‘I don't care whether it's HPV or ABC, I just want to know if I have cancer.’ Factors influencing women's emotional responses to undergoing human papillomavirus testing in routine management in cervical screening: a qualitative study

Authors


  • Linked article: This article is commented on by McCourt C, pp. 1430 in this issue.

Abstract

Objective

To explore emotional responses, and predictors of negative reactions, among women undergoing human papillomavirus (HPV) tests in routine clinical practice.

Design

Exploratory qualitative interview study.

Setting

A large busy colposcopy clinic in a Dublin hospital.

Sample

Twenty-seven women who had had an HPV DNA test in the previous 6 months following one or more low-grade cytology tests or treatment for cervical intraepithelial neoplasia (CIN).

Methods

In-depth semi-structured interviews were conducted. Interview transcripts were analysed using a thematic approach (Framework Analysis).

Main outcome measures

Women's emotional responses and predictors of negative emotional reactions.

Results

For most women, having a test for high-risk HPV types generated little negative or positive emotional impact. Adverse emotional responses related to HPV infection rather than testing. Factors that influenced whether women experienced negative emotional responses were: concerns over abnormal cytology or diagnosis of CIN; HPV knowledge; awareness of HPV being sexually transmitted; awareness of HPV prevalence; and HPV information needs. Women's concerns about abnormal cytology/CIN dominated all other issues.

Conclusions

These qualitative data suggest that in the context of follow up of abnormal cytology or treatment for CIN, the emotional impact of HPV testing may be modest: women's primary concerns at this time relate to abnormal cytology/CIN.

Introduction

The causal relationship between certain strains of human papillomavirus (HPV) and cervical cancer[1] is transforming cervical cancer screening strategies. It is widely anticipated that screening for cervical cancer in the future will involve testing for infection with high-risk HPV types, instead of conventional cervical cytology,[2-4] but primary HPV screening will not be implemented until there is greater clarity around appropriate follow up of women who test HPV-positive. In the meantime, HPV testing is being incorporated into screening in other ways. It is being used for co-testing with cytology in some settings,[5] has recently been implemented for triage of women with low-grade abnormal cervical cytology in England;[6] and has been incorporated into the follow-up protocol for women who have been treated for cervical intraepithelial neoplasia (CIN) in various countries.[6-8]

Existing evidence suggests that HPV testing, although clinically effective and most likely cost-effective,[9, 10] may result in a significant psychological burden for women. A recent systematic review concluded that women have concerns about HPV testing, and have worries surrounding the disclosure of having a sexually transmitted infection.[11] Specifically, quantitative research in the UK found that receipt of an HPV-positive result may be associated with a range of negative emotional consequences including distress and anxiety;[12-14] moreover, receipt of a negative HPV test result was not reassuring.[12]

There are several limitations in the available evidence regarding women's emotional responses to HPV testing. No studies have yet investigated women's emotional responses to HPV testing in the context of the new HPV protocols. The studies included in the systematic review[11] were conducted within clinical trials, or in the USA where there is no organised cervical screening programme. Two studies asked women to hypothetically think how they would feel if they underwent HPV testing or if they tested positive for HPV[15, 16] and the findings may not reflect the emotional responses of women tested routinely within organised screening. Studies mainly investigated the negative impact of HPV testing; little is known about positive impacts (e.g. reassurance) or what influences whether a woman has an emotional response. Moreover, the introduction of HPV vaccination programmes may have changed women's awareness of HPV and this could impact on women's reactions to HPV testing.[17]

In order to extend the existing evidence-base, we conducted exploratory in-depth interviews among women who had had an HPV test as part of routine follow up after an abnormal cytology test or treatment for CIN. Our objectives were to (1) explore women's emotional reactions (both positive and negative) to undergoing HPV testing and (2) identify factors that influence negative emotional responses to HPV testing.

Methods

Setting

The study was conducted in Ireland in 2011. Since 2008, a national cervical screening programme, CervicalCheck, has been implemented, offering free cervical cytology tests to women aged 25–60 years.[18] In 2010, a school-based national HPV vaccination programme (nonmandatory) was initiated targeting girls aged 12–13 years, with catch-up for those up to 18 years.[19] In 2012, testing for high-risk HPV types was routinely introduced for post-treatment follow up of women treated for CIN 2/3 in colposcopy clinics affiliated with CervicalCheck.

Participants and recruitment

Colposcopy clinic administrative staff in a public hospital affiliated with CervicalCheck identified the 200 women who had most recently had an HPV DNA test in the previous 6 months following one or more low-grade cytology tests or treatment for CIN. Women who were pregnant at the time of the HPV test were excluded (those who were pregnant at the time of the interview were eligible to take part). Women were stratified by the test result (high-risk HPV-positive/HPV-negative), and sent a letter signed by the lead clinician (WP), inviting them to take part. Interested women returned a reply slip to the research team, and an interviewer (MOC and LC) contacted them to arrange an interview.

The joint Research Ethics Committee of St James Hospital and the Adelaide and Meath Hospital, Dublin approved the study. All participants provided written informed consent before being interviewed.

Interviews

In-depth interviews were carried out in the woman's home or at another convenient location. A semi-structured topic guide (see Supporting information, Appendix S1), developed from literature review, guided the interviews; this was allowed to evolve as interviews progressed. Core issues covered in the topic guide included: screening history; understanding of HPV and abnormal cytology results; having the HPV test; emotional impact of the test result; and information needs. Questions were somewhat specific to whether the woman had a positive or negative test result. Examples of questions asked about emotional responses to the test result include: ‘How did you feel at the time (of the test result)?’ and ‘How did you feel when you learned your HPV test result was negative?’ HPV and its association with sexual activity was not explicitly discussed in the interview unless raised by the participant. Interviews were audio-recorded with the woman's consent and ranged from 25 to 70 minutes in length (mean 48 minutes). Saturation of data, for the group as a whole, was reached after 27 interviews since no new themes or issues related to the topics under investigation had been reported by the interviewees during the last three interviews.[20]

Analysis

Interviews were transcribed verbatim and anonymised. Concurrent data collection and analysis allowed for issues that arose in earlier interviews to inform the content of subsequent interviews. The interviewers independently reviewed and coded transcripts of the first two interviews, discussed these to arrive at consensus, and combined the codes into families. The codes were applied to the rest of the data set and the code lists were refined and developed as the analysis progressed. The interviewers held regular discussions to discuss uncertainties and reach consensus on all aspects of the data. Thematic analysis was undertaken using the Framework Approach to organise the data and identify emerging themes.[21] This involves the development of a matrix, with themes or subthemes comprising the columns, and cases the rows, of the matrix. Data were summarised within the framework matrix to facilitate systematic organisation of the data and examination of themes and cases. Associations, relationships and explanations within the data were explored using the framework. Results reported here relate to emotional responses; findings in relation to women's information needs will be reported elsewhere. O'Connor M, Costello L, Murphy J, Prendiville W, Martin CM, O'Leary JJ, Sharp L (unpublished observations). Direct quotes that illustrate participants' narratives and are representative of themes and subthemes relating to emotional responses to HPV testing have been presented. Each quote is followed by the relevant participant ID number (INT) and what the woman believed her HPV test result was (HPV+, HPV−, or HPV result not known for women who could not recall their test results).

Results

The sociodemographic characteristics of the 27 women interviewed are shown in Table 1. Women ranged in age from 26 to 61 years (median 35 years). Six women stated that they had tested HPV-positive, 11 that they were HPV-negative and ten could not recall their test result. Two major themes were identified: (1) emotional responses and (2) factors influencing negative emotional responses.

Table 1. Demographic characteristics of participants (= 27)
Age  
<30 years4
30–49 years21
≥50 years2
Marital status
Single5
In a relationship, not cohabiting4
Cohabiting3
Married12
Divorced/separated2
Widowed1
Education level
Secondary level—lower1
Secondary level—upper6
Third level—nondegree6
Third level—degree14

Emotional responses

Most of the women interviewed did not describe any emotional reactions: this was irrespective of their HPV test result. Only nine women reported an emotional response to HPV infection testing or receipt of test results. The emotional reactions comprised: (1) positive emotional responses, which included relief, happiness or reassurance and (2) negative emotional responses, which included (a) shame, embarrassment or stigma (which were the most common negative reactions), (b) regret or self-blame and (c) anxiety or worry (Table 2). Among women who experienced negative emotional reactions, their response was predominately related to HPV infection rather than to HPV testing per se.

Table 2. Common emotional responses to HPV infection, testing and/or test results, with illustrative quotes
  Sample quotes
  1. a

    Participant ID number.

  2. b

    Woman stated she was HPV-negative.

  3. c

    Woman stated she was HPV-positive.

Positive emotional responsesRelief‘Thank God like it's all done and dusted…it's all clear you know…there was that nagging doubt that…there'd be something wrong.’ (INT27a, HPV−b)
Happiness‘I was delighted I got tested and when it came back negative it was like, ‘oh thank God just park that up there now for a while.’ (INT24, HPV−)
Reassurance‘It would bring you peace of mind and reassurance [HPV test] because I know I keep saying this about smear tests but I just feel that it's going to be a waste of time because it's going to show nothing.’ (INT28, HPV−)
Negative emotional responsesShame‘I felt really ashamed yea even though…I never slept with anybody else oh God, you know.’ (INT19, HPV+c)
Embarrassment‘I was embarrassed and I was like you know like I was really embarrassed and I was kind of oh God, how did I get this.’ INT20, HPV+)
Stigma‘They don't think oh well it can be from something else or straight away it's like you must be sleeping around.’(INT36, HPV−)
Regret‘And I look back on my life and I you know I suppose there's one part that says you know I should have been more careful.’ (INT03, HPV+)

Self-blame

Anxiety

‘First of all I was going “oh God, I shouldn't have slept with all those people.’ (INT43, HPV+)

‘Like automatically when I heard the word virus, I was like, ‘Ok, so you're saying I have something that might cause me to get cervical cancer.’ (INT04, HPV+)

Worry‘Did I still carry a virus that I could give to someone else? That was one of my concerns.’ (INT03, HPV+)
 ‘The worry was that it would bring back the…symptoms of it again which were the genital warts.’ (INT24, HPV−)

Relief, happiness or reassurance

For a very few women, receipt of an HPV-negative test result was associated with feelings of relief or happiness. For instance, one woman was ‘delighted’ she had been tested and felt that it was one less thing for her to worry about. In addition, a very few women expressed reassurance in relation to undergoing testing per se. For example, one woman, who could not recall her test result, felt that it was better to know if she had an HPV infection than to be unaware. Another woman, who recalled that her test result was negative, felt that having regular HPV tests would be reassuring for women.

Shame, embarrassment or stigma

The shame and embarrassment expressed by some of the women interviewed resulted from HPV being sexually transmitted. One woman compared HPV to sexually transmitted infections like gonorrhoea and chlamydia, describing the HPV virus as ‘dirty’ and ‘disgusting’. Because the virus is sexually transmitted, a few women feared they would experience stigma, and be judged promiscuous by their peers, because of having had an HPV test, irrespective of their test result. One woman (who had a negative result) observed that she would have felt stigma regarding HPV if she had tested positive and was single, but being married protected her from this.

Regret or self-blame

Some of the women interviewed who had tested HPV-positive expressed regret in relation to their past and current lifestyle choices. For instance, one woman believed that her HPV-positive test result was related to a previous genital warts diagnosis: she also expressed regret that she currently smoked. Another woman expressed regret at having had numerous sexual partners in the past. These women blamed themselves for their HPV infections, describing feelings of responsibility and guilt. Other women wondered who had infected them: some queried whether it was their husband or current sexual partner, but most thought it had probably been a previous partner.

Anxiety or worry

Some of the women interviewed were anxious about the potential implications of being HPV-positive. For example, one woman was worried about infecting someone else and another that having the infection in her system would cause past genital warts to recur.

Factors influencing negative emotional responses

Several factors that influenced whether or not these women had a negative emotional reaction to HPV infection, testing and/or test results were identified: (1) concerns over abnormal cytology or diagnosis of CIN; (2) level of HPV knowledge; (3) awareness of HPV being sexually transmitted; (4) awareness of HPV being common among sexually active people; and (5) HPV-related information needs (Figure 1).

Figure 1.

Factors influencing whether or not women experienced negative emotional responses1 to HPV infection, testing and/or test results.

Concerns over abnormal cytology or diagnosis of CIN

In general, women's anxieties surrounding their abnormal cytology, a diagnosis of CIN, or treatment outweighed any concerns about HPV. Most women—whether HPV-positive, HPV-negative or HPV status unknown—were preoccupied with concerns over their abnormal cytology results and related issues: these concerns distracted them from HPV and trying to understand the meaning of their test results. For a very few women, the receipt of an HPV-positive test result added to their existing worry and concerns about their abnormal cytology, a CIN diagnosis or treatment. For instance, one woman had major concerns that she may have cervical cancer due to her abnormal cytology test result and learning about the link between the HPV virus and cervical cancer exacerbated her fears.

Level of HPV knowledge

For most women who reported no negative emotional response to HPV, it became apparent during their interviews that they had relatively low levels of knowledge about HPV infection and testing. In contrast, women who experienced negative emotional responses to their HPV test result tended to have greater knowledge.

Awareness of HPV being sexually transmitted

Some of the women interviewed who had experienced shame and embarrassment knew that HPV could be transmitted sexually. These women learned about sexual transmission from a health professional, friend or family member, or the internet and were shocked and worried about the negative connotations of testing HPV-positive. In contrast, feelings of stigma, and other negative emotions such as regret, were not apparent in women who were unaware of the sexual nature of HPV transmission.

Awareness of HPV being common among sexually active population

Some—but not all—women interviewed were aware that HPV infection is very common and that the majority of women will become infected in their lifetime. These women less often described negative emotional reactions. Most felt that it was important for medical professionals to assure women of how common HPV infections are so as to minimise anxiety and distress.

Information needs surrounding HPV

For almost every woman interviewed who experienced a negative emotional response, it emerged during their interview that they had high HPV information needs. In contrast, for those women for whom the HPV test had minimal emotional impact, it was apparent from their interviews that they had relatively low HPV information needs.

Discussion

Main findings

This study explored the emotional responses, and factors influencing negative emotional responses, in women who underwent HPV testing as part of triage for low-grade abnormal cytology or follow up after treatment. Most women did not experience an emotional reaction. However, a very few women did experience positive emotional reactions. In addition, some women experienced negative emotional reactions and various factors influenced this: concerns over abnormal cytology or diagnosis of CIN; level of HPV knowledge; awareness of HPV being sexually transmitted; awareness of HPV being common among the sexually active population; and HPV information needs.

Strengths and limitations

As far as we are aware, this is the only qualitative study involving women who had undergone HPV testing for triage or as part of follow up within routine screening. The study fills an important gap in the evidence-base relating to women's emotional reactions to HPV testing. A possible limitation is that the study was conducted among women attending one colposcopy clinic. However, this clinic covers a socio-economically diverse population and is likely to reflect other clinics in Ireland. A maximum variation sample was recruited: both HPV-positive and HPV-negative women were interviewed and participants' sociodemographic characteristics were diverse. As with all qualitative research, it is possible that women who were interested in the topic opted to participate. However, this seems unlikely because so few women could recall their results. The interviews aimed to capture responses to HPV both at the time of receipt of the result and afterwards. However, women were interviewed some months after their test and any immediate negative emotional reactions may have dissipated by the interview to the extent that women failed to recall it. Moreover, a limitation of the qualitative approach is that the relative weight or importance of themes and subthemes is not always clear. However, the credibility of the process is evidenced in the opinions expressed in the data set, suggesting that the themes identified will be transferrable to other settings. A further strength is that this paper complies with the COREQ checklist for reporting of qualitative studies.[22]

Interpretation

Our objectives were to investigate women's emotional reactions to HPV testing and the factors that influenced these. In terms of the first objective, our qualitative data suggest a lack of strong negative emotional impact. This contrasts with the findings of previous studies, both qualitative and quantitative.[12, 23, 24] These studies found that receipt of an HPV-positive result was associated with adverse psychosocial outcomes. Our study was conducted after the introduction of an HPV vaccination programme, which may have led to increased HPV awareness and alleviated negative responses. However, HPV knowledge levels among women in the general population remain low despite the introduction of vaccination programmes.[25, 26] In terms of more plausible explanations, in previous studies, women were asked to think hypothetically about HPV testing:[15, 16] this contrasts with our study in which women were actually tested. Women who undergo HPV testing, especially in the context of a colposcopy clinic, receive support from health professionals regarding their HPV test and this may minimise adverse responses.

The psychological impact of receiving abnormal cytology results and undergoing follow up is well documented. Women experience distress in the form of fear of cancer, feelings of self-blame, and infertility worries.[27-31] In fact, women in our study were preoccupied by their abnormal cytology to the extent that these matters dominated adverse reactions that they might otherwise have had to HPV testing. Moreover, many women in our study could not recall their HPV test result, which in itself reveals the extent to which HPV testing or their test results were unimportant in comparison to their abnormal cytology.

Unlike most previous studies,[13, 24, 32] which focused on negative emotional responses, we explored both negative and positive responses to HPV testing. Very few women expressed positive responses. This is consistent with results of a UK survey, that found testing HPV-negative was not reassuring.[12] In our study, women's overriding concerns about their abnormal cytology may explain why more women did not find reassurance in HPV testing, or receiving an HPV-negative result. The lack of reassurance provided by HPV testing is worrying as the new HPV testing protocols offer women less intensive follow up if they test negative.[6-8] Unless women perceive a negative HPV test to be reassuring then these new strategies may fail to help reduce the psychological burden associated with screening.

It has been noted, in the context of other medical tests, that a negative/normal test result does not provide reassurance.[33, 34] According to Leventhal's common-sense model of illness,[33, 35] this is due to the representations held by the individual of the ‘condition’ and of the particular test. Research into women's illness representations around cervical screening is limited.[36] Research around the illness representations of women who have abnormal cytology/CIN, and their representations of HPV testing in these contexts, would help to inform development of strategies to maximise the chances that women who are discharged to less intensive follow up feel sufficiently reassured.

The negative emotional responses of women who did experience these in this study were consistent with those in previous studies.[24, 25, 37] Women's adverse emotional responses were mainly directed at HPV infection itself, and not HPV testing. Women feared that they would be judged as being promiscuous for having a sexually transmitted infection. This finding is consistent with other studies that have reported associations with feelings of stigma following an HPV diagnosis.[16, 37, 38] It was noteworthy that the women who reported feelings of stigma still experienced these at the time of interview, suggesting that this may be a more long-term negative consequence of HPV testing. Our study confirms that, in the context of triage or post-treatment follow up, stigma is likely to be one of the most common, and potentially the most damaging, psychological consequence of testing HPV-positive.

In terms of positive responses to HPV testing, those expressed in our study were similar to those reported elsewhere.[39] However, while some studies found that some women feel reassured or empowered by an HPV-positive result[15, 40] we did not find this: only women who were HPV-negative had a positive reaction, describing reassurance that they were HPV-negative. These contrasting results may be because one study that described empowerment asked women to think hypothetically about how they might feel about HPV testing[15] or because the other study was conducted in the USA, where the health culture is different to Ireland.[40]

In common with other studies,[25, 41, 42] it was clear to the interviewers in this study that women's HPV knowledge levels were mostly low. HPV knowledge was related to whether women experienced a negative emotional response: women who had good knowledge more often experienced negative emotional responses. This finding is striking, in so far as, previous research suggests the opposite—poor HPV knowledge exacerbates psychological distress in women undergoing HPV testing.[39] We have shown, in the same study population, that women with greater knowledge had higher HPV information needs. In addition, women vary in their information needs and a ‘one-size fits all’ approach will not work in terms of HPV information provision. O'Connor M, Costello L, Murphy J, Prendiville W, Martin CM, O'Leary JJ, Sharp L (unpublished observations). These findings present a challenge for screening programmes, suggesting that providing women with (more) information could increase information needs and increase the potential for psychological distress.

Our findings raise important issues for clinical practice in relation to HPV testing in triage and post-treatment. Although our results suggest that adverse responses to HPV testing may be infrequent, screening programmes need to ensure that women's views of cervical screening are not negatively affected by their HPV testing experiences. This will be important to ensure that screening participation and follow up does not decline. This is particularly pertinent given that rates of default from follow up are high.[8, 43-45]

Conclusion

The findings of this robust qualitative study suggest that the emotional impact of HPV testing—in the context of triage or post-treatment follow up—may be modest. The lack of strong emotional reaction is the result of women's concerns surrounding their abnormal cytology taking precedent over all other issues. A range of factors may influence whether or not women suffer adverse emotional reactions to HPV testing. These factors, as well as women's concerns surrounding abnormal cytology, need to be taken into account when medical professionals are counselling women undergoing HPV testing. Although the negative emotional impact was minimal, positive emotional responses were also rare. As the new protocols will return women to routine recall if they test negative for HPV, the lack of reassurance provided by HPV testing could be an issue for screening programmes. Moreover, clinicians and other medical professionals involved in the follow up of women with abnormal cytology need to be prepared to support those women who experience negative emotional responses or a lack of reassurance.

Disclosure of interests

None.

Contribution to authorship

MO'C, JM and LS designed the study. MO'C and LC conducted the interviews, and planned and undertook the analysis. MO'C wrote the initial and subsequent drafts of the manuscript. WP, JM, LS, LC, CM, JJO'L contributed to revising the manuscript. All authors have approved the final manuscript.

Details of ethics approval

The study was approved by the joint Research Ethics Committee of St James Hospital and the Adelaide and Meath Hospital, Dublin (reference: 2010/04/11). Date of approval 1 April 2010.

Funding

This study was undertaken as part of the CERVIVA research consortium (www.cerviva.ie). CERVIVA is funded by the Health Research Board, Ireland (HS-05-09). MOC is an ICE postdoctoral fellow funded by the Health Research Board (ICE/2011/2).

Acknowledgements

We thank the colposcopy clinic staff at the Adelaide and Meath Hospital, Dublin and the women who participated in the study. We are grateful to Ms Kate Higney and Ms Claire O'Callaghan for transcribing the interviews.

Information provision for screening programmes requires a complex, person-centred approach

  • C McCourt

  • Department of Midwifery and Child Health, City University London, London, UK

Linked article: This article is a mini commentary on O'Connor M et al., pp 1421–29. To view this article visit http://dx.doi.org/10.1111/1471-0528.12741.

Why is a study of women's views of a screening programme important, and why small qualitative studies such as described in this article? The perceived psychological burden of human papillomavirus (HPV) testing is considered to be a barrier to using HPV testing within cervical cancer screening programmes. Although they lack the scope of larger-scale surveys, studies using a qualitative approach can help researchers to unpick the ‘why’ and ‘how’ of what matters about screening, to inform policy and practice. Researchers engaged in this kind of research need to be clear about their theoretical framework (their explanatory models—even if tacit) and to consider how their selection of, and approach to, those who use the services might influence the findings. Although a population sample is not the aim in a study of this scale, an appropriate sample should be sought to address or explore the questions being asked, and this should be purposively or theoretically framed. In many cases, the aim of a study is clear but the questions that need to be asked are less so, and an open, exploratory approach has particular advantages here. It enables the respondents to frame issues in their own terms and in relation to what matters most to them and their own lived experience. The findings cannot simply be extrapolated to an entire population but need to be used thoughtfully by researchers to consider what the implications for a programme might be. Additionally, the findings of a range of small qualitative studies can be integrated through systematic review and meta-synthesis.

This study raises a number of interesting points for practitioners to consider, such as that an increased level of knowledge may be linked to increased anxiety—for example, knowing that HPV is sexually transmitted and associated with cancer may increase anxiety, whereas more thorough knowledge (HPV is very common in the population) may alleviate this. This finding echoes wider studies of information provision, which suggest that information provision in health care is often partially, inconsistently or inequitably provided, and may often be too superficial to address women's questions and worries effectively. The study also highlighted some women's lack of reassurance from negative results, an issue that has been found in wider literature on the psychological impact of screening. Conversely, however, the study also illuminated the relevance of ‘context’ in that women may experience little emotional reaction to HPV testing in comparison with the more threatening impact of a potential cancer diagnosis. More specific to some forms of screening, the study also indicated that some women experienced a sense of shame and stigma related to HPV diagnosis. This is potentially important for design of screening programmes in weighing up the benefits or costs and risks. For example, whether they should be focused in a targeted or more universal fashion may be influenced by psychological considerations such as tested–related anxiety but also concepts of stigma or shame. It would be useful to see studies of longer-term impacts on the women involved, as initial emotional impact may be unavoidable with certain forms of screening. Additionally, studies can be conducted building on this work to frame question design with larger and more diverse groups of women.

Disclosure of interests

There are no conflicts of interest to disclose.

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