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Risk perception, worry, and test acceptance in average-risk women who undergo ovarian cancer screening

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Risk perception, worry, and test acceptance in average-risk women who undergo ovarian cancer screening
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  ONCOLOGY  Risk perception, worry, and test acceptance in average-risk women who undergo ovarian cancer screening Laura L. Holman, MD; Karen H. Lu, MD; Robert C. Bast Jr, MD; Mary A. Hernandez, RN, MSN; Diane C. Bodurka, MD;Steven Skates, PhD; Charlotte C. Sun, DrPH, MPH OBJECTIVE:  We evaluated baseline knowledge of ovarian cancer risk and perceptions toward ovarian cancer screening (OCS) by initiatingthe normal risk ovarian screening study. STUDY DESIGN:  Average-risk, postmenopausal women were enrolledbetween 2001 and 2011 as they entered the normal risk ovarianscreening study. Participants completed baseline surveys of risk perception, cancer worry (Cancer Worry Scale), anxiety (State-TraitAnxiety Inventory), health and well-being survey (SF-36 HEALTHSURVEY), and acceptability of OCS. RESULTS:  Of the 1242 women who were enrolled, 925 women(74.5%) completed surveys. The respondents estimated a mean life-time risk of ovarian cancer of 29.9%, which is much higher than theactual risk of 1.4% for women in the United States. Only 2.8% ofparticipants correctly estimated their risk; 35.4% of the participantsreported their lifetime risk to be  50%. Cancer worry was low, with amedian Cancer Worry Scale score of 7 of 24. Anxiety was comparablewith published norms for women in this age group, with median STAI-State and STAI-Trait scores of 30 and 29 of 80, respectively. Overall,women reported good physical and mental well-being. In terms of OCSacceptability, 97.2% of respondents agreed or strongly agreed that“the benefits of screening outweigh the difficulties.” Very few womenwere reluctant to undergo OCS because of time constraints (1.1%),pain (2.0%), or embarrassment (1.9%). CONCLUSION:  Average-risk women who underwent OCS highlyoverestimated their risk of ovarian cancer. Despite this, participantsreported low cancer worry and anxiety. The discrepancy betweenknowledge of and attitudes toward ovarian cancer risk highlights theneed for educational efforts in this area. Key words:  acceptability of screening, cancer worry, ovarian cancerscreening, risk perception Cite this article as: Holman LL, Lu KH, Bast RC, et al. Risk perception, worry, and test acceptance in average-risk women who undergo ovarian cancer screening. Am JObstet Gynecol 2014;210:257.e1-6. A lthough not common, ovariancancer is the most deadly gyneco-logic malignancy; there were 22,000 new cases and > 14,000 deaths anticipated in2013. 1 Although stage I disease is asso-ciatedwitha90%5-yearsurvivalrate,theprognosis for advanced stages is poor.Because of the nonspeci 󿬁 c symptoms of early ovarian cancer, 80% of women arestage III or IV at the time of diagnosis. 2 One strategy to decrease the mortality rateistoestablishaneffectivemethodforthe detection of early-stage ovarian can-cer. To date, however, potential screening methods for ovarian cancer have hadunacceptably high false-positive rateswithout any demonstration of a signi 󿬁 -cant reduction in ovarian cancer deaths,which has led to recommendationsagainst routine ovarian cancer screening for the general population. 3 From the Departments of Gynecologic Oncology and Reproductive Medicine (Drs Holman, Lu, Bodurka, and Sun) and Experimental Therapeutics(Dr Bast and Ms Hernandez), The University of Texas MD Anderson Cancer Center, Houston, TX, and Biostatistics Center, Massachusetts GeneralHospital, Boston, MA (Dr Skates).Received July 10, 2013; revised Oct. 15, 2013; accepted Nov. 13, 2013.SupportedbyfundsfromtheM.D.AndersonSPOREinOvarianCancer,NCIP50CA83639,andgrantnumberT32CA101642fromaNationalInstitutesof Health National Research Service Award, the Bioinformatics Shared Resources of the MD Anderson CCSG NCI P30 CA16672, the NationalFoundation for Cancer Research, philanthropic support from Golfers Against Cancer, the Tracey Jo Wilson Foundation, the Mossy Foundation, theNorton family, and Stuart and Gaye Lynn Zarrow; and in part by grant number CA152990 from National Cancer Institute ’ s Early Detection ResearchNetwork (S.S.). The contents of this study report are solely the responsibility of the authors and do not necessarily represent the of  󿬁 cial views of the National CancerInstitute or National Institutes of Health.R.C.B.receivesroyaltiesforCA125fromFujirebioDiagnosticsInc(Malvern,PA)andhonorariafromVermillionInc(Austin,TX)forserviceontheirScienti 󿬁 c AdvisoryBoard;S.S.isafacultymemberatMassachusettsGeneralHospital,whichhaslicensedtheRiskofOvarianCancerAlgorithm.Allotherauthorsreport no con 󿬂 ict of interest.Presented in poster format at the 43rd annual meeting on Women ’ s Cancer of the Society of Gynecologic Oncology, Austin, TX, March 24-27, 2012.Reprints: Karen H. Lu, MD, The University of Texas MD Anderson Cancer Center, Department of Gynecologic Oncology- Unit 1362, 1155 HermanPressler, CPB6.3244, Houston, TX 77030-3721. khlu@mdanderson.org. 0002-9378/$36.00    ª 2014 Mosby, Inc. All rights reserved.    http://dx.doi.org/10.1016/j.ajog.2013.11.022 MARCH 2014  American Journal of Obstetrics &  Gynecology  257.e1 Research  www. AJOG .org   A single-arm, multiinstitutional pro-spectivestudyofovariancancerscreening that used the Risk of Ovarian CancerAlgorithm, known as the Normal Risk Ovarian Screening Study (NROSS), iscurrently underway in the United States.This study involves annual CA125 mea-surements in postmenopausal womenwho have an average (eg, normal,population-based) risk of the develop-ment of ovarian cancer. The screening algorithm incorporates a woman ’ s ageand the change in her CA125 measure-ment over time to estimate her risk of having undetected ovarian cancer.Womendeemedtobeatintermediaterisk (between 1 in 2000 and 1 in 500) aretriaged to undergo a repeat CA125 mea-surement in 3 months, although womenwho are found to be at an elevated risk are triaged to undergo a transvaginal ul-trasound scan and referral to a gyneco-logic oncologist. Recently publishedresults demonstrate that ovarian cancerscreening with the Risk of OvarianCancer Algorithm is feasible, with apositive predictive v alue of 40% and aspeci 󿬁 city of 99.9%. 4 Therehavebeenfew publishedstudiesregarding ovarian cancer knowledgeand risk perception among average-risk women who undergo ovarian cancerscreening. Baseline analysis of partici-pants in the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS),which is a prospective trial of ovariancancerscreeningintheUnitedKingdom,found that, although  > 40% of womencorrectly identi 󿬁 ed their risk, approxi-mately one-half of respondents under-estimated their ovarian cancer risk. 5 Incontrast, studies in the United Stateshave found that most women tend tooverestimate their ovarian cancer risk. 6 This lack of knowledge regarding per-sonal cancer risk is not surprising giventhat multiple studies have demonstratedthat women generally are unaware of ovarian cancer risk factors. 5,7,8 Little isknown about ovarian cancer worry oracceptance of screening among average-risk women who undergo ovarian can-cer screening.The present study was designed as acompanion to the NROSS. We aimedprospectively to assess ovarian cancerrisk perception, ovarian cancer worry,and acceptability of ovarian cancerscreening among women who initiate anovarian cancer screening trial that usesthe Risk of Ovarian Cancer Algorithm. M ATERIALS AND  M ETHODS Between July 2001 and October 2012,1457 womenwere enrolled prospectively in the NROSS at MD Anderson CancerCenter. Most of these women wererecruited to the trial from MD Ander-son ’ s Cancer Prevention Clinic, which isa clinic that provides care to patientswithout activecancer.Other participantsfound out about the trial through word-of-mouth from women who already were enrolled in the trial. Women whowere eligible for the NROSS were post-menopausal, from 50-75 years old, hadat least 1 ovary, had no active cancer andno history of ovarian cancer, and werewilling to undergo annual blood draws,follow-up CA125 measurements, andtransvaginal ultrasound scans as recom-mendedbytheNROSSprotocol.Womenwere ineligible if they were at high risk for the development of ovarian cancer. High-risk   was de 󿬁 ned as a patient withat least 1 of the following: (1)  BRCA1  or BRCA2  mutation, (2) known or sus-pected Lynch syndrome, (3) a  󿬁 rst- orsecond-degree male relative with breastcancer, (4) Ashkenazi Jewish descentwith premenopausal breast cancer or afamily history of ovarian cancer or pre-menopausal breast cancer, or (5) 2  󿬁 rst-or second-degree relatives with ovariancancer, premenopausal breast cancer, orboth. The full details of the NROSSprotocol have been published. 4 After informed consent was obtainedfor NROSS, women who could readand speak English were offered partici-pation in the questionnaire portion of thetrial.Becauseof  󿬁 nancialconstraints,only NROSS participants at MD Ander-son Cancer Center were asked to enrollin the questionnaire study. Of the 1457women who were eligible for the survey,1242 women (85.2%) provided separatewritten, informed consent to partici-pate before study enrollment. This study wasapprovedbytheInstitutionalReview Board of The University of Texas MDAnderson Cancer Center.On entry into the study and beforeundergoing ovarian cancer screening,participants were given the study ques-tionnaires. Patient demographics andmedical history were collected prospec-tively. The survey assessed ovarian can-cer risk perception and the acceptability of ovarian cancer screening, ovariancancer worry with the use of a modi 󿬁 edLerman breast cancer worry scale, anxi-ety with the use of the Spielberger State/Trait Anxiety Inventory (STAI), andgeneral qualit y of  life with the SF-36Health Survey. 9-11 No educational ma-terialswereprovidedaspartofthisstudy.The SF-36 Health Survey, STAI, andthe Cancer Worry Scale were scored ac-cording to the respective scoring mech-anism for each instrument. Baselinedemographic information was summa-rized with descriptive statistics thatincluded medians, means, standard de-viations, ranges, and frequencies. Mann-Whitney   U   and  c 2 tests were used tocompare differences between groups.IBM SPSS Statistics for Windows(version 19.0; IBM Corp, Armonk, NY)wasusedforstatisticalanalysis.A2-sidedprobability value of   <  .05 was consid-ered statistically signi 󿬁 cant. R  ESULTS Of the 1242 women who were enrolled inthe study, 925 women (74.5%) completedthe surveys. Table 1 shows a comparisonof the demographics of women who com-pleted surveys (responders) to those whodid not (nonresponders). Overall, thegroups were similar, although responderswere slightly older and more likely tobe white than were nonresponders.In general, survey participants highly overestimated their risk of ovarian can-cer. Respondents estimated their meanlifetime risk to be 29.9% (Figure).Approximately one- 󿬁 fth of the partici-pants stated that their risk of ovariancancer was 25-49%, and more than one-third of them believed their risk to be  50%. Only 2.8% of women correctly identi 󿬁 ed their risk as 1-2% (Table 2).When asked what their chances of get-ting ovarian cancer were compared with “ other women your age, ”  45.3% of therespondents said they were  “ about thesame. ”  However, 22.2% of the women Research  Oncology  www.AJOG.org  257.e2  American Journal of Obstetrics &  Gynecology  MARCH 2014  believed their ovarian cancer risk was  “ alittle higher ”  or  “ much higher ”  thanother women. Interestingly, only 26.4%of the womenwho responded noted thatthey were  “ fairly certain ”  or  “ very certain ”  about their opinions on ovariancancer risk. Of note, 55% of respondentssaid that they received their informationabout ovarian cancer from television,newspapers, or magazines, although justover one-quarter of them relied on theirhealthcare provider for this information.Although survey participants tendedto overestimate their risk of ovariancancer, they were optimistic regarding the ability to screen for the disease. Of the respondents, 93.6%  “ agreed ”  or “ strongly agreed ”  that ovarian cancercould be cured when detected early.Furthermore, 91.5% of the womenbelieved that transvaginal ultrasonogra-phycould detect ovarian cancer at a stagewhen it could be cured; 86.4% of themthought the same of a single CA125value. Additionally, in spite of perceiving themselves to be at high risk for ovariancancer, few women (12%) were afraidthattheirovariancancerscreeningresultswould be abnormal. Likewise, only 4.4%of respondents reported that they oftenthought about ovarian cancer; 0.6% of them stated that thoughts about ovariancancer affected their mood, and 0.3% of them reported that thoughts aboutovarian cancer interfered with theirability to perform their daily activities.A modi 󿬁 ed cancer worry scale and theSTAI were used to measure objectively study participants ’  anxiety and ovariancancer worry. As expected, given par-ticipants ’  responses regarding frequency ofovariancancerthoughts,cancerworry was low, with a median score of 7.0(range, 6.0 e 20.0) of 24. The STAI alsofound anxiety to be low overall. Themedian STAI-State (STAI-S) score,which measures anxiety about an event,was 30 of 80. The median STAI-Trait(STAI-T) score, which measures one ’ sbaseline anxiety, was 29 of 80. This iscomparable with the published norms of postmenopausal women for these scalesof 32.2 and 31.79, respectively. 11 As evidenced by the SF-36 HealthSurvey scores, study participants demon-strated good physical and mental health.Table 3 lists participants ’  median scoresfor each of the 8 scales on the SF-36Health Survey as well as the 50th and75th percentiles of SF-36 Health Survey scores for women in the g eneral popula-tion in the United States. 10 Survey par-ticipants were also queried regarding acceptability of ovarian cancer screening (Table 3). The overwhelming majority of women “ agreed ” or “ stronglyagreed ” thatthereweremorebene 󿬁 tstoovariancancerscreening than dif  󿬁 culties. Very few womensaidpain,embarrassment,ortimeconstraints were reasons that they wouldbe reluctant to undergo screening. Themost commonly cited reason to not bescreened was fear of insurance notcovering the cost of the tests.Post-hoc subgroup analyses wereperformed on women with a history of breast cancer and women with no per-sonal cancer history. Women with abreast cancer history had signi 󿬁 cantly higher median estimates of their lifetimeovarian cancer risk than women with nocancer history (35.0% vs 25.0%;  P   ¼ .001). Additionally, breast cancer survi-vors tended to have poorer physicalfunctioning than women with no cancerhistory, with signi 󿬁 cantly worse scoreson all 4 physical functioning scales of theSF-36 Health Survey (all  P   <  .05).However, there were no statistically sig-ni 󿬁 cant differences between groups inother aspects of the survey, including the cancer worry scale, the STAI-S, theSTAI-T, or acceptability of ovarian can-cer screening (all  P  > .05). C OMMENT As anticipated, our study populationdemonstrated minimal baseline knowl-edge of ovarian cancer risk. Althoughmost study participants reported thatthey believed their risk of the develop-ment of ovarian cancer was similar to TABLE 1 Demographics of survey responders vs nonresponders (N [ 1242) Variable Responders (n [ 925) Nonresponders (n [ 317)  P   value  Age, y .004Median, range 59 (50 e 74) 58 (50 e 74)Mean 60.1 59Race, n (%)  < .001White 792 (85.6) 236 (74.4) African American 43 (4.6) 29 (9.1)Hispanic 43 (4.6) 30 (9.5) Asian 46 (5.0) 21 (6.6)Other 1 (0.1) 1 (0.3)Parity, n (%) .325Parous 745 (80.5) 257 (81.1)Nulliparous 179 (19.4) 52 (16.4)Unknown 1 (0.1) 8 (2.5)Cancer history, n (%) .101None 402 (43.5) 145 (45.8)Breast cancer 234 (25.3) 80 (25.2)Other cancer 289 (31.2) 92 (29.0)Family history, n (%)Breast cancer 325 (35.1) 99 (31.2) .185Ovarian cancer 71 (7.7) 26 (8.2) .782 Holman. Perceptions regarding ovarian cancer screening. Am J Obstet Gynecol 2014 .  www.AJOG.org   Oncology  Research MARCH 2014  American Journal of Obstetrics &  Gynecology  257.e3  other women their age, few of themcorrectly identi 󿬁 ed their ovarian cancerrisk. In fact, most women greatly over-estimated their risk. This result is incontrasttothoseofthebaselinesurveyof UKCTOCS participants. When queriedabout their personal ovarian cancer risk,42.3%ofwomenintheUKCTOCSstudy accurately identi 󿬁 ed their risk as 1 in 70,although 50.1% underestimated theirrisk at 1 in 500. 5 The discrepancy be-tween the  󿬁 ndings of the UKCTOCSstudy and those in our study may bea re 󿬂 ection of the difference betweenpopulations in the United Kingdom andthe United States because other studiesthat have been performed in the UnitedStates have found that both average- andhigh-risk women tend to ov erestimatetheir ovarian cancer risk. 6,12 Addition-ally, although women in the presentstudywereaskedtoprovidetheirovariancancer risk on a scale of 0-100%, womenin UKCTOCS were asked about theirrisk in a multiple choice fashion withpossible answers that ranged from 1 in12 to 1 in 500. It is well-established thatpeople interpret information differently based on the manner in which it is pre-sented or  “ framed. ”  This is known as the “ framing effect ” and mayaccount for thedifferences in the results that were seenin the 2 studies. 13 Despite survey participants ’  percep-tion that their ovarian cancer risk wasvery high, the median scores for theCancer Worry Scale, STAI-T, and STAI-Ssuggest that overall worry and anxiety that are associated with ovarian cancerwere low. The reasons for this discrep-ancy are unclear. Studies of high-risk women who undergo ovarian cancerscreening have demonstrated an associ-ation between high levels of perceivedovarian cancer risk and high levels of anxiety. 14,15 To date, however, there havebeen no published studies that haveassessed cancer-related anxiety or worry among women with average-risk whoundergo cancer screening. Additionally,despite the current lack of evidence insupport of population-based screening,most respondents indicated that early-stage ovarian cancer can be cured andthat transvaginal ultrasound scanning orasingleCA125testwouldbesuf  󿬁 cientto detect ovarian cancer at an early stage. This belief about ovarian cancerscreening suggests that women may over-estimate the effectiveness of eitherof these methods to detect early-stageovarian cancer and may explain the in-congruity between participants ’  percep-tions of ovarian cancer risk and theirreported worry and anxiety.Ovarian cancer screening was accept-able to our study population. A smallnumber of women were concerned thatthe blood tests and ultrasound scanswould be too painful, time consuming,or embarrassing. The most commonly cited reason against screening was fearthat insurance would not cover theprocedures. However, only 21% of re-spondents believed that this would be anissue. Furthermore, most respondentsbelieved that the bene 󿬁 ts of screening outweighed any dif  󿬁 culties. It shouldbe noted that few survey questionsaddressed ovarian cancer screening acceptability and that these questionswere phrased in the form of statementswith which respondents were asked toagree or disagree. This may limit theconclusions that can be made regarding ovarian cancer screening acceptability among our population. However, ourresults mirror the  󿬁 ndings from thesmall number of other studies that haveattempted to determine women ’ s ac-ceptability of ovarian cancer screening.In their study of   > 2200 average-risk  TABLE 2 Median SF-36 Health Survey scores of survey respondents comparedwith norms for women in the United States SF-36 HealthSurvey domainsMedian surveyparticipant score50th percentilefor women in theUnited States 10 75th percentilefor women in theUnited States 10 Physical functioning 90.0 90.0 100.0Role-physical 100.0 100.0 100.0Bodily pain 84.0 74.0 100.0General health 82.0 72.0 85.0 Vitality 70.0 60.0 75.0Social functioning 100.0 87.5 100.0Role-emotional 100.0 100.0 100.0Mental health 88.0 80.0 88.0 Holman. Perceptions regarding ovarian cancer screening. Am J Obstet Gynecol 2014 . TABLE 3 Ovarian Cancer Screening Acceptability Survey questions Survey questions a Agree/stronglyagree, n (%) The benefits of ovarian cancer screening outweigh the difficulties. 818 (97.2)I don’t have time for ovarian cancer screening. 826 (1.1)I am reluctant to undergo ovarian cancer screening because theprocedures are painful.814 (2.0)I am reluctant to undergo ovarian cancer screening because theprocedures are embarrassing.820 (1.9)I am reluctant to undergo ovarian cancer screening because myinsurance won’t pay for the tests.792 (21.8) a Participants were asked if they strongly agree, agree, disagree, or strongly disagree with these statements. Holman. Perceptions regarding ovarian cancer screening. Am J Obstet Gynecol 2014 . Research  Oncology  www.AJOG.org  257.e4  American Journal of Obstetrics &  Gynecology  MARCH 2014  women who underwent  “ symptom trig-gered ”  ovarian cancer screening, Goff et al 16 reported that most women foundthe screening for symptoms to beacceptable. Furthermore, the womenwho underwent CA125 testing or trans-vaginal ultrasound scanning had a highrate of acceptability for the procedures.However, only 27 of the 47 womenwho underwent a procedure completed asurvey.Ourstudy participants ’ misperceptionsregarding personal risk of ovarian canceremphasize the need for education in thisarea. Previous studies have also demon-strated a lack of awareness regarding gy-necologic malignancies among women inthe United States. With respect to ovariancancer speci 󿬁 cally, study populationsrepeatedlyhavedisplayedlittleknowledgeregarding risk factors and symptoms. 8,17 To complicate matters, it appears thatmany women learn about ovarian cancerfrom the mass media. In our own study, > 50% of respondents reported receiving their ovarian cancer information fromthe media, although only 25% spoke totheir healthcare provider about it. How-ever, where women learn about ovariancancer may be due to more than simply patient preference. In 1 survey of  > 1200women, 80% of respondents reportedthat their physician had never discussedsymptoms and risk  factors of ovariancancer with them. 8 Educational initia-tives, such as the Centers for DiseaseControl ’ s  Inside Knowledge : Get the Facts about Gynecologic Cancer, 18 have beendeveloped in an attempt to use the mediato raise gynecologic cancer awareness.However, the impact of these campaignsis not yet known.Educational efforts also must befocused on screening for ovarian cancer.There is evidence that women in thegeneral population erroneously believethat routine tests, such as the Papanico-laou test, screen for a variety of malig-nancies, including ovarian cancer. 8,17 Furthermore, despite the lack of conclu-sive evidence to support widespreadovarian cancer screening, the presentstudy and the survey of UKCTOCS par-ticipants found that women tend tobelieve that ovarian cancer screening willlead to fewer advanced-stage cancers andimprove morbidity. 5 Although the pre-liminary   󿬁 ndings of the UKCTOCS andNROSS are promising, the  󿬁 nal resultsare not yet available. 4,19 If they supportthe implementation of ovarian cancerscreening for the general population, itis critical that women are educatedregarding the bene 󿬁 ts and possible limi-tations of ovarian cancer screening.A potential for bias in our study liesin the method by which our study population was recruited. All study participants volunteered to enroll in astudy of ovarian cancer screening, andmost of them were recruited from acancerpreventionclinicatMDAnderson.As such, their attitudes and beliefs re-garding ovarian cancer screening arepotentiallydifferentfromthoseofwomenin the general population. Additionally,most of the women in the study werewhite, meaning our results may not begeneralizable to a minority population.Another limitation is the potential fornonresponse bias. This bias is likely minimal, however, given our highoverall response rate and the few dif-ferences that were noted betweensurvey responders and nonresponders(Table 1). It should also be noted thatsome women did not answer all survey questions. Potential reasons for thisinclude that they did not believe thatthey had time to complete the survey,they did not know some of the answersto some questions, or that they werenot comfortable with some of thequestions.In our study, all participants answeredsurvey questions before undergoing ovarian cancer screening. Although itis valuable to understand how womenfeel about ovarian cancer screening atbaseline because this indicates howlikely they are to initiate screening, it is possiblethat their opinions may change once they have had experience with screening.Additionally, a subset of women whoundergo screening will have false-positiveresultsthatpromptadditionaltesting.Itisimportant to evaluate whether thesewomen have a change in their anxiety,cancer worry, or psychologic well-being as compared with women who only have normal testing. We currently areattempting to assess this in our study population by administering follow-upsurveys to those women who have FIGURE Respondents estimate of personal ovarian cancer risk  Responses to the question: “What do you think your chances are of getting ovarian cancer in yourlifetime?” Holman. Perceptions regarding ovarian cancer screening. Am J Obstet Gynecol 2014 .  www.AJOG.org   Oncology  Research MARCH 2014  American Journal of Obstetrics &  Gynecology  257.e5
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