengths and Limitations

Several strengths exist in this study. The relatively large sample size of women and providers from urban and rural settings allows generalization of the results to a broader population. The authors were able to compare healthcare providers’ and women’s level of awareness of the symptoms and risk factors for ovarian cancer within a geographic region, which can help to focus the develop- ment of educational interventions in the future.

Limitations of this study include the use of a convenience sample of individuals presenting to a health fair, which presents a source of response bias. In addition, two questions were in- advertently left off some of the surveys, potentially biasing the responses to those specific questions. Although sample numbers were relatively large, the sample did not accurately represent the geographic area in terms of racial or educational level (U.S. Cen-

sus Bureau, 2015). Overall, more participants in the current study had college and postgraduate degrees than the general population of Colo- rado or the United States (55% versus 36% and 29%, respectively) (U.S. Census Bureau, 2015). Although it may be assumed that this sample of women is more motivated to care for their health, they still had low levels of awareness of the symptoms of ovarian cancer. The sample of healthcare providers was drawn from those participating in the health fair, which may in- dicate a bias to providers who are particularly interested in healthcare screening and preven- tion. The majority of healthcare providers sampled were nurse practitioners and family practitioners, which may not accurately repre- sent the number or types of providers caring for women in the community (Scholle, Chang, Harman, & McNeil, 2002; Scroggs, Griffin, Bayerl, & Schulkin, 1997; Visscher, 1995). The survey tool used in this study was not validated, and its reliability and generalizability needs to be confirmed if it is used again.

Implications for Practice Nurses and advanced nurse practitioners play

a critical role in raising patient awareness of ovarian cancer symptoms. As demonstrated in this study, knowledge deficits regarding symp- toms of ovarian cancer exist among this same group of providers. It is important for nurses at all levels and in all settings to continue to pro- vide patient education of symptoms of ovarian cancer and consistently update and maintain their own knowledge.

Continued effort to educate and empower individuals and groups to endorse policies to

TABLE 4. Women’s Knowledge of Ovarian Cancer Symptoms by Self-Reported Familiarity With Symptoms

Total (N = 759)

Familiar With Symptoms (n = 303)a

Unfamiliar With Symptoms (n = 456)a

Symptom n % n % n % p

Frequent or urgent need to urinate

166 22 87 29 79 17 < 0.001

Bloating; pelvic or abdominal swelling

540 71 262 86 278 61 < 0.001

Unexplained weight gain or loss

413 54 212 70 201 44 < 0.001

Difficulty eating or feeling full quickly

244 32 152 50 92 20 < 0.001

Vague or persistent stomach discomfort such as gas, nausea, or indigestion

387 51 217 72 170 37 < 0.001

Unexplained changes in bowel habits

303 40 155 51 148 32 < 0.001

Ongoing unusual tiredness 363 48 187 62 176 39 < 0.001

Pelvic or abdominal pain 384b 73b 180 59 204 45 < 0.001

Inability to finish a meal ordinarily able to finish

135b 26b 84 28 51 12 < 0.001

Frequent headachesc 110 14 52 17 58 13 0.063

Continuous feverc 160 21 63 21 97 21 0.465

Abnormal Papanicolaou testc 431 57 161 53 270 59 0.119

a Differences in total number occur because of missing data. b N = 528 c Not a symptom of ovarian cancer

Implications for Practice

u Raise patient awareness of the risks of ovarian cancer because patients will then be more inclined to raise health concerns to their providers.

u Educate other healthcare providers to improve deficits in knowledge by incorporating risk factors and symptoms of ovarian cancer in the curriculum.

u Inform patients of symptoms of ovarian cancer using na- tional campaigns that are currently underway.

Clinical Journal of Oncology Nursing • Volume 19, Number 2 • Ovarian Cancer Symptom and Risk Factor Awareness 211

promote awareness are needed. The declaration of September as National Ovarian Cancer Awareness Month in the United States and the designation of a teal ribbon to raise awareness is encouraging. How- ever, to obtain observable impact from the efforts to increase awareness, greater levels of funding, en- ergy, and effort will be required. Additional targeted research in education interventions performed by nurses and physicians has the potential to save lives through early detection and treatment.

Conclusions This study demonstrated the lack of awareness and

knowledge among women about the symptoms of ovarian cancer as well as deficits in awareness among providers. Ovarian cancer is no longer the silent killer it was once thought to be and has repeatedly been shown to cause symptoms prior to diagnosis, even in early stages (Bankhead, Kehoe, & Austoker, 2005; Goff et al., 2004; Wynn, Chang, & Peipins, 2007). Health- care providers must be taught and encouraged to query women at all healthcare encounters about symptoms of ovarian cancer. The incorporation of symptoms into medical school and nursing school curricula has been done, but penetration to older generations is lacking. The Inside Knowledge campaign, an educational campaign developed by the Centers for Disease Control and Prevention, is currently underway for all gynecologic malignancies and is a step in the right direction (Rim, Polonec, Stewart, & Gelb, 2011). The National Ovarian Cancer Coalition and Ovarian Cancer National Alliance (OCNA) provide a wide array of printed and online resources for patients, providers, and the general public that are used to raise awareness. In addition, OCNA sponsors a national program of survivors teaching students that is presented in many medical and nursing schools. However, funding for further de- velopment of interventions for ovarian cancer is uncertain, and greater efforts are needed on the local and national levels.

The authors gratefully acknowledge 9Health Fair for pro- viding access to participants and contributing to participant recruitment, the National Ovarian Cancer Coalition for providing additional information on allocation of funds for ovarian cancer campaigns, the Program of Excellence in Cancers of the Ovary in Colorado for supporting this project with time and faculty involvement, and Suzanne White, MS, for providing guidance for the design of this project.

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