Iranian HPV-positive Women's Needs and Preferences in Relation to Receiving Health Services: A Qualitative Study

Background: HPV testing is performed in primary care, and in case of abnormal results, the patient is referred to specialized care for follow-up and treatment. Participating in HPV test and receiving an HPV diagnosis can create adverse psychosocial responses. In developing countries that HPV testing recently has been integrated in cervical cancer screening program, to enhance the quality of health services provided to HPV-positive women we need to assess their perceptions. This qualitative study aims to explore HPV-positive women's needs and experiences of receiving health services. Methods: We conducted 40 semi-structured interviews with HPV-positive women. Recorded interviews transcribed and analyzed using conventional content analysis approach. Results: Women sought information on HPV types, transmission, prevalence, and clearance. They also required information about other STIs, potential benets of HPV vaccine, and the risk of HPV-related cancers. Women with abnormal cytology asked about HPV cofactors for cervical cancer. Participants sought ways to improve immunity and sexual health. HPV-positive women's expectations of health care providers (HCPs) include professional principles, communication and counseling skills and HPV-knowledge. Women prefer that HCPs treat them with non-judgmental attitude and do not ask for HIV/hepatitis tests immediately after HPV-diagnosis. "Precancerous" and "high-risk" words and watching colposcopy monitor during procedure had made women anxious. Weak referral system and limited interactions among gynecologists and other HCPs highlighted by participants. Conclusion: The results of this study, based on the experiences and perceptions of HPV women receiving health care, contain messages to healthcare providers at the primary and specialized levels of care to facilitate patient-provider communication around HPV. These practical tips will improve the quality of care for HPV-positive women.


Introduction
Human Papillomavirus is a common sexually transmitted infection, with potentially serious health consequences like cervical cancer (CC)1, 2. CC is eminently preventable through the availability of HPV vaccination and the possibilities of high-risk HPV screening tests3. Health organizations place a higher priority on HPV testing in developing countries where HPV vaccination coverage is poor3.
In Iran, the national HPV vaccination program has not started but Gardasil can be purchased around $100 in some pharmacies. The national CC screening program recommends co-testing (Pap smear and HPV testing) for women aged 30 to 59 every 5 years4. Although co-test has been available for two years in all primary healthcare centers throughout the country, public/private insurance plans do not cover cotesting. There are limited government-funded centers in provincial capitals that charge less for screening.
With more women being screened for or diagnosed with HPV, patient education and counseling efforts are increasingly important and more attention should be given to provider-patient communications5.
Research indicates that participating in HPV test and receiving an HPV diagnosis can create adverse psychosocial responses6-8. In order to avoid anxiety and psychological distress, mass patient education must accompany HPV testing9. Counseling HPV patients presents particular challenges for both physician and patient10.
Promoting patient-centered care practices and good patient-physician communication can lead to positive health outcomes11, 12. In primary healthcare, trust refers to the patients' optimistic believes about care providers and leads to greater patient adherence to care, and better disclosure of sensitive information 13. Emotional and informational support and private counseling space increase patient satisfaction. Patient satisfaction is the comparison of expected care with the patient's perception of care14, 15. Limited studies have investigated HPV communication needs and gaps between HCPs and vaccine-eligible adolescent or HPV-related cancer patients9, [16][17][18][19][20]. It would be valuable to provide a deep understanding of HPV-positive women's challenges, views and experiences of communicating HCPs in receiving healthcare21. Moreover, HPV discussion may be more challenging in societies where HPV is not prevalent and it is attached with intense stigma. Therefore, we designed a qualitative interview study to ll this gap by exploring health needs and preferences of HPV-positive women in relation to receiving health services from their perspectives.

Methods
This qualitative content analysis research was conducted from September 2018 to December 2019 at Valiasr outpatient referral gynecology-oncology clinic (located in Imam Khomeini hospital complex serving a large population of women across the country). Five oncologist-gynecologists and two midwives run the clinic. The time given to each patient is limited and the waiting period for this clinic can be as long as 4-6 months for patients needing follow-up visits; therefore, treatment attrition is relatively high.
The clinic coordinator (a midwife) sent all HPV-positive women (either only hrHPV or both high-risk and low-risk strains) to the interviewer (KQ-female-no contact with participants) in a quiet, comfortable room to provide information on the study's goals and methods and invite quali ed women to participate in the study. Women were eligible for interview if they were over 18 years of age with a heterosexual partnership; had no serious illness (including CC) and were willing to share experience. A purposeful maximum variation sampling was used to recruit information-rich HPV-positive candidates (N = 40) with a diverse age, marital status, education, and socio-economic status (Table 1). Midwives and gynecologists take cervical examinations in Iran. We also interviewed ten providers (Table 2) at two care levels to explore their communication strategies and recommendations to promote communication with HPV-positive women.  The accuracy of this qualitative study was assured based on the four parameters of Guba and Lincoln: credibility, reliability, con rmability, and transferability22, 23. The credibility criterion was achieved by prolonged engagement and member checking. Peer debrie ng and external checking ensured performance con rmability and reliability. Two observers reviewed all transcripts, codes, and categories. Lastly, this process concluded with several discussions among the research team on areas of disagreement before achieving nal consensus. We tried to consider maximum variation during sampling to enhance transferability. In qualitative study, generalizability was labeled as a full description of setting, participants, and categories in rich detail through the outside reader's lens. To achieve reliability, the study procedure was described comprehensive. Direct quotes from participants have presented.
Qualitative content analysis method, described by Burnard et al. 24, was performed using MAXQDA-10 software simultaneously with data collection. Initially, interview transcripts, memos, and eld notes were integrated, and two coders (KQ and STM) read transcripts repeatedly to formulate a general understanding of entire data. Open coding was conducted. The extracted codes were combined with similarities and variations. In higher abstraction levels, sub-categories with related content were interpreted into the main categories.

Results
Participant characteristics shown in Table 1 demonstrate the heterogeneity of sample. Women averaged 34.07 years (21-52 years). All had visited healthcare providers regarding their HPV infection in the 12 months preceding the interview. Half received a diagnosis from a gynecologist, fteen percent from a general practitioner and remain from a primary healthcare provider. All saw a provider other than the one who initially diagnosed them.
Women were asked about their experiences with providers through a series of questions (Appendix1). The analysis of the data led to the extraction of three main categories, including: communication and counseling skills, commitment to professional principles, and HPV-knowledge of providers (Table 3). Details in parentheses following quotes represent the participant's identi cation number (W.=HPV-positive Woman, Pr.=Provider). Counseling women to refer to a genital warts or oral lesions specialist

Communication and Counseling Skills
Women diagnosed with HPV implied communicating preferences and needs in four sub-categories: HPV discussion, emotional support and acceptance, providing recommendations, and clinical consideration.

HPV Discussion
Women preferred face-to-face delivery of their results (HPV/cytology) to receive complex information about their problem's name, HPV types, symptoms, transmission, prevalence, consequences and treatments. Women sought information on other STIs, potential bene ts of HPV vaccine, and the risk of HPV-related cancers. Women with abnormal cytology asked about HPV cofactors for cervical cancer.
They mentioned some points that should be stressed when presenting HPV-information to patients: using plain language, avoiding over-simplifying the disease and sticking to the reality of HPV, gradually transmitting information at multiple appointments, comparing the prevalence of HPV infections and occurrence of cervical cancer (to diminish patients fear of cancer), and expressing that "no one can determine when and from whom a woman get HPV." Participants showed frustration with providers who break diagnosis news in a way that instilled fear and anxiety. To prevent misunderstanding and ensure patient awareness, participants recommended that HCPs provide HPV information over several appointments. Often, patients wished they could ask doctor their questions between visits.
All providers offered examples of women's needs and questions regarding HPV. They implied points that were considered useful. A provider stated: "Pointing out that HPV is common and most women are unaware of their infection changes women's attitudes toward diagnosing HPV from a threat to an opportunity to prevent cancer."(Pr.8) To prove that most women with HPV will not develop CC, some providers compare the prevalence of HPV with the incidence of cervical cancer. They believed this comparison reduces patient anxiety.
Some patients expressed dissatisfaction with the time spent by physicians addressing their concerns. They implied time constraint as key barriers to high-quality care. "A few doctors take the time to talk to patient."(W.23) Women's questions on HPV were often inadequately answered, particularly in specialized governmental referral clinics. "No gynecologist has the patience to answer questions."(W.12) Few women reported even primary HCPs having referred them to the specialized clinic without explaining their health problems.

Emotional Support
Women stated they see their doctor as a source of emotional support. Respondents were more satis ed with compassionate providers who can reassure frightened patients.
"Every illness needs a good doctor. The patient's thoughts are focused on doctor's words. My doctor treated me well. She gave me spirit."(W.2) According to participants' point of view, the cold, annoying, and repulsive behaviors of the doctor hinders successful follow-up and treatment. They found the doctor's excessive self-protection (e.g. wearing three pairs of gloves) repulsive, but HCPs attributed it to the insu cient knowledge of clinician.

Providing Recommendations
HCPs had challenges discussing HPV treatment for patients. They acknowledged that telling patients that "HPV has no cure" makes them nervous. On the other hand, HPV infections will clear up or become undetectable on their own and this is promising. A provider stated: "After saying that 'HPV's most common prognosis is clearance,' some women ask: 'Why hasn't my infection been cleared?' They ask about a test to check the immune system and what can be done to reduce the risk of cancer to negligible levels."(Pr.5) Women discussed feeling powerless if they can't do anything to maintain their health. Some providers pointed to providing simple, practical and inexpensive tips to strengthen immunity of patients. Women needed advice on sexual health too. A gynecologist-oncologist mentioned: "Due to cultural sensitivities, neither patients nor doctors are inclined to speak about sexual issues."(Pr.1) Women with apparent genital warts needed additional information on surgical or medical anti-wart therapies.

Clinical Considerations
Regarding clinical appointments, women needed to be treated gently and respectfully.
"I no longer go to sample due to the intense pain I experienced."(W. 22) Few women expressed anxiety due to hearing the term "precancerous and high-risk" and watching the colposcopy monitor during the procedure.
"I can't get that frightening colposcopy picture off my mind!"(W.9) They wanted verbal or written information before the colposcopy procedure. They also preferred HIV and hepatitis tests not be asked at the very rst visit.

Commitment to Professional Principles
Some HPV-positive women were disappointed with healthcare providers' performance. Their statements showed that few HCPs are not fully committed to professional principles.

Gaining Patients' Trust
Women stated very few doctors had recommended or prescribed unproven medications for HPV cure. Patients were not sure if it was a research project.
Most women pointed to the physicians' success in earning patient con dence as a factor related to care continuity. HCPs emphasized that uncertainties such as HPV-vaccination of HPV-infected people should be addressed in HPV-discussion.

Con dentiality and Privacy
Women were less satis ed with physicians who unintentionally highlight stigma by judging patients' sexual behavior. They did not trust such HCPs and were reluctant to share private information with them. Participants noted that all staff dealing with sexually transmitted patients should be trained in patient secrecy.
"I think OB/GYN visits require the most privacy. I went to a famous GYN clinic. There were other patients in the room besides me. I was embarrassed. Imagine sitting next to a complete stranger who might hear you and talk about sensitive topics that are very di cult to discuss."(W.10)

Avoid Financial Misconduct
Participants indicated lack of insurance coverage for diagnostic and therapeutic services. Patient pessimistic believes about nancial misconducts of HCPs revealed in some interviews. "I paid 10,000,000 IRR for colposcopy in a private o ce. If my doctor had referred me here [Valiasr], I could've had a colposcopy for 400,000 IRR! She deliberately did not refer me here!"(W.14) Few women were upset of HCPs who treat them based on their economic status.
"My doctor recommended colposcopy and when she found out that I had no money for it, she stopped explaining it and did not answer my questions"(W.17)

HPV-Knowledge of Providers
As an important obstacle to high quality HPV management, participants indicated inadequate knowledge and training in HCPs. Providers pointed to a lack of continuous and integrated training program for physicians and midwives.

Adherence to Screening Guidelines
Successful management of CC screening is hindered by guideline discordant. A 34-years-old HPV screening eligible woman reported: "After my husband's genital warts, I went to a gynecologist. I was scared. The doctor said: 'It doesn't matter. Since you don't have a lesion, you don't need HPV testing."(W.31) A few participants, on the other hand, reported another form of guideline discordant in which some gynecologists appeared to overuse screening tests to provide greater reassurance, whether the HPV-DNA test or the Pap test. To better monitoring of high-risk cases such as CIN-2, most providers have proposed a systematic national registry system.
Avoid misconceptions Women exposed misinformation conveyed by a few HCPs who may lack current HPV information. A woman reported that a provider had recommended her cesarean section because of vaginal warts.
Using extra-protective equipment such as wearing three pairs of surgical gloves nonverbally indicated to a misconception that non-sexual transmission of the virus is serious.

Taking Multidisciplinary Approach
More than half of the women interviewed had seen at least three doctors in the 12 months before the interview. Satisfaction and HPV-knowledge did appear to rise among this subset of women.
Patients reported attending to a number of different HCPs including general practitioner, gynecologistoncologist, dental professional, infectious disease specialist, dermatologist, dentist, urologist, nurse, lab technician, and midwife. According to participants' point of view, there is not an optimal cross-disciplinary referral system among gynecologists and other HCPs.
A woman with oral ulcers worried about HPV-related precancerous oral lesion. "I've seen ENT specialist and dentist to get other opinions just to be on the safe side."(W. 28) Participants indicated that physicians' con icting opinions on HPV vaccination and using condoms in those already infected with HPV were among the reasons to frequent visits.

Discussion
The perceptions and preferences clearly described in this study may provide deeper insight to HCPs working with HPV-infected people to establish evidence-based strategies to support patient-provider communication around HPV. Findings indicated that providers' communication strategies is as important as content. The way in which information on HPV is conveyed needs careful consideration. How providers communicate women about their HPV results can have an in uence on their emotional responses to HPV diagnosis25.
Findings noted that healthcare providers should be cautious in choosing their words; since ASCCP consensus (2020) is hesitant that pre-cancer is the best de nition for CIN2 or CIN3 and higher26, 27.
Using new risk tables, to risk estimates, and management of abnormal screening tests, which are freely available online at https://CervixCa.nlm.nih.gov/RiskTables,28 could alter providers' interpretation of positive results.
Women veri ed that requesting HIV-test in the rst appointment after diagnosis requires consultation.
Gynecologists should consider that some women prefer not to look at the colposcopy monitor during the procedure.
In this study women expected caregivers to spend enough time to answer their questions. Due to the limited number of gynecologist-oncologists, it is expected that at the primary level of care, more time can be allocated for patient education and counseling than specialized level. In addition, to provide basic HPV-information, waiting room posters or lea ets or an educational website could be bene cial. Therefore more time will leave to face-to-face appointments to answer questions and make a patientcentered two-way HPV communication19, 29.
HPV testing may lead to questions regarding sexual history, which clinicians should be prepared to discuss30. Iranian religious beliefs that physicians may hold about sexuality can be a barrier to optimal sexual health care31. In our setting, midwives are quali ed communicators because they are of the same sex and are trained for sexual counseling.
Our ndings suggest ways to build trust, such as addressing current gaps in HPV-knowledge. Gaining patient con dence is critical in decisions to receive medical services, compliance, and healthcare satisfaction13. Another study2 addressed the importance of disclosing existing limitations in HPVknowledge with patients.
A study indicated that HPV patients may perceive certain physician behavior as negative even though the doctor does not plan to30. HPV patients may be more pessimistic in societies with religious-cultural sensitivity and strong stigma. Caregivers should note that these cultures have instilled a STI of embarrassment and guilt. HCPs are critical in informing patients and moderating patients' psychosocial response.
Our results emphasize the need for patient consent to participate in HPV clearance trials. This is not only their right, but also increases their trust. The success of physicians in gaining patient trust leads to continued treatment.
Providers should be aware of the privacy and secrecy issues associated with an STD diagnosis, particularly in culturally sensitive societies. A study noted privacy as a factor of high-quality primary services14.
Due to the high cost of colposcopy, Iranian health insurance providers were suggested to include CC screening procedures in their service packages32.
Our study showed that HCPs require continuing education programs for guideline adherence and updated knowledge. Doctors must make deliberate efforts to improve their HPV-related communication skills34, 35 Gynecologists' awareness of the provision of the HPV-DNA test, such as time intervals and test series, was unsatisfactory in another study. It was because of the multiplicity and rapidly evolving guidelines33.
Potential overuse of HPV testing among women's health providers was reported in another study34. This may indicate the patient-centered care or knowledge de ciency. Further studies are needed to characterize compliance of providers with national guidelines for HPV testing.
As previous studies have emphasized, doctors, medical students, and dental providers need training to provide appropriate basic HPV-knowledge to patients16, 35, 36. HCPs also should know that HPV may contaminate protective equipment but HPV-DNA transfer to medical personnel is unlikely to occur37.
Since the most women interviewed had visited at least three doctors, Iranian physicians must follow a multidisciplinary approach and, knowing their own limitations, refer patients to proper specialist facilities as a rst step towards effective management.
We acknowledge the study's limitations. Our study environment was one busy specialized center for HPVpatients so it is possible that emerged themes would be different from other clinics nationally. Therefore, caution is required when interpreting data. We should comment on the potential in uence of a highly educated sample (~ 60% with university education) as another limitation. Naturally, qualitative research is not targeted at representativeness, but it seems likely that less-educated women's viewpoints were not thoroughly explored. Some of the ndings are cultural-speci c and cannot be generalized to all communities.
Like other qualitative studies, the generalizability and relative weight of emergent categories are not obvious. This paper follows COREQ checklist for reporting qualitative studies38. Participants in this study

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