European Journal of Oncology Nursing 18 (2014) 201e205
Contents lists available at ScienceDirect
European Journal of Oncology Nursing journal homepage: www.elsevier.com/locate/ejon
Knowledge, attitudes and practices of physicians and nurses regarding the link between IVF treatments and breast cancer Ilana Kadmon a, b, *, Yelena Goldin c, Yuval Bdolah d, Morshid Farhat d, Michal Liebergall-Wischnitzer a, b a
Henrietta Szold School of Nursing, Israel Hadassah/Hebrew University Medical Center, Hadassah Hospital, Kiryat Hadassah POB 12000, Jerusalem, Israel Clalit Health Services, Kiryat Moshe, Jerusalem, Israel d Reproductive Endocrinology Division, Department of Obstetrics and Gynecology, Hadassah-Hebrew University Medical Center, Mount Scopus, Kiryat Hadassah POB 12000, Jerusalem, Israel b c
a b s t r a c t Keywords: IVF Breast cancer Fertility nursing risk assessment Clinical breast exam
Purpose: The ovarian stimulating hormones used in In-Vitro Fertilization may increase the incidence of breast cancer. Little research has been conducted to ascertain health professionals’ knowledge or practices regarding this possible connection and if they communicate this risk to their patients. This study described the knowledge, attitudes and practices of doctors and nurses regarding the causative link between In-Vitro Fertilization treatments and breast cancer, and to determine if these health professionals were assessing or communicating this possible risk to their patients. Method: Seventy gynecologists and nurses who worked in fertility clinics, had at least one year of experience in fertility and were literate in Hebrew were asked to complete the questionnaires. Ten clinics around the country were contacted and the questionnaires were distributed and collected on the same day. Results: 35 Nurses and 35 gynecologists completed the survey. Although the majority of the physicians (68%) and nurses (69%) thought that there was a possible connection between the hormonal treatment of IVF and breast cancer, physicians were significantly more likely to inform their patients about the connection than were nurses. Conclusions: There is a gap between the attitudes and practices of both physicians and nurses in communicating possible cancer risk to IVF clients. It would be beneficial to create a standardized risk communication protocol that would include information and guidelines for practice. More research must be conducted in this area, as there is almost no data on possible maternal risk from IVF treatment. Ó 2013 Elsevier Ltd. All rights reserved.
Introduction In-Vitro Fertilization (IVF) is a common infertility treatment throughout the world, and it has been increasing in popularity since 1978. One in every 50 births in Sweden, 1 in 60 in Australia, and 1 in every 80e100 births in the United States are the result of IVF. In 2003, more than 100,000 IVF cycles were reported by 399 clinics in the US, with a live birth rate of more than 48,000 babies (Van
* Corresponding author. Henrietta Szold Hadassah Hebrew University School of Nursing, P.O.B 12000, Jerusalem 91120, Israel. Tel.: þ972 2 6777757; fax: þ972 2 6439020. E-mail addresses: [email protected] (I. Kadmon), ybdolah@hadassah. org.il (Y. Bdolah). 1462-3889/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejon.2013.10.009
Voorhis, 2007). In 2012, there were an estimated 5 million infants born through IVF technology (ESHRE, 2013). In relation to the population size and the number of IVF treatments performed, Israel is the leader, out of 48 counties, in the number of IVF/ICSI cycles per million people per year (Collins, 2002). In contrast to other Western European countries, IVF is covered in Israel by the national health insurance up to the age of 45 and for two live births (Simonstein, 2010), which greatly expands its availability to the infertile population. Infertility treatments include ovarian stimulating hormonal medications that may have potential negative side effects, including the development of cancer due to inter-cell modifications caused by the treatments. There is little discussion, however, as to if, how and when physicians or any health professional should discuss this particular risk, or other maternal health risks, with the
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patient, and whether the patient should be informed of these possible risks. Pre-Artificial Reproductive Technology (ART) risk assessment, both psychological and the risk for developing breast cancer, has been poorly studied, yet due to the growing number of IVF cycles performed each year, further research into its implementation may be recommended.
of physicians (Hunter et al., 1998; Graham et al., 1998; Walter and Britten, 2002; Preissig and Rigby, 2010). It is evident from those studies and additional theoretical reviews that there is often a conflict between institutional protocol and provider implementation, but perhaps more importantly between provider attitude and actual practice (Aarons, 2005).
Background
The study
The influence of female hormones on the etiology and the development of breast cancer are well known (Lipworth, 1995). Early menstruation and late menopause both are related to long term exposure to high levels of circulating endogens and to the risk for developing breast cancer (Bernstein, 2002; Borini and Rebellato, 2008). The use of ecogene hormones during fertility treatments raises questions regarding their usage and the risk of developing breast cancer (Healy and Venn, 2003; Kanakas and Mantzavinos, 2006; Katz et al., 2008). In a study conducted in the US involving more than 12,000 women who had undergone IVF treatment between 1965 and 1988 with Clomephene Citrate and gonadotrophines, there was a significant increase of breast cancer found among these women as compared to the general population (Brinton et al., 2005, 2004). On the other hand, Burkman et al. (2003) retrospectively examined 4575 women with breast cancer, as compared to a control group, and found that the drugs used for IVF did not cause a higher risk for breast cancer. Similarly, Braga et al. (1996), studying women with fertility problems, also demonstrated that although hormonal treatment for these women did raise their risk for developing breast cancer, it was not statistically significant. A Finnish study examined a cohort of 9175 women who purchased IVF medications and followed these women for a period of two years. They concluded that the general cancer risk of hormonal related cancers in women was not increased by IVF treatment (Yli-Kuha et al., 2012). In 2013, Li and colleagues reported a meta-analysis of eight cohort studies and they concluded that there is no significant association between IVF and cancer risk (Li et al., 2013). Brinton et al., also in 2013, in their study of 87,000 women who went through IVF and looking at their overall cancer risk, also found no significant relationship between IVF and the risk for breast, ovarian and endometrial cancers (Brinton et al., 2013). Although they concurred that, in the general population, there was no significant additional risk of breast cancer, Katz et al.’s (2008) large cohort study did find that over the age of 30 there is increased breast cancer risk while Stewart et al. (2012) study of 21,025 women also found significant breast cancer risk for women under 24 years of age. To date, the most current research suggests that there is not a link between IVF treatment and future development of breast cancer.
Aims
Doctors and nurses knowledge, attitudes and practice, regarding IVF and breast cancer Very little research has been conducted as to how health professionals incorporate Evidence based practice (EBP) into their own daily clinical activity, or how they feel when EBP protocols are imposed upon them (Graham, 1998). In addition, little is known about the congruence between health professionals’ attitudes and actual practice toward many routine procedures. For this study, no articles could be located describing health professionals’ attitudes toward a possible connection between IVF and breast cancer, or any other possible maternal risk of IVF treatment at all. Ascertaining physician or nurse attitude and practice toward other protocols was also difficult. For the few studies that were conducted, anonymous questionnaires requesting information about knowledge, practice and attitudes were sent to large groups
The purpose of this study was to describe the knowledge, attitudes and practices of doctors and nurses regarding the causative link between IVF treatments and breast cancer, and to elucidate the relationship between their knowledge, attitudes and practices regarding this link and sociodemographic variables. Design This is a cross-sectional correlational study with convenience sampling of physician and nurse employees of fertility clinics throughout Israel. Sample/participants The sample included nurses and gynecologists who were employed in IVF clinics in 10 hospitals in Israel. Gynecologists and nurses who had worked in an IVF clinic, for at least one year and were literate in Hebrew were eligible to participate in this study. The initial suggested sample size was 128 participants, divided equally between nurses and physicians, in order to reach a power of 80% with p ¼ 0.05, and assuming a medium effect size. However, only 70 participants were surveyed, due to logistic limitations. Data collection As there was no instrument found in the literature created to ascertain physician or nurse attitudes toward IVF protocol and possible risks, both physician and nurse questionnaires were designed by the one of the researchers (Y.G) after collaborating with IVF, breast cancer and methodological experts. A total of 19 questions were divided into three sections: knowledge, attitudes and practices. As there is no gold standard for validation, expert validation by two physicians who run fertility centers, three expert IVF nurses and two clinical breast care nurse specialists was received. After questionnaire review and modification, the present versions were accepted. A sociodemographic questionnaire was also included. A pilot study was then conducted to further validate the questionnaires. Ethical consideration Approval was received by the ethics review committee of the sponsoring hospital. Participants signed a consent form prior to completing the questionnaire and no identifying information was collected, keeping the responses anonymous. Data analysis The statistical analysis included descriptive statistics, Independent t-test for continuous variables and Pearsons correlation for categorical variables. Factor analysis using the Manova was also conducted to analyze possible significant differences between physician and nurse responses.
I. Kadmon et al. / European Journal of Oncology Nursing 18 (2014) 201e205
Validity and reliability The Physician IVF KAP had a Cronbach’s a of 0.80 and the Nurse IVF KAP a Cronbach’s a of 0.69. Results This study included 70 participants, of them 35 (50%) were nurses and 35 (50%) were physicians, all employed in IVF clinics throughout Israel. Twenty-three (33%) were men and the rest were women. The average age of each participant was 46 (SD ¼ 8.74), ranging from 27 to 67 years of age. Most of the participants (90%) were married and the rest were divorced, single or widowed. All the participants had at least one child. Forty seven percent of them were senior gynecologists and two were residents. The average time of employment in an IVF clinic was nine years, ranging from three to 39 years (Table 1). Knowledge, attitudes and practice Most physicians and nurses (46, 67%) felt a possible connection exists between IVF and breast cancer. Fourteen (41%) of the physicians and fourteen (43%) of the nurses answered that a definitive connection between age of the patient and breast cancer incidence had not been proven (see Table 2). Fifteen (44%) of the physicians and thirteen (37%) of the nurses felt that the age limit of 45 should be maintained and not changed but that women over 40 should receive information about possible increased risk of future breast cancer incidence. Sixteen (50%)
Table 1 Sociodemographic variables. Variable
Category
Frequency
% Response
Gender
Female Male
47 23
67 33
Marital status
Single Married Divorced Widowed
1 63 5 1
1 90 7 1
Children
Yes No
70 e
100 e
Profession
Nurse Doctor
35 35
50 50
Degree
Certified Nurse BSc. MSc. MD
10 19 6 35
14 27 9 50
Professional status
Nurse Resident Physician
35 33 2
50 47 3
Working status
Full-time Part-time
31 39
44 56
Country of Origin
Israel Former U.S.S.R Europe Other
45 16 6 1
66 24 9 1
Religion
Jewish Christian Muslim
65 2 3
93 3 4
Religious affinity
Ultra Orthodox/Very Religious Religious Traditional Secular
1 17 14 38
1 24 20 54
203
physicians and twenty-six (74%) nurses felt that the medical establishment should increase the level of awareness of a possible connection between IVF and breast cancer, as it is the public’s right to know. Thirty-three (97%) of physicians and thirty-two (91%) of nurses felt that patient’s request for minimal hormone exposure should be taken into account when deciding whether to conduct treatment, together with a clinical explanation as to possible treatment failure. Ten (29%) of the physicians and twenty-one (60%) of the nurses feel that limiting the number of IVF cycles should be determined by the number of risk factors that the patient has to develop breast cancer. The majority of physicians (67%) and nurses (69%) felt that the practitioner should present the possible connection to the patient. The overwhelming majority of the participants, 74% of the physicians and 69% of the nurses felt that this risk information should be added to the informed consent form in the IVF clinic. We did not find significant differences between doctors and nurses in any of the 19 questions, and we did not find significant differences in the 19 questions between various demographic subgroups. Therefore, we performed a factor analysis of the 19 questions that resulted in four scales which explained 68.5% of the variance: treatment risk and risk management; breast examination; providing the patient with relevant risk information; consideration of the patient’s needs. A total of 13 variables had significant loadings onto one of the four factors. In a comparison of physician and nurse scores using these four scales (using Manova), a significant difference was found between doctors and nurses in the practice of giving information: physicians tend to inform the clients about the connection between IVF treatment and breast cancer more than nurses do (F (1, 65) ¼ 4.301; p ¼ 0.042). Sixteen (47%) of the physicians and twelve (34.3%) of the nurses said they would discuss the possible connection between hormonal treatment and breast cancer only if the woman presented with a breast cancer risk factor and seven (21%) of the physicians and nine (25.7%) of the nurses said they would only discuss the possible connection if the patient brought up the issue. In regards to providing information on the possible connection, the majority of physicians (18, or 56%) and nurses (14, or 56%) would tell the patient that it is likely that there is a connection between hormonal treatment and breast cancer. Thirteen (38%) of the physicians said they always conduct clinical breast exams (CBE), by themselves, before proceeding with an IVF treatment, compared to thirteen (38%) of the physician participants that said they never conduct CBE prior to treatment. Twenty (59%) of the physicians reported that they always refer the patient to a surgeon for CBE. In Israel, it is the norm for breast surgeons to conduct CBE instead of the gynecologist (Israeli Ministry of Health, 2005). The nurses were asked if the physicians in their wards conduct CBE on new patients. Thirteen (37%) responded that the physician always conducts a CBE and 12 (34%) said the physician never conducts a CBE. Twenty (59%) of the physicians stated that they always refer a woman to receive a CBE by a surgeon prior to the IVF treatment. When the nurses were asked, they responded that eighteen (51%) of the physicians always refer the patient to a surgeon to receive a CBE prior to treatment. Twenty-one (61%) of the physicians said they would not begin treatment without the results of a breast exam and fifteen (43%) of the nurses concurred. Seventy one percent of both physicians and nurses said that there was an institutional protocol in place requiring that a breast exam be conducted prior to initiating IVF treatment. There was no statistically significant connection between attitudes and any of the sociodemographic variables, age, education, age at immigration, years of experience, or years working in an IVF clinic for neither nurses nor physicians.
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Discussion The survey was based on the model of the theory of reasoned action, which suggests that the attitude toward a particular object or concept influences eventual behavior, but it is not the only predictor and is influenced by a spectrum of contextually based variables (Ajzen and Fishbein, 1977; Bagozzi, 1992). In this study, both physicians and nurses felt there was potential risk for the patient but did not actually change their behavior with the patient to address her of this risk. The majority of physicians and nurses felt that there was a connection between IVF and breast cancer, despite the growing body of evidence that suggests that there is no connection between the two. They also support, in part, their current institutional protocol that requires the physician to conduct a clinical breast exam or at least refer a woman to an exam prior to initiating the treatment. However, neither the physician nor the nurse is raising the issue of possible risk with the patient herself. Approximately 40% of doctors and nurses answered that there is no definite connection between age and breast cancer incidence. Although there is a large body of evidence to suggest that IVF does not increase breast cancer risk generally, there is research supporting that IVF does increase risk for women beginning IVF treatments after the age of 30 (Katz et al., 2008) and prior to age 24 (Stewart et al., 2012). This implies that women undergoing IVF treatment at an older age may be at increased risk for developing breast cancer. It was interesting to note that both doctors and nurses thought that it is important to add the information of the possible connection between IVF and breast cancer to the informed consent before the treatment initiation (the current form does not include such information). There seems to be a gap between the professional attitudes toward the issue and actual practice. Although the majority of physicians and nurses stated that they knew there was an institutional protocol for CBE and that they themselves either examined the patient or had the woman physically examined for breast malignancies prior to the treatment, most practitioners did not discuss possible increased breast cancer risk with the patient. It was not part of the provider patient dialogue at all. This raises interesting questions as to how much providers discuss risk with their patients in general even if the provider believes there to be a risk. Communicating possible risk of a procedure to the patient can be challenging for the health professional, especially in a situation where the objective risk is unclear and the subjective outcome for the patient is also uncertain (Bogardus et al., 1999). However, the health professional may have an obligation to insure that the patient understands all of the possible risks and benefits of the procedure before deciding to commit to the treatment (Bogardus et al., 1999). Health professional assisted decision-making should help “minimize the chances of undesired consequences according to the best possible scientific evidence” (O’Connor et al., 2003, p. 736). Segev et al. (2011) proposed a pre-ART medical assessment to identify possible risk factors for maternal morbidity during pregnancy and immediately post partum for women over 40 (2011). Yet breast cancer may not be the only possible risk for women undergoing IVF procedures. Research has suggested a possible connection with endometrial and ovarian cancers (Calderon-Margalit et al., 2009). Perhaps an additional risk communication component should be added for non-pregnancy related morbidity potentially associated with IVF treatment. Although some discussion about a standardized approach for risk disclosure has been described in the literature (Bogardus et al., 1999), there is no current dialogue about standardized maternal risk disclosure for IVF treatment.
Although there has been concern among researchers and practitioners about the possible connection between IVF treatment and future breast cancer, an abundance of data asserts the lack of connection. This study suggests that nurses and physicians are still concerned about their patients’ risk enough to implement protocols that moderately assess breast cancer risk before treating the patient; however the patient is not yet part of the risk communication dialogue. Perhaps review and standardization of protocols is suggested, along with protocols for discussion of maternal risk, in general, in regards to fertility treatment. Limitations No questionnaires were found in the literature regarding the knowledge, attitudes and practices assessment of physicians and nurses regarding possible connection between IVF treatments and breast cancer. Therefore, the validity and reliability of the questionnaire was tested only in the specific study population. The study involved a convenience sample of doctors and nurses who were specifically approached by the researcher, with minimal diversity in culture, education or age.
Conclusions and implication for practice It will be beneficial for physicians and nurses to have a standardized pre ART risk assessment protocol, which would include a standardized risk discussion with the patient. Given the current research, it is advisable that every patient would sign informed consent that would include relevant information of the possible connection between IVF treatments and breast cancer. In addition, nurses working in fertility clinics are in an ideal position to engage patients in a discussion of risk assessment so that the patient may make a truly informed decision about IVF treatments. Conflict of interest statement None declared. Role of funding source No external sources of funding. Acknowledgments The authors would like to thank Aviva Yoselis of Israel Health Consulting for her editorial assistance in preparing this manuscript. Appendix A. Supplementary material Supplementary material associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ejon. 2013.10.009. References Aarons, G.A., 2005. Measuring provider attitudes toward evidence-based practice: consideration of organizational context and individual differences. Child Adolesc. Psychiatr. Clin. N. Am. 14, 255e271. Ajzen, I., Fishbein, M., 1977. Attitude-behavior relations: a theoretical analysis and review of empirical research. Psychol. Bull. 84, 888e918. Bagozzi, R.P., 1992. The self-regulation of attitudes, intentions, and behavior. Psychol. Q. 55, 178e204. Bernstein, L., 2002. Epidemiology of endocrine-related risk factors for breast cancer. J. Mammary Gland Biol. Neoplasia 7, 3e15.
I. Kadmon et al. / European Journal of Oncology Nursing 18 (2014) 201e205 Bogardus Jr., S.T., Holmboe, E., Jekel, J.F., 1999. Perils, pitfalls, and possibilities in talking about medical risk. J. Am. Med. Assoc. 281, 37e41. Borini, A., Rebellato, E., 2008. Focus on breast and ovarian cancer. Placenta 29, 184e 190. Braga, C., Negri, E., La Vecchia, C., Parazzini, F., Dal Maso, L., Franceschi, S., 1996. Fertility treatment and risk of breast cancer. Hum. Reprod. 11, 300e303. Brinton, L.A., Moghissi, K.S., Scoccia, B., Westhoff, C.L., Lamb, E.J., 2005. Ovulation induction and cancer risk. Fertil. Steril. 83, 261e274. Brinton, L.A., Scoccia, B., Moghissi, K.S., Westhoff, C.L., Althuis, M.D., Mabie, J.E., et al., 2004. Breast cancer risk associated with ovulation-stimulating drugs. Hum. Reprod. 19, 2005e2013. Brinton, L.A., Trabert, B., Shalev, V., Lunenfeld, E., Sella, T., Chodick, G., 2013. In vitro fertilization and risk of breast and gynecologic cancers: a retrospective cohort study within the Israeli Maccabi Healthcare Services. Fertil. Steril. 99, 1189e 1196. Burkman, R.T., Tang, M.T., Malone, K.E., Marchbanks, P.A., McDonald, J.A., Folger, S.G., et al., 2003. Infertility drugs and the risk of breast cancer: findings from the National Institute of Child Health and Human Development Women’s Contraceptive and Reproductive Experiences Study. Fertil. Steril. 79, 844e851. Calderon-Margalit, R., Friedlander, Y., Yanetz, R., Kleinhaus, K., Perrin, M.C., Manor, O., et al., 2009. Cancer risk after exposure to treatments for ovulation induction. Am. J. Epidemiol. 169, 365e375. Collins, J., 2002. An international survey of the health economics of IVF and ICSI. Hum. Reprod. Update 8, 265e277. ESHRE (European Society of Human Reproduction and Embryology) (2013, July 1). ART fact sheet. Retrieved from: http://www.eshre.eu/Guidelines-and-Legal/ ART-fact-sheet.aspx. Graham, I., Stiell, I., Laupacis, A., O’Connor, A., Wells, G., 1998. Emergency physicians’ attitudes toward and use of clinical decision rules for radiography. Acad. Emerg. Med. 5, 134e140. Graham, J., 1998. Perspectives. AHCPR’s evidence-based centers: will their findings guide clinical practice? Med. Health 52, 1e4. Healy, D.L., Venn, A., 2003. Infertility medications and the risk of breast cancer. Fertil. Steril. 79, 852e854.
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Hunter, A., Wright, P., Cappelli, M., Kasaboski, A., Surh, L., 1998. Physician knowledge and attitudes towards molecular genetic (DNA) testing of their patients. Clin. Genet. 53, 447e455. Israeli Ministry of Health, 2005. Health Ministry Report and Protocol Recommendations: Breast Cancer Prevention and Early Discovery. Retrieved from http:// www.health.gov.il/hozer/mk25_2005.pdf. Kanakas, N., Mantzavinos, T., 2006. Fertility drugs and gynecologic cancer. Ann. N. Y. Acad. Sci. 1092, 265e278. Katz, D., Paltiel, O., Peretz, T., Revel, A., Sharon, N., Maly, B., et al., 2008. Beginning IVF treatments after age 30 increases the risk of breast cancer: results of a casee control study. Breast J. 14, 517e522. Li, L.L., Zhou, J., Qian, X.J., Chen, Y.D., 2013. Meta-analysis on the possible association between in vitro fertilization and cancer risk. Int. J. Gynecol. Cancer 23, 16e24. Lipworth, L., 1995. Epidemiology of breast cancer. Eur. J. Cancer Prev. 4, 7e30. O’Connor, A.M., Légaré, F., Stacey, D., 2003. Risk communication in practice: the contribution of decision aids. BMJ 327, 736e740. Preissig, C.M., Rigby, M.R., 2010. A disparity between physician attitudes and practice regarding hyperglycemia in pediatric intensive care units in the United States: a survey on actual practice habits. Crit. Care 14, R11. Retrieved from: http://ccforum.com/content/14/1/R11 (01.07.13). Segev, Y., Riskin-Mashiah, S., Lavie, O., Auslender, R., 2011. Assisted reproductive technologies: medical safety issues in the older woman. J. Women’s Health (Larchmt) 20, 853e861. Simonstein, F., 2010. IVF policies with emphasis on Israeli practices. Health Policy 97, 202e208. Stewart, L.M., Holman, C.D., Hart, R., Bulsara, M.K., Preen, D.B., Finn, J.C., 2012. In vitro fertilization and breast cancer: is there cause for concern? Fertil. Steril. 98, 334e340. Van Voorhis, B.J., 2007. Clinical practice. In vitro fertilization. N. Engl. J. Med. 356, 379e386. Walter, F.M., Britten, N., 2002. Patients’ understanding of risk: a qualitative study of decision-making about the menopause and hormone replacement therapy in general practice. Fam. Pract. 19, 579e586. Yli-Kuha, A.N., Gissler, M., Klemetti, R., Luoto, R., Hemminki, E., 2012. Cancer morbidity in a cohort of 9175 Finnish women treated for infertility. Hum. Reprod. 27, 1149e1155.
Contents lists available at ScienceDirect
European Journal of Oncology Nursing journal homepage: www.elsevier.com/locate/ejon
Knowledge, attitudes and practices of physicians and nurses regarding the link between IVF treatments and breast cancer Ilana Kadmon a, b, *, Yelena Goldin c, Yuval Bdolah d, Morshid Farhat d, Michal Liebergall-Wischnitzer a, b a
Henrietta Szold School of Nursing, Israel Hadassah/Hebrew University Medical Center, Hadassah Hospital, Kiryat Hadassah POB 12000, Jerusalem, Israel Clalit Health Services, Kiryat Moshe, Jerusalem, Israel d Reproductive Endocrinology Division, Department of Obstetrics and Gynecology, Hadassah-Hebrew University Medical Center, Mount Scopus, Kiryat Hadassah POB 12000, Jerusalem, Israel b c
a b s t r a c t Keywords: IVF Breast cancer Fertility nursing risk assessment Clinical breast exam
Purpose: The ovarian stimulating hormones used in In-Vitro Fertilization may increase the incidence of breast cancer. Little research has been conducted to ascertain health professionals’ knowledge or practices regarding this possible connection and if they communicate this risk to their patients. This study described the knowledge, attitudes and practices of doctors and nurses regarding the causative link between In-Vitro Fertilization treatments and breast cancer, and to determine if these health professionals were assessing or communicating this possible risk to their patients. Method: Seventy gynecologists and nurses who worked in fertility clinics, had at least one year of experience in fertility and were literate in Hebrew were asked to complete the questionnaires. Ten clinics around the country were contacted and the questionnaires were distributed and collected on the same day. Results: 35 Nurses and 35 gynecologists completed the survey. Although the majority of the physicians (68%) and nurses (69%) thought that there was a possible connection between the hormonal treatment of IVF and breast cancer, physicians were significantly more likely to inform their patients about the connection than were nurses. Conclusions: There is a gap between the attitudes and practices of both physicians and nurses in communicating possible cancer risk to IVF clients. It would be beneficial to create a standardized risk communication protocol that would include information and guidelines for practice. More research must be conducted in this area, as there is almost no data on possible maternal risk from IVF treatment. Ó 2013 Elsevier Ltd. All rights reserved.
Introduction In-Vitro Fertilization (IVF) is a common infertility treatment throughout the world, and it has been increasing in popularity since 1978. One in every 50 births in Sweden, 1 in 60 in Australia, and 1 in every 80e100 births in the United States are the result of IVF. In 2003, more than 100,000 IVF cycles were reported by 399 clinics in the US, with a live birth rate of more than 48,000 babies (Van
* Corresponding author. Henrietta Szold Hadassah Hebrew University School of Nursing, P.O.B 12000, Jerusalem 91120, Israel. Tel.: þ972 2 6777757; fax: þ972 2 6439020. E-mail addresses: [email protected] (I. Kadmon), ybdolah@hadassah. org.il (Y. Bdolah). 1462-3889/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ejon.2013.10.009
Voorhis, 2007). In 2012, there were an estimated 5 million infants born through IVF technology (ESHRE, 2013). In relation to the population size and the number of IVF treatments performed, Israel is the leader, out of 48 counties, in the number of IVF/ICSI cycles per million people per year (Collins, 2002). In contrast to other Western European countries, IVF is covered in Israel by the national health insurance up to the age of 45 and for two live births (Simonstein, 2010), which greatly expands its availability to the infertile population. Infertility treatments include ovarian stimulating hormonal medications that may have potential negative side effects, including the development of cancer due to inter-cell modifications caused by the treatments. There is little discussion, however, as to if, how and when physicians or any health professional should discuss this particular risk, or other maternal health risks, with the
202
I. Kadmon et al. / European Journal of Oncology Nursing 18 (2014) 201e205
patient, and whether the patient should be informed of these possible risks. Pre-Artificial Reproductive Technology (ART) risk assessment, both psychological and the risk for developing breast cancer, has been poorly studied, yet due to the growing number of IVF cycles performed each year, further research into its implementation may be recommended.
of physicians (Hunter et al., 1998; Graham et al., 1998; Walter and Britten, 2002; Preissig and Rigby, 2010). It is evident from those studies and additional theoretical reviews that there is often a conflict between institutional protocol and provider implementation, but perhaps more importantly between provider attitude and actual practice (Aarons, 2005).
Background
The study
The influence of female hormones on the etiology and the development of breast cancer are well known (Lipworth, 1995). Early menstruation and late menopause both are related to long term exposure to high levels of circulating endogens and to the risk for developing breast cancer (Bernstein, 2002; Borini and Rebellato, 2008). The use of ecogene hormones during fertility treatments raises questions regarding their usage and the risk of developing breast cancer (Healy and Venn, 2003; Kanakas and Mantzavinos, 2006; Katz et al., 2008). In a study conducted in the US involving more than 12,000 women who had undergone IVF treatment between 1965 and 1988 with Clomephene Citrate and gonadotrophines, there was a significant increase of breast cancer found among these women as compared to the general population (Brinton et al., 2005, 2004). On the other hand, Burkman et al. (2003) retrospectively examined 4575 women with breast cancer, as compared to a control group, and found that the drugs used for IVF did not cause a higher risk for breast cancer. Similarly, Braga et al. (1996), studying women with fertility problems, also demonstrated that although hormonal treatment for these women did raise their risk for developing breast cancer, it was not statistically significant. A Finnish study examined a cohort of 9175 women who purchased IVF medications and followed these women for a period of two years. They concluded that the general cancer risk of hormonal related cancers in women was not increased by IVF treatment (Yli-Kuha et al., 2012). In 2013, Li and colleagues reported a meta-analysis of eight cohort studies and they concluded that there is no significant association between IVF and cancer risk (Li et al., 2013). Brinton et al., also in 2013, in their study of 87,000 women who went through IVF and looking at their overall cancer risk, also found no significant relationship between IVF and the risk for breast, ovarian and endometrial cancers (Brinton et al., 2013). Although they concurred that, in the general population, there was no significant additional risk of breast cancer, Katz et al.’s (2008) large cohort study did find that over the age of 30 there is increased breast cancer risk while Stewart et al. (2012) study of 21,025 women also found significant breast cancer risk for women under 24 years of age. To date, the most current research suggests that there is not a link between IVF treatment and future development of breast cancer.
Aims
Doctors and nurses knowledge, attitudes and practice, regarding IVF and breast cancer Very little research has been conducted as to how health professionals incorporate Evidence based practice (EBP) into their own daily clinical activity, or how they feel when EBP protocols are imposed upon them (Graham, 1998). In addition, little is known about the congruence between health professionals’ attitudes and actual practice toward many routine procedures. For this study, no articles could be located describing health professionals’ attitudes toward a possible connection between IVF and breast cancer, or any other possible maternal risk of IVF treatment at all. Ascertaining physician or nurse attitude and practice toward other protocols was also difficult. For the few studies that were conducted, anonymous questionnaires requesting information about knowledge, practice and attitudes were sent to large groups
The purpose of this study was to describe the knowledge, attitudes and practices of doctors and nurses regarding the causative link between IVF treatments and breast cancer, and to elucidate the relationship between their knowledge, attitudes and practices regarding this link and sociodemographic variables. Design This is a cross-sectional correlational study with convenience sampling of physician and nurse employees of fertility clinics throughout Israel. Sample/participants The sample included nurses and gynecologists who were employed in IVF clinics in 10 hospitals in Israel. Gynecologists and nurses who had worked in an IVF clinic, for at least one year and were literate in Hebrew were eligible to participate in this study. The initial suggested sample size was 128 participants, divided equally between nurses and physicians, in order to reach a power of 80% with p ¼ 0.05, and assuming a medium effect size. However, only 70 participants were surveyed, due to logistic limitations. Data collection As there was no instrument found in the literature created to ascertain physician or nurse attitudes toward IVF protocol and possible risks, both physician and nurse questionnaires were designed by the one of the researchers (Y.G) after collaborating with IVF, breast cancer and methodological experts. A total of 19 questions were divided into three sections: knowledge, attitudes and practices. As there is no gold standard for validation, expert validation by two physicians who run fertility centers, three expert IVF nurses and two clinical breast care nurse specialists was received. After questionnaire review and modification, the present versions were accepted. A sociodemographic questionnaire was also included. A pilot study was then conducted to further validate the questionnaires. Ethical consideration Approval was received by the ethics review committee of the sponsoring hospital. Participants signed a consent form prior to completing the questionnaire and no identifying information was collected, keeping the responses anonymous. Data analysis The statistical analysis included descriptive statistics, Independent t-test for continuous variables and Pearsons correlation for categorical variables. Factor analysis using the Manova was also conducted to analyze possible significant differences between physician and nurse responses.
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Validity and reliability The Physician IVF KAP had a Cronbach’s a of 0.80 and the Nurse IVF KAP a Cronbach’s a of 0.69. Results This study included 70 participants, of them 35 (50%) were nurses and 35 (50%) were physicians, all employed in IVF clinics throughout Israel. Twenty-three (33%) were men and the rest were women. The average age of each participant was 46 (SD ¼ 8.74), ranging from 27 to 67 years of age. Most of the participants (90%) were married and the rest were divorced, single or widowed. All the participants had at least one child. Forty seven percent of them were senior gynecologists and two were residents. The average time of employment in an IVF clinic was nine years, ranging from three to 39 years (Table 1). Knowledge, attitudes and practice Most physicians and nurses (46, 67%) felt a possible connection exists between IVF and breast cancer. Fourteen (41%) of the physicians and fourteen (43%) of the nurses answered that a definitive connection between age of the patient and breast cancer incidence had not been proven (see Table 2). Fifteen (44%) of the physicians and thirteen (37%) of the nurses felt that the age limit of 45 should be maintained and not changed but that women over 40 should receive information about possible increased risk of future breast cancer incidence. Sixteen (50%)
Table 1 Sociodemographic variables. Variable
Category
Frequency
% Response
Gender
Female Male
47 23
67 33
Marital status
Single Married Divorced Widowed
1 63 5 1
1 90 7 1
Children
Yes No
70 e
100 e
Profession
Nurse Doctor
35 35
50 50
Degree
Certified Nurse BSc. MSc. MD
10 19 6 35
14 27 9 50
Professional status
Nurse Resident Physician
35 33 2
50 47 3
Working status
Full-time Part-time
31 39
44 56
Country of Origin
Israel Former U.S.S.R Europe Other
45 16 6 1
66 24 9 1
Religion
Jewish Christian Muslim
65 2 3
93 3 4
Religious affinity
Ultra Orthodox/Very Religious Religious Traditional Secular
1 17 14 38
1 24 20 54
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physicians and twenty-six (74%) nurses felt that the medical establishment should increase the level of awareness of a possible connection between IVF and breast cancer, as it is the public’s right to know. Thirty-three (97%) of physicians and thirty-two (91%) of nurses felt that patient’s request for minimal hormone exposure should be taken into account when deciding whether to conduct treatment, together with a clinical explanation as to possible treatment failure. Ten (29%) of the physicians and twenty-one (60%) of the nurses feel that limiting the number of IVF cycles should be determined by the number of risk factors that the patient has to develop breast cancer. The majority of physicians (67%) and nurses (69%) felt that the practitioner should present the possible connection to the patient. The overwhelming majority of the participants, 74% of the physicians and 69% of the nurses felt that this risk information should be added to the informed consent form in the IVF clinic. We did not find significant differences between doctors and nurses in any of the 19 questions, and we did not find significant differences in the 19 questions between various demographic subgroups. Therefore, we performed a factor analysis of the 19 questions that resulted in four scales which explained 68.5% of the variance: treatment risk and risk management; breast examination; providing the patient with relevant risk information; consideration of the patient’s needs. A total of 13 variables had significant loadings onto one of the four factors. In a comparison of physician and nurse scores using these four scales (using Manova), a significant difference was found between doctors and nurses in the practice of giving information: physicians tend to inform the clients about the connection between IVF treatment and breast cancer more than nurses do (F (1, 65) ¼ 4.301; p ¼ 0.042). Sixteen (47%) of the physicians and twelve (34.3%) of the nurses said they would discuss the possible connection between hormonal treatment and breast cancer only if the woman presented with a breast cancer risk factor and seven (21%) of the physicians and nine (25.7%) of the nurses said they would only discuss the possible connection if the patient brought up the issue. In regards to providing information on the possible connection, the majority of physicians (18, or 56%) and nurses (14, or 56%) would tell the patient that it is likely that there is a connection between hormonal treatment and breast cancer. Thirteen (38%) of the physicians said they always conduct clinical breast exams (CBE), by themselves, before proceeding with an IVF treatment, compared to thirteen (38%) of the physician participants that said they never conduct CBE prior to treatment. Twenty (59%) of the physicians reported that they always refer the patient to a surgeon for CBE. In Israel, it is the norm for breast surgeons to conduct CBE instead of the gynecologist (Israeli Ministry of Health, 2005). The nurses were asked if the physicians in their wards conduct CBE on new patients. Thirteen (37%) responded that the physician always conducts a CBE and 12 (34%) said the physician never conducts a CBE. Twenty (59%) of the physicians stated that they always refer a woman to receive a CBE by a surgeon prior to the IVF treatment. When the nurses were asked, they responded that eighteen (51%) of the physicians always refer the patient to a surgeon to receive a CBE prior to treatment. Twenty-one (61%) of the physicians said they would not begin treatment without the results of a breast exam and fifteen (43%) of the nurses concurred. Seventy one percent of both physicians and nurses said that there was an institutional protocol in place requiring that a breast exam be conducted prior to initiating IVF treatment. There was no statistically significant connection between attitudes and any of the sociodemographic variables, age, education, age at immigration, years of experience, or years working in an IVF clinic for neither nurses nor physicians.
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Discussion The survey was based on the model of the theory of reasoned action, which suggests that the attitude toward a particular object or concept influences eventual behavior, but it is not the only predictor and is influenced by a spectrum of contextually based variables (Ajzen and Fishbein, 1977; Bagozzi, 1992). In this study, both physicians and nurses felt there was potential risk for the patient but did not actually change their behavior with the patient to address her of this risk. The majority of physicians and nurses felt that there was a connection between IVF and breast cancer, despite the growing body of evidence that suggests that there is no connection between the two. They also support, in part, their current institutional protocol that requires the physician to conduct a clinical breast exam or at least refer a woman to an exam prior to initiating the treatment. However, neither the physician nor the nurse is raising the issue of possible risk with the patient herself. Approximately 40% of doctors and nurses answered that there is no definite connection between age and breast cancer incidence. Although there is a large body of evidence to suggest that IVF does not increase breast cancer risk generally, there is research supporting that IVF does increase risk for women beginning IVF treatments after the age of 30 (Katz et al., 2008) and prior to age 24 (Stewart et al., 2012). This implies that women undergoing IVF treatment at an older age may be at increased risk for developing breast cancer. It was interesting to note that both doctors and nurses thought that it is important to add the information of the possible connection between IVF and breast cancer to the informed consent before the treatment initiation (the current form does not include such information). There seems to be a gap between the professional attitudes toward the issue and actual practice. Although the majority of physicians and nurses stated that they knew there was an institutional protocol for CBE and that they themselves either examined the patient or had the woman physically examined for breast malignancies prior to the treatment, most practitioners did not discuss possible increased breast cancer risk with the patient. It was not part of the provider patient dialogue at all. This raises interesting questions as to how much providers discuss risk with their patients in general even if the provider believes there to be a risk. Communicating possible risk of a procedure to the patient can be challenging for the health professional, especially in a situation where the objective risk is unclear and the subjective outcome for the patient is also uncertain (Bogardus et al., 1999). However, the health professional may have an obligation to insure that the patient understands all of the possible risks and benefits of the procedure before deciding to commit to the treatment (Bogardus et al., 1999). Health professional assisted decision-making should help “minimize the chances of undesired consequences according to the best possible scientific evidence” (O’Connor et al., 2003, p. 736). Segev et al. (2011) proposed a pre-ART medical assessment to identify possible risk factors for maternal morbidity during pregnancy and immediately post partum for women over 40 (2011). Yet breast cancer may not be the only possible risk for women undergoing IVF procedures. Research has suggested a possible connection with endometrial and ovarian cancers (Calderon-Margalit et al., 2009). Perhaps an additional risk communication component should be added for non-pregnancy related morbidity potentially associated with IVF treatment. Although some discussion about a standardized approach for risk disclosure has been described in the literature (Bogardus et al., 1999), there is no current dialogue about standardized maternal risk disclosure for IVF treatment.
Although there has been concern among researchers and practitioners about the possible connection between IVF treatment and future breast cancer, an abundance of data asserts the lack of connection. This study suggests that nurses and physicians are still concerned about their patients’ risk enough to implement protocols that moderately assess breast cancer risk before treating the patient; however the patient is not yet part of the risk communication dialogue. Perhaps review and standardization of protocols is suggested, along with protocols for discussion of maternal risk, in general, in regards to fertility treatment. Limitations No questionnaires were found in the literature regarding the knowledge, attitudes and practices assessment of physicians and nurses regarding possible connection between IVF treatments and breast cancer. Therefore, the validity and reliability of the questionnaire was tested only in the specific study population. The study involved a convenience sample of doctors and nurses who were specifically approached by the researcher, with minimal diversity in culture, education or age.
Conclusions and implication for practice It will be beneficial for physicians and nurses to have a standardized pre ART risk assessment protocol, which would include a standardized risk discussion with the patient. Given the current research, it is advisable that every patient would sign informed consent that would include relevant information of the possible connection between IVF treatments and breast cancer. In addition, nurses working in fertility clinics are in an ideal position to engage patients in a discussion of risk assessment so that the patient may make a truly informed decision about IVF treatments. Conflict of interest statement None declared. Role of funding source No external sources of funding. Acknowledgments The authors would like to thank Aviva Yoselis of Israel Health Consulting for her editorial assistance in preparing this manuscript. Appendix A. Supplementary material Supplementary material associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ejon. 2013.10.009. References Aarons, G.A., 2005. Measuring provider attitudes toward evidence-based practice: consideration of organizational context and individual differences. Child Adolesc. Psychiatr. Clin. N. Am. 14, 255e271. Ajzen, I., Fishbein, M., 1977. Attitude-behavior relations: a theoretical analysis and review of empirical research. Psychol. Bull. 84, 888e918. Bagozzi, R.P., 1992. The self-regulation of attitudes, intentions, and behavior. Psychol. Q. 55, 178e204. Bernstein, L., 2002. Epidemiology of endocrine-related risk factors for breast cancer. J. Mammary Gland Biol. Neoplasia 7, 3e15.
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