Ovarian Cancer Knowledge Among Advanced Providers in a University Setting

Ovarian Cancer Knowledge Among Advanced Providers in a University Setting

ORIGINAL RESEARCH Ovarian Cancer Knowledge Among Advanced Providers in a University Setting Carol L. Goldstein, PhD, Jeanelle Sheeder, PhD, Erin Medl...

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ORIGINAL RESEARCH

Ovarian Cancer Knowledge Among Advanced Providers in a University Setting Carol L. Goldstein, PhD, Jeanelle Sheeder, PhD, Erin Medlin, MD, Patricia L. Cullen, PhD, CPNP-PC, Daniel Hyman, MD, and Kian Behbakht, MD ABSTRACT

Ovarian cancer is usually diagnosed at a late stage of the disease. Nurse practitioners and physician assistants are often the first contact, and awareness of the signs and symptoms of the disease may improve diagnosis and outcome. A knowledge survey of risk factors and symptoms was distributed to all nurse practitioners and physician assistants at a university health system. Knowledge of signs and symptoms of ovarian cancer in these providers was low. Early satiety, abdominal fullness, and urinary urgency were frequently missed by both groups. Our findings illustrate the need for the development and availability of materials to address knowledge gaps. Keywords: advanced practice providers, nurse practitioner education, ovarian cancer Ó 2016 Elsevier Inc. All rights reserved.

INTRODUCTION

O

varian cancer is the 11th most common cancer in the United States, the fifth leading cause of cancer mortality among women, and the most lethal gynecologic cancer with 14,240 deaths anticipated for 2016.1,2 Poor survival is attributable in part to the late stage of diagnosis and lack of screening modalities.3 Five-year survival for patients diagnosed with late-stage disease is 39%-59%, whereas 5-year survival for early-stage disease is 70%-94%.2 Multiple large trials of ovarian cancer screening that have included ultrasound and cancer antigen 125 (CA125) have not shown a survival benefit.4-7 Although symptoms of ovarian cancer may be vague, Goff et al. were the first to note that recurrent and frequent symptoms of bloating, increased abdominal size, urinary frequency, and early satiety were common in ovarian cancer patients.8 Despite the frequency and recurrence of these symptoms, primary care physicians often do not recommend ovarian cancer testing.9 This is due in part to limited awareness of common signs and symptoms among both women and health care providers.10 In a survey study, knowledge of symptoms among women was shown to be low at www.npjournal.org

15%. Knowledge of symptoms was also low among health care providers, with less than two thirds of them correctly identifying symptoms of ovarian cancer.10 The US is facing a shortage of primary care providers and that is likely to increase in the near future with expansion of insurance coverage.11 In many settings, the role of the primary care provider is increasingly being filled by nurse practitioners (NPs) and physician assistants (PAs).12-15 Although only 1.4 million adults in the US identify an NP or PA as their primary source of care, there are 32 million adult visits to primary care providers annually.16 Indeed, women’s health NPs are playing an increasing role in the care of women as they are employed by 62% of obstetrician/gynecologists, with an anticipated expansion in this role in the next 5 years.17 The American College of Physician’s 2009 Policy Monograph on the role of NPs in primary care calls for a collaborative role of physicians with NPs and/or PAs in the delivery of primary care.18 In spite of the excellent care provided by NPs and PAs, educational gaps do exist.19 As NPs and PAs assume a larger role in primary care, and especially in women’s health care, there is a critical need for adequate The Journal for Nurse Practitioners - JNP

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education for these providers regarding the common signs and symptoms of ovarian cancer and appropriate follow-up actions. Previous studies have shown significant deficits among women and providers in the knowledge of the signs and symptoms of ovarian cancer.20-23 In a previous study, our group surveyed 857 women and 188 providers at a community health fair. Findings were consistent with other studies and demonstrated overall poor awareness and knowledge of signs and symptoms and risk factors for ovarian cancer.10 However, no previous studies have specifically evaluated the level of knowledge and awareness of the signs and symptoms of ovarian cancer among NPs and/or PAs. The primary aim of this study was to determine that level of awareness among these providers. Additional aims were to determine whether there was a knowledge difference between NPs and PAs, to find out what information NPs and PAs received about ovarian cancer in their initial education, and to determine how they continue to receive information on this subject. METHODS

A survey our group used in a previous study addressing awareness of ovarian cancer was modified and piloted in a small group of NPs (n ¼ 6) for validation.10 PAs were not included in the pilot survey due to lack of availability. The responses were reviewed and minor adjustments in the wording were made to further enhance clarity. The survey was distributed to all NPs and PAs (identified as advanced practice providers) at a university medical center in the Rocky Mountain region via an e-mailed link to Survey MonkeyÒ. To expand the sample size, the survey was also linked to members of a secure forum for doctors of nursing practice (DNPs) (http://www .doctorsofnursingpractice.org/), many of whom are NPs. Respondents were included if they identified as being either an NP or PA, regardless of specialty. All subspecialties were included due to varying practice patterns over a provider’s career.24 Non-NP DNPs either did not respond or were excluded from the final analysis. The target participants were initially e-mailed information from the primary investigator about the purpose of the study as well as the link to the survey on e2

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August 13, 2015. Information in that message also included the estimated time to complete the survey (5 minutes) and contact information for the primary investigator. A follow-up e-mail was sent on October 21, 2015. Participants were allowed a total of 12 weeks to respond. Additional repeat correspondence or time was not permitted due to limited evidence of improvement in response rate and, therefore, additional responses were not anticipated.25,26 Consent for participation was inferred by voluntary participation. Respondents could only respond to the survey one time from their account e-mail. The study was reviewed and approved as exempt as per Category 2 by the appropriate institutional review board. Although the survey was anonymous, at the end respondents could request the key to the correct answers for the knowledge-based questions, and the principal investigator provided this material. Statistical Methods

Limited demographic data, including age, profession, and subspecialty, were collected and analyzed with general descriptive statistics. Age was binned to allow for comparison between age groups. Pearson chisquare tests for independence were used to compare NPs to PAs and to determine whether the age of the provider responses associated with knowledge. For dichotomous variables in which cell sizes were < 5, Fisher’s exact test was used. P < .05 was considered statistically significant. All analyses were performed with SPSS Statistics, version 23 (IBM SPSS, Armonk, NY). RESULTS Demographics

A total of 350 surveys were distributed via e-mail to the group of advanced practice providers at the university and all its satellite clinics. An indeterminate number was accessed through the DNP blog. A total of 159 surveys were completed between August 13, 2015 and November 18, 2015. A response rate could not be accurately determined due to the possibility of additional respondents from the DNP blog or from multiple e-mail accounts. However, it was estimated from those distributed via e-mail to the university that the response rate was approximately 45.4%. Of the 159 respondents, 48.4% (n ¼ 77) self-identified as Volume

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NPs, 34.0% (n ¼ 54) identified themselves as PAs, and 17.6% (n ¼ 28) identified themselves as “other.” The participants classifying themselves as “other” were excluded, resulting in a final sample of 131 available for analysis. NPs and PAs were similar with regard to age, with 36.4% of NPs and 46.3% of PAs < 40 years old (P ¼ .25). Areas of practice included family medicine, internal medicine, obstetrics and gynecology, pediatrics, and other. Identification of Symptoms of Ovarian Cancer

The rates of correct identification and correct dismissal of symptoms of ovarian cancer are presented in Table 1. NPs and PAs were similar in their ability to correctly identify which symptoms may (or may

not) lead them to consider a differential diagnosis of ovarian cancer. Overall, participants identified or dismissed 8.1  2.5 (68%) of the 12 symptoms listed correctly. Most respondents correctly identified 2 symptoms commonly associated with ovarian cancer: “bloating; pelvic and/or abdominal swelling” (96.9%) and “pelvic or abdominal pain” (95.3%). However, “difficulty eating or feeling full quickly” (67.7%, missed 32.3%) and “frequent or urgent need to urinate (without UTI)” (38.3%, missed 61.7%) were frequently missed. A majority of participants correctly identified the less-specific symptoms, such as “pelvic or abdominal pain” (95.3%), “unexplained weight loss or weight gain” (88.2%), and “vague or persistent stomach discomfort, such as gas, nausea, or

Table 1. Identification of Possible Symptoms of Ovarian Cancer by Practice and Age Groups Total (N ¼ 131)

PA (n ¼ 54)

NP (n ¼ 77)

P valuea

Age < 40 years (n ¼ 53)

Age  40 years (n ¼ 78)

P valuea

Bloating; Pelvic and/or abdominal swelling or bloating

96.9%

94.2%

98.7%

.16

98.0%

96.1%

.54

Pelvic or abdominal pain

95.3%

94.3%

96.0%

.66

96.2%

94.7%

.71

Frequent or urgent need to urinate (without UTI)

38.3%

34.6%

40.8%

.48

41.2%

36.4%

.58

Difficulty eating or feeling full quickly

67.7%

71.2%

65.3%

.49

74.5%

63.2%

.18

Inability to finish a meal patient would ordinarily be able to finish

61.5%

59.3%

63.2%

.65

62.3%

61.0%

.89

Unexplained weight loss or weight gain

88.2%

90.4%

86.7%

.52

90.2%

86.8%

.57

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

81.1%

82.7%

80.0%

.7

84.3%

78.9%

.45

Unexplained change in bowel habits

74.8%

73.1%

76.0%

.71

70.6%

77.6%

.37

Ongoing unusual tiredness

69.6%

76.9%

64.4%

.13

68.0%

70.7%

.75

Abnormal Pap test

62.0%

57.7%

64.9%

.41

58.8%

64.1%

.55

Frequent headaches

57.9%

52.9%

61.3%

.35

52.0%

61.8%

.27

Continuous fever

44.1%

34.6%

50.7%

.07

52.9%

38.2%

.1

8.1  2.5

7.9  2.7

8.3  2.4

.45

8.1  2.5

8.2  2.6

.87

67.9%

66.2%

69.1%

.45

67.6%

68.2%

.87

Total number correct (of 12) Percent correct

NP ¼ nurse practitioner; PA ¼ physician’s assistant; UTI ¼ urinary tract infection. a Pearson’s chi-square test for independence and Fisher’s exact test were used for statistical analysis.

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Table 2. Identification of Possible Risk Factors of Ovarian Cancer by Practice and Age Groups Total (N ¼ 131)

PA (n ¼ 54)

NPa (n ¼ 77)

Age < 40 Years (n ¼ 53)

Age  40a Years (n ¼ 78)

100.0%

100.0%

100.0%

100.0%

100.0%

Genetic predisposition

96.9%

96.2%

97.4%

96.2%

97.4%

Increasing age

82.2%

88.5%

77.9%

82.7%

81.8%

Being on birth control pills for an extended period of time

60.0%

54.7%

63.6%

56.6%

62.3%

Use of high-dose estrogen without progesterone

25.4%

28.3%

23.4%

20.8%

28.6%

Obesity

69.2%

66.0%

71.4%

75.5%

64.9%

Undesired infertility

33.1%

32.1%

33.8%

39.6%

28.6%

4.7  0.94

4.6  0.86

4.7  1.0

4.6  1.0

4.7  0.82

66.6%

66.3%

66.8%

66.2%

67.1%

Which of the following are risk factors for ovarian cancer? Personal or family history of ovarian, breast or colon cancer

Total number correct (of 7) Percent correct NP ¼ nurse practitioner; PA ¼ physician’s assistant. a

Pearson’s chi-square test for independence and Fisher’s exact test were used for statistical analysis. No significant differences were noted.

indigestion” (81.1%). Regardless of practice group, participants who were < 40 and  40 years old were similar in their ability to the correctly identify symptoms of ovarian cancer.

(age  40) were more likely to order pelvic ultrasound (P ¼ .01), but exhibited a trend toward less referral for genetic testing (P ¼ .06). There were no differences in responses between NPs and PAs.

Identification of Risk Factors for Ovarian Cancer

Sources of Education on Ovarian Cancer

All questions and responses for risk factors are presented in Table 2. NPs and PAs were also similar in their ability to correctly identify risk factors for ovarian cancer. Overall, participants identified 4.7  0.94 of the 7 risk factors listed correctly. Most participants correctly identified “Personal or family history of ovarian, breast or colon cancer” (100%), “genetic predisposition” (96.9%), and “increasing age” (82.2%). Providers commonly missed “undesired infertility” (33.1%). Participants who were < 40 and  40 years old were similar with regard to the correct identification of risk factors.

Data on education and sources of information are presented in Table 4. PAs were more likely than NPs to report having learned about ovarian cancer in their initial formal education (83.0% vs. 65.3%; P ¼ .027). Less than half (42.7%), however, reported that they had received any information on the signs and symptoms of ovarian cancer since completing their education. The most commonly reported sources of obtaining this information were TV ads (100%) and talks by organizations (100%). NPs were more likely than PAs to report obtaining information from articles in professional journals (41.6% vs. 24.1%; P ¼ .038) and continuing education units on the internet (14.3% vs. 1.9%; P ¼ .015). Individuals, regardless of practice group, were more likely to recall having training on ovarian cancer as part of their formal education if they were < 40 years old (84.3% vs. 64.9%; P ¼ .016). However, those  40 were more likely to report that they had received information on the signs and symptoms

Reported Frequency of Ordering Tests by Group

We asked questions regarding the frequency of ordering tests to further evaluate for a possibility of ovarian cancer (CA125 and pelvic ultrasound) and the frequency of ordering genetic testing based on family history or self-reported religious affiliation. Results are listed in Table 3. Older respondents e4

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Table 3. Reported Frequency of Ordering Tests by Group Total (N ¼ 131)

PA (n ¼ 54)

NP (n ¼ 77)

P valuea

Age < 40 Years (n ¼ 53)

Age  40 Years (n ¼ 78)

.26

How often have you ordered a CA125 on a patient without a known diagnosis because you were worried about ovarian cancer?

.38

Never

69.2%

61.1%

75.0%

73.6%

66.2%

1-5

23.8%

29.6%

19.7%

22.6%

24.7%

6-10

3.8%

3.7%

3.9%

3.8%

3.9%

>10

3.1%

5.6%

1.3%

0.0%

5.2%

.37

How often have you ordered an ultrasound on a patient without a known diagnosis because you were worried about ovarian cancer?

P valuea

.01

Never

47.3%

46.3%

48.1%

54.7%

42.3%

1-5

23.7%

29.6%

19.5%

32.1%

17.9%

6-10

12.2%

7.4%

15.6%

3.8%

17.9%

>10

16.8%

16.7%

16.9%

9.4%

21.8%

Never

68.2%

71.2%

66.2%

79.2%

60.5%

1-5

19.4%

19.2%

19.5%

17.0%

21.1%

6-10

6.2%

7.7%

5.2%

1.9%

9.2%

>10

6.2%

1.9%

9.1%

1.9%

9.2%

How often have you ordered genetic testing for cancer susceptibility on a patient based on a family history and/or religious affiliation? .39

.06

CA125 ¼ cancer antigen 125; NP ¼ nurse practitioner; PA ¼ physician’s assistant. a Pearson’s chi-square test for independence and Fisher’s exact test were used for statistical analysis.

of ovarian cancer since completing their education (52.6% vs. 28.3%; P ¼ .006). Individuals < 40 years old were also less likely to say they had received information at conferences (11.3% vs. 33.3%; P ¼ 0.004), in articles in professional journals (20.8% vs. 43.6%; P ¼ .007), and from talks by organizations (7.5% vs. 24.4%; P ¼ .018). DISCUSSION

The lack of available screening for ovarian cancer challenges the care provider to have a heightened awareness and be well informed about the signs and symptoms of this disease. Patients and providers have previously been shown to have low levels of awareness www.npjournal.org

and knowledge of the common signs and symptoms related to ovarian cancer.10 Our study has focused on NPs and PAs and has again shown an awareness and knowledge deficit with regard to ovarian cancer. In addition, continued educational opportunities for this group of providers appear to be lacking. In this study, NPs and PAs had significant deficits in their ability to correctly identify the most common symptoms of ovarian cancer. Although participants were able to correctly identify bloating and pelvic/ abdominal pain > 90% of the time, urinary symptoms and early satiety were often overlooked. Following a survey of women with ovarian cancer, Goff et al. established a symptom index for identifying ovarian The Journal for Nurse Practitioners - JNP

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Table 4. Sources of Education Regarding Ovarian Cancer Total (N ¼ 131)

PA (n ¼ 54)

NP (n ¼ 77)

P valuea

Age < 40 Years (n ¼ 53)

Age  40 Years (n ¼ 78)

P valuea

Do you remember learning about ovarian cancer in your initial NP or PA education?

72.7%

83.0%

65.3%

.027

84.3%

64.9%

.016

Have you received any information about the signs and symptoms of ovarian cancer since completing your education?

42.7%

35.2%

48.1%

.143

28.3%

52.6%

.006

Conferences

24.4%

18.5%

28.6%

.19

11.3%

33.3%

.004

Articles in professional journals

34.4%

24.1%

41.6%

.038

20.8%

43.6%

.007

Articles in the lay press

6.9%

5.6%

7.8%

.62

3.8%

9.0%

.31

Print media (brochures, symptom cards, newspaper, magazines)

3.8%

5.6%

2.6%

.38

3.8%

3.8%

Internet

5.3%

5.6%

5.2%

1.9%

7.7%

100.0%

100.0%

100.0%

100.0%

100.0%

9.2%

1.9%

14.3%

.015

3.8%

12.8%

.12

17.6%

11.1%

22.1%

.1

7.5%

24.4%

.018

100.0%

100.0%

100.0%

100.0%

100.0%

If you have received information about ovarian cancer since completing your training, please indicate the way(s) in which you received this information

Television ads CEUs on the web Talks by health care professionals Talks by organizations (eg, the Colorado Ovarian Cancer Alliance)

1.0

1.0

.24

CEU ¼ continuing education unit; NP ¼ nurse practitioner; PA ¼ physician’s assistant. a Pearson’s chi-square test for independence and Fisher’s exact test were used for statistical analysis.

cancer that included early satiety and urinary symptoms as important symptoms.8 Most women had symptoms before diagnosis, but distinguishing these symptoms from common primary care complaints remains problematic. In the study by Goff et al.,8 95% of women had at least 1 symptom in the previous year and 72% had recurring symptoms. Goff et al. further emphasized the importance of not attributing ovarian cancer symptoms to the aging process and concluded that providers need to be cognizant with regard to when to conduct further diagnostic testing.27 More than a decade later, our study findings show that this problem continues. e6

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Loerzel et al. demonstrated knowledge deficits in NP students and identified a paucity of literature for NPs on early detection strategies.28 In their study, as in ours, the majority of respondents (68%) believed that a Pap test screened for ovarian cancer. Loerzel et al. identified knowledge deficits among NP students who had not completed training. Our study showed continued deficits while NPs were in practice. A foundation for awareness and knowledge of women’s cancers must be set early in training and reinforced at appropriate times. In addition, both NPs and PAs were inconsistent in their ability to correctly identify the most Volume

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important risk factors for ovarian cancer, with similar rates across providers and age groups. Genetic predisposition, personal history, increased age, and infertility are the risk factors for this disease and, although personal history and genetic predisposition were correctly identified by almost all providers, increasing age was not recognized as often and infertility was not recognized. Seiser identified a lack of awareness of risk factors by NPs and, although that study is dated, it suggested NPs educate themselves and their patients about the known risk factors for ovarian cancer and emphasized the importance of taking a complete and thorough family history from all patients.29 As our study and others have highlighted poor awareness of risk factors and thus higher risk individuals for ovarian cancer, continued work in raising awareness of these factors for both providers and patients is warranted to improve early detection. The goal of raising awareness and knowledge about ovarian cancer is to improve early detection and ultimately improve survival. The early diagnosis of ovarian cancer has been elusive. Multiple largescale screening studies for ovarian cancer have failed to show improvements in either early detection or survival, but they have been limited to the use of ultrasound and biologic markers. Ovarian cancer had previously been called a “silent killer.” However, Goff et al. suggested that, in some patients, symptoms may facilitate earlier detection and that women who complain of abdominal/pelvic pain, increased abdominal size/bloating, and/or difficult eating and feeling full quickly (ie, if < 12 months in duration and occurring > 12 times/month) be evaluated for potential ovarian cancer.27 Pelvic ultrasounds and computed tomography imaging may be used to further evaluate patients for ovarian cancer in the presence of these symptoms, although the utility of these tests done at a single time-point has not been demonstrated. In our survey, younger respondents ordered fewer tests but referred more often for genetic testing. This may reflect better knowledge in younger respondents of the controversies in ordering laboratory testing as well as the utility of these tests and a greater awareness of the genetic risks associated with ovarian cancer. www.npjournal.org

Approximately 73% of participants reported receiving education on the signs and symptoms of ovarian cancer as part of their formal education, but only 43% received any education since completion of their degrees. Furthermore, all respondents reported that the postgraduate/continuing education they received about ovarian cancer was from television ads and talks by organizations. Very few reported receiving information from more traditional and reliable sources such as conferences, articles in professional journals, and didactic presentations by health care professionals or continuing education units. This finding illustrates the need for not only more and current information on ovarian cancer but it challenges educators to find ways in which to reach these providers more effectively. As primary care delivery continues to incorporate NPs and PAs as major partners of the care team, they will be tasked with preventive screening as well as early identification of disease.15,28,30 In its landmark report, The Future of Nursing: Leading Change, Advancing Health, the Institute of Medicine (IOM) proposed that nurses be encouraged to practice to the full extent of their education and that they serve as full partners in the redesign and improvement efforts of the health care system.31 When viewing ovarian cancer from an epidemiologic perspective, it is clear that NPs and PAs should be able to function in both primary and secondary spheres.32 Although there is currently no primary prevention modality for this disease, completing a thorough patient history, including a detailed family history, may provide important foundational information that could lead providers to consider patients at risk for developing ovarian cancer. Likewise, improved awareness of the signs and symptoms of ovarian cancer may encourage providers to include ovarian cancer in any differential diagnosis. Strengths and Limitations

There are several strengths to this study. Our study employed a short, easy-to-complete online survey that provided information about the current knowledge base of a relatively large cohort of NPs and PAs in a university setting. As the number of NPs and PAs continues to expand and function in a wide variety of The Journal for Nurse Practitioners - JNP

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settings, continued research on this group of providers is warranted. Finally, providers from a variety of subspecialties were surveyed. NPs and PAs have the flexibility to switch subspecialties, and continued broad-based knowledge of gynecologic cancers is needed. Because NPs and PAs are often the first to see women in primary care settings as well as in specialty clinics, it was important to determine the level of knowledge about ovarian cancer in this population. Our study has several limitations. First, despite a wide distribution, our estimated response rate was low. However, this is in line with previously published research on response rates in provider internet-based surveys.25 Second, distribution of the survey on a webbased blog limited our ability to determine the exact response rate for the survey. Third, we had a limited sampling of family practice and women’s health NPs and PAs, a group that is likely serving in a primary care role for women. Although the survey was distributed to all advanced care providers (NPs and PAs) within the university health system, a limited response from this group of providers was noted. These limitations diminished our overall sample size and thus the generalizability of these results. Finally, there is no established acceptable level of knowledge about ovarian cancer for health care professionals regarding the signs and symptoms or the risk factors. Although the ability to recall and apply 100% of signs would be desirable, it is unclear what the exact goal should be or if this knowledge would improve patient outcomes. CONCLUSIONS

Our investigation has demonstrated that a population of NPs and PAs employed in a large university setting had gaps in their knowledge of the signs, symptoms, and risk factors for ovarian cancer. Continued research and efforts should be focused on educational initiatives and program development for NPs and PAs with regard to ovarian cancer. In addition to traditional education resources, opportunities exist for development of social media platforms or webbased learning to meet this need.33 The goal would be not only to educate this population, and potentially other health care professionals about the key signs, symptoms, and important risk factors for this disease, but also to provide prompts as to when e8

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further diagnostic testing is warranted, such as a CA125, ultrasound, or computed tomography. Ways by which these sites could be made available as well as methods to entice users will need to be investigated, but this goal should be achievable. In addition, engagement between oncology providers and primary care practitioners needs to be enhanced through continued education at national NP and PA symposia. Such cross-pollination could provide meaningful communication and opportunities to collaboratively improve the outcomes for ovarian cancer patients. References 1. Seibaek L, Petersen LK, Blaakaer J, Hounsgaard L. Symptom interpretation and health care seeking in ovarian cancer. BMC Womens Health. 2011;11:31. http://dx.doi.org/10.1186/1472-6874-11-31. 2. American Cancer Society. Cancer Facts & Figures 2016. Atlanta, Ga: American Cancer Society; 2016. 3. Trepanier AM, Supplee L, Blakely L, McLosky J, Duquette D. Public health approaches and barriers to educating providers about hereditary breast and ovarian cancer syndrome. Healthcare (Basel). 2016;4(1). http://dx.doi.org/ 10.3390/healthcare4010019. 4. Buys SS, Partridge E, Greene MH, et al. Ovarian cancer screening in the Prostate, Lung, Colorectal and Ovarian (PLCO) cancer screening trial: findings from the initial screen of a randomized trial. Am J Obstet Gynecol. 2005;193(5):1630-1639. http://dx.doi.org/10.1016/j.ajog.2005.05.005. 5. Lu KH, Skates S, Hernandez MA, et al. A 2-stage ovarian cancer screening strategy using the Risk of Ovarian Cancer Algorithm (ROCA) identifies earlystage incident cancers and demonstrates high positive predictive value. Cancer. 2013;119(19):3454-3461. http://dx.doi.org/10.1002/cncr.28183. 6. Menon U, Ryan A, Kalsi J, et al. Risk algorithm using serial biomarker measurements doubles the number of screen-detected cancers compared with a single-threshold rule in the United Kingdom Collaborative Trial of Ovarian Cancer Screening. J Clin Oncol. 2015;33(18):2062-2071. http://dx.doi.org/ 10.1200/JCO.2014.59.4945. 7. van Nagell JR Jr, DePriest PD, Ueland FR, et al. Ovarian cancer screening with annual transvaginal sonography: findings of 25,000 women screened. Cancer. 2007;109(9):1887-1896. http://dx.doi.org/10.1002/cncr.22594. 8. Goff BA, Mandel LS, Melancon CH, Muntz HG. Frequency of symptoms of ovarian cancer in women presenting to primary care clinics. JAMA. 2004;291(22):2705-2712. http://dx.doi.org/10.1001/jama.291.22.2705. 9. Goff BA, Matthews B, Andrilla CH, et al. How are symptoms of ovarian cancer managed? A study of primary care physicians. Cancer. 2011;117(19): 4414-4423. http://dx.doi.org/10.1002/cncr.26035. 10. Goldstein CL, Susman E, Lockwood S, Medlin EE, Behbakht K. Awareness of symptoms and risk factors of ovarian cancer in a population of women and healthcare providers. Clin J Oncol Nurs. 2015;19(2):206-212. http://dx.doi.org/ 10.1188/15.CJON.206-212. 11. Health Resources and Services Administration, US Department of Health and Human Services. Projecting the supply and demand of primary care practitioners through 2020. 2013. https://bhw.hrsa.gov/sites/default/files/bhw/ nchwa/projectingprimarycare.pdf. Accessed June 10, 2016. 12. Martinez-Gonzalez NA, Berchtold P, Ullman K, Busato A, Egger M. Integrated care programmes for adults with chronic conditions: a meta-review. Int J Qual Health Care. 2014;26(5):561-570. http://dx.doi.org/10.1093/intqhc/ mzu071. 13. Mundinger MO, Kane RL. Health outcomes among patients treated by nurse practitioners or physicians. JAMA. 2000;283(19):2521-2524. 14. Mundinger MO, Kane RL, Lenz ER, et al. Primary care outcomes in patients treated by nurse practitioners or physicians: a randomized trial. JAMA. 2000;283(1):59-68. 15. Rovner J. Some experts dispute claims of looming doctor shortage. St. Louis Post-Dispatch, November 24, 2014. http://www.stltoday.com/news/special -reports/mohealth/some-experts-dispute-claims-of-looming -doctors-shortage/article_49d61a57-7848-5732-b102-c038e19de310.html/. Accessed June 1, 2016. 16. Davis MA, Guo C, Titler MG, Friese CR. Advanced practice clinicians as a usual source of care for adults in the United States. Nurs Outlook. doi: 10. 1016/j.outlook.2016.07.006.

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17. Farrow VA, Lawrence H, Schulkin J. Women’s healthcare providers’ range of services and collaborative care. J Healthc Qual. 2014;36(2):39-49. http://dx.doi.org/10.1111/j.1945-1474.2012.00216.x. 18. American College of Physicians. Nurse practitioners in primary care. 2009. https://www.acponline.org/system/files/documents/advocacy/current_policy_ papers/assets/np_pc.pdf. Accessed June 1, 2016. 19. Shaffer T, Tuggy M, Abercrombie S, et al. Education gaps between family physicians and licensed nurse practitioners. Ann Fam Med. 2012;10(3): 270-271. http://dx.doi.org/10.1370/afm.1409. 20. Cooper CP, Polonec L, Stewart SL, Gelb CA. Gynaecologic cancer symptom awareness, concern and care seeking among US women: a multi-site qualitative study. Fam Pract. 2013;30(1):96-104. http://dx.doi.org/10.1093/fampra/cms040. 21. Gajjar K, Ogden G, Mujahid MI, Razvi K. Symptoms and risk factors of ovarian cancer: a survey in primary care. ISRN Obstet Gynecol. 2012:754197. http://dx.doi.org/10.5402/2012/754197. 22. Jones SC, Magee CA, Francis J, et al. Australian women’s awareness of ovarian cancer symptoms, risk and protective factors, and estimates of own risk. Cancer Causes Control. 2010;21(12):2231-2239. http://dx.doi.org/10.1007/ s10552-010-9643-1. 23. Lockwood-Rayermann S, Donovan HS, Rambo D, Kuo CW. Women’s awareness of ovarian cancer risks and symptoms. Am J Nurs. 2009; 109(9):36-46. http://dx.doi.org/10.1097/01.NAJ.0000360309.08701.73. 24. Hooker RS, Cawley JF, Leinweber W. Career flexibility of physician assistants and the potential for more primary care. Health Aff (Millwood). 2010;29(5): 880-886. http://dx.doi.org/10.1377/hlthaff.2009.0884. 25. Cunningham CT, Quan H, Hemmelgarn B, et al. Exploring physician specialist response rates to web-based surveys. BMC Med Res Methodol. 2015;15:32. http://dx.doi.org/10.1186/s12874-015-0016-z. 26. Willis GB, Smith T, Lee HJ. Do additional recontacts to increase response rate improve physician survey data quality? Med Care. 2013;51(10):945-948. http:// dx.doi.org/10.1097/MLR.0b013e3182a5023d. 27. Goff BA, Mandel LS, Drescher CW, et al. Development of an ovarian cancer symptom index: possibilities for earlier detection. Cancer. 2007;109(2):221-227. http://dx.doi.org/10.1002/cncr.22371. 28. Loerzel VW, Hunt D, Rash E. A Pap test does not screen for everything: nurse practitioner knowledge of ovarian cancer. J Am Assoc Nurse Pract. 2015;27(3): 124-130. http://dx.doi.org/10.1002/2327-6924.12151. 29. Seiser BV. Ovarian cancer strategies for nurse practitioners. J Am Acad Nurse Pract. 2001;13(8):359-363. 30. Kuo YF, Loresto FL Jr, Rounds LR, Goodwin JS. States with the least restrictive regulations experienced the largest increase in patients seen by nurse practitioners. Health Aff (Millwood). 2013;32(7):1236-1243. http://dx.doi.org/ 10.1377/hlthaff.2013.0072. 31. Institute of Medicine. The future of nursing: leading change, advancing health. 2011. http://www.nap.edu/catalog/12956. Accessed May 20, 2016. 32. Gordis L. Epidemiology. 5th ed. Philadelphia, Pa: Elsevier Saunders; 2014. 33. Gagnon K, Sabus C. Professionalism in a digital age: opportunities and considerations for using social media in health care. Phys Ther. 2015;95(3):406-414. http://dx.doi.org/10.2522/ptj.20130227.

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Carol L. Goldstein, PhD, is an affiliate faculty member in the Rueckert-Hartman College for Health Professions at the Loretto Heights School of Nursing of Regis University in Denver, CO. Jeanelle Sheeder, PhD, is an associate professor of Obstetrics and Gynecology in the Division of Family Planning at the University of Colorado School of Medicine in Aurora. Erin Medlin, MD, is an instructor in the Division of Gynecologic Oncology, Department of Obstetrics, Gynecology, and Women’s Health, at the University of Louisville, in Louisville, KY. Patricia L. Cullen, PhD, CPNP-PC, is a professor and director of doctoral and master’s nurse practitioner programs at the Loretto Heights School of Nursing of Regis University. She can be reached at pcullen@ regis.edu. Daniel Hyman, MD, is a resident physician in the Department of Obstetrics and Gynecology at the Baylor College of Medicine in Houston, TX. Kian Behbakht, MD is a professor in the Division of Gynecological Oncology, Department of Obstetrics and Gynecology, at the University of Colorado in Aurora. The authors thank the University of Colorado Hospital for their cooperation in distributing the survey instrument and the Colorado Ovarian Cancer Alliance for their continued willingness to support our research efforts. In compliance with national ethical guidelines, the authors report no relationships with business or industry that would pose a conflict of interest.

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