- Email: [email protected]
What is the quality of information on social oocyte cryopreservation provided by websites of Society for Assisted Reproductive Technology member fertility clinics?
ORIGINAL ARTICLES: FERTILITY PRESERVATION
What is the quality of information on social oocyte cryopreservation provided by websites of Society for Assisted Reproductive Technology member fertility clinics? Sarit Avraham, M.D.,a Ronit Machtinger, M.D.,a Tal Cahan, M.D.,a Amit Sokolov, B.Sc.,b Catherine Racowsky, Ph.D.,c and Daniel S. Seidman, M.D., M.M.Sc.a a IVF Unit, Department of Obstetrics and Gynecology, the Chaim Sheba Medical Center, and the Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel; b Department of Statistics and Operations Research, the Raymond and Beverly Sackler Faculty of Exact Sciences, Tel Aviv University, Tel Aviv, Israel; and c Department of Obstetrics, Gynecology and Reproductive Biology, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts
Objective: To evaluate adequacy and adherence to American Society for Reproductive Medicine (ASRM) guidelines of internet information provided by Society for Assisted Reproductive Technology (SART)-affiliated clinics regarding social oocyte cryopreservation (SOC). Design: Systematic evaluation of websites of all SART member fertility clinics. Setting: The internet. Patient(s): None. Intervention(s): All websites offering SOC services were scored using a 0–13 scale, based on 10 questions designed to assess website quality and adherence to the ASRM/SART guidelines. The websites were analyzed independently by two authors. Whenever disagreement occurred, a third investigator determined the score. Main Outcome Measure(s): Scores defined website quality as excellent, R9; moderate, 5–8; or poor, %4 points. Result(s): Of the 387 clinics registered as SART members, 200 offered oocyte cryopreservation services for either medical or social reasons; 147 of these advertised SOC. The average website scores of those clinics offering SOC was 3.4 2.1 (range, 2–11) points. There was no significant difference in scores between private versus academic clinics or clinics performing more or less than 500 cycles per year. Conclusion(s): The majority of the websites do not follow the SART/ASRM guidelines for SOC, indicating that there is a need to improve the type and quality of information provided on SOC Use your smartphone by SART member websites. (Fertil SterilÒ 2014;101:222–6. Ó2014 by American Society for to scan this QR code Reproductive Medicine.) and connect to the Key Words: Nonmedical oocyte cryopreservation, internet, websites Discuss: You can discuss this article with its authors and with other ASRM members at http:// fertstertforum.com/avrahams-oocyte-cryopreservation-internet-websites-sart/
T
he ability to cryopreserve oocytes efficiently has greatly improved over the last few years with the introduction of new techniques such as vitrification (1). Consequently, the
clinical use of oocyte cryopreservation (OC) has been on the rise. The use of OC for fertility preservation of women with unique medical problems (e.g., cancer), as well as within ovum dona-
Received June 10, 2013; revised and accepted September 6, 2013; published online October 17, 2013. S.A. has nothing to disclose. R.M. has nothing to disclose. T.C. has nothing to disclose. A.S. has nothing to disclose. C.R. has nothing to disclose. D.S.S. has nothing to disclose. Reprint requests: Daniel S. Seidman, M.D., M.M.Sc., Department of Obstetrics and Gynecology, Chaim Sheba Medical Center, 52621 Tel-Hashomer, Israel (E-mail: [email protected]). Fertility and Sterility® Vol. 101, No. 1, January 2014 0015-0282/$36.00 Copyright ©2014 American Society for Reproductive Medicine, Published by Elsevier Inc. http://dx.doi.org/10.1016/j.fertnstert.2013.09.008 222
discussion forum for this article now.*
* Download a free QR code scanner by searching for “QR scanner” in your smartphone’s app store or app marketplace.
tion programs and for surplus oocyte storage, is widely accepted (1). However, the use of OC for fertility preservation among women desiring to extend their fertile years (i.e., social oocyte cryopreservation [SOC]) has remained a more controversial issue (2). The recent reports showing improved fertilization and pregnancy rates of cryopreserved mature oocytes when vitrified and warmed led the practice committees of the American Society for Reproductive Medicine VOL. 101 NO. 1 / JANUARY 2014
Fertility and Sterility® (ASRM) and the Society for Assisted Reproductive Technology (SART) to state that this technique should no longer be considered experimental (3). However, it is emphasized in the new guidelines that most of the data reported so far were derived from the experience of a few clinics with healthy young oocyte donors and limited vitrification duration (3, 4). Therefore, it is assumed that these data cannot be readily extrapolated to all clinics, different patient populations, and diverse cryopreservation protocols. Several studies suggest that success rates appear to decline with maternal age via either slow freeze or vitrification (5–7). A very recent prospective study compared IVF outcomes with vitrified oocytes versus sibling fresh oocytes in women aged 30–39 (8). The researchers showed that maternal age seemed to be the determining factor for treatment success instead of the vitrification process or the stimulation protocol, with clear advantages for younger patients. The younger group presented a statistically significant higher number of goodquality embryos and a trend towards higher implantation and clinical pregnancy rates, which was limited by the small sample size. Despite the limited number of deliveries, it seems that there is no increased risk of congenital anomalies or differences in birth weight among those born from oocyte vitrification compared with those born from fresh IVF (9). However, long-term data on developmental outcomes and safety data in diverse populations are missing. The ASRM/ SART committees concluded that in cases of elective cryopreservation to defer childbearing, the data on the safety, efficacy, cost-effectiveness, and emotional risks are insufficient to recommend SOC. Moreover, it is noted in the ASRM/SART guidelines that marketing of this technology for social purposes may give women false hope and encourage them to delay childbearing. These patients should be carefully counseled about age and clinic-specific success rates, risks, costs, and alternatives to using this approach. Earlier guidelines from the ASRM/SART practice committee in regard to advertising and marketing by assisted reproductive technology (ART) programs (10) suggest that claims made in advertising must be supported by reliable data, ‘‘success rates’’ should include live-birth data if available to avoid misleading patients, and outcomes of all initiated cycles in a specific category must be reported. In 2007, Abusief et al. (11) evaluated the compliance of SART member fertility clinic websites with ASRM/SART guidelines for general advertising of fertility treatments on websites. Adherence to guidelines was low in all categories in both private and academic clinics. General criteria for website quality assessment usually include content (reliability and accuracy), design and aesthetics (layout and interactivity), currency of information, and disclosure of author and sponsors (12). The aim of the present study was to evaluate the way SOC services are presented on the internet by SART-affiliated clinics. These regulated clinics must have accredited laboratories and report their data annually to the U.S. government through SART. We established a scoring system that assesses the main issues noted in the ASRM/SART guidelines and applied it to appraise the current quality of data presented VOL. 101 NO. 1 / JANUARY 2014
on the websites of all SART member ART clinics that offer SOC services.
MATERIALS AND METHODS During November–December 2012, we systematically evaluated all SART member fertility clinic websites, as registered in the SART official website (13). If no website was identified for a clinic, we searched the web using Google and confirmed the clinic by the name of the medical director as reported to SART. The clinics were assessed for offering OC services for medical indications, social indications, or both. In addition, we noted whether the clinic was private or had an academic affiliation and the number of cycles performed per year, as reported to SART. When OC services were not noted in the main services page of the website, we used the keywords ‘‘cryopreservation,’’ ‘‘egg freezing,’’ and ‘‘fertility preservation’’ in the website’s search engine, when available, to assure that we did not miss the availability of OC treatment. These keywords were obtained after random sites navigation. The websites that offer SOC were scored using a 0–13 point scale (Table 1), which was based on 10 questions designed to assess the quality of websites for those clinics that offer SOC services and their adherence to the ASRM guidelines described
TABLE 1 Clinic scoring system for oocyte cryopreservation services. Question
Possible score
Is the name of the clinic clearly mentioned? Is contact information given? Is graphic explanation of the oocyte freezing process given? Is an explanation of the safety of the oocyte freezing process given?
1 point
Are the source and date of the data accurately provided? Are explanations of success rates given? Are the data based on the clinic’s experience? Are the success rates based on autologous oocytes? Is the efficacy of conceiving from frozen oocytes accurately stated according to the patient’s age? Is the cost of the procedure given?
1 point
Explanation of scoring
1 point 1 point 2 points
2 points
Showing potential risks to the woman or the fetusa; presenting the potential risks to both the woman and the fetus
Pregnancy rate; live birth rate
1 point 1 point 1 point
2 points
Global pricing; elaborate pricing
a Risks to the woman: ovarian hyperstimulation syndrome must be mentioned in order to receive 1 point; risks to the fetus: it must be declared that long-term developmental risks are unknown to receive 1 point.
Avraham. SOC in SART member clinics, websites. Fertil Steril 2014.
223
ORIGINAL ARTICLE: FERTILITY PRESERVATION above. This questionnaire was discussed by all authors before evaluation of the websites and was first checked for 10 pilot websites. Each website was analyzed independently by two of the authors (S.A., T.C.). Whenever disagreement occurred, a third investigator (R.M.) evaluated the score, and the score was given according to the majority (2:1). A clinic’s website was considered excellent, in regard to SOC, if it received a score of 9 points or above; moderate if the score was 5–8; and poor if it accumulated only 4 points or less. The scores were also analyzed according to whether a clinic was private or university affiliated and by the number of cycles performed per year. Medical OC was reported according to the website selfinformation. Although this term was mostly used for cancer patients, the exact inclusion criteria for medical conditions for medical OC were not always reported.
Statistics Categorical data are presented as numbers and percentages; continuous data include mean and SDs. For categorical comparisons we used Fisher’s exact test. For continuous data of two categories we used Wilcoxon rank test or t-test when normality could be assumed; as well as Pearson’s correlation. For continuous data with three or more categories, we used analysis of variance. P< .05 was considered statistically significant; to control for increased chance of type l error due to multiple comparisons, we used Bonferroni correction.
RESULTS We identified 387 clinics registered as SART member clinics from the official site as provided by SART; 293 were private clinics and 86 were university affiliated. Of the 387 clinics, 98% had an active website, and 200 clinics offered OC services (both medical and social): 151 private and 49 with academic affiliation. Of those clinics, 147 clinics advertised SOC (Fig. 1). There was no statistical difference between the proportion of private versus academic clinics that offer some type of OC (51.5% and 57.0%, respectively). Private clinics were significantly more likely to offer SOC compared with
FIGURE 1
university-affiliated clinics, which were more likely to offer OC for medical indications only (P< .0001). Approximately 5% of both private and academic clinics failed to specify whether they offered OC for social versus medical reasons. Of the 200 websites that were evaluated, disagreement between the two investigators was found in six cases (3%). The disagreement did not exceed 1 point. The average website score of all clinics that offer SOC was 3.4 2.13 points (range, 2–11 points). Only seven (4.8%) clinics achieved an ‘‘excellent’’ (R9) score, and 21 (14.3%) reached a ‘‘moderate’’ (5–8) score. The rest of the clinics were in the ‘‘poor’’ (%4) score category. There was no significant difference in the score categories between private and university-affiliated clinics (P ¼ .345) or in the total scores (P ¼ .98). In general, most of the websites achieved relatively low scores regardless of being universityaffiliated or private clinics. For example, only 3.1% of the private clinics and none of the university-affiliated clinics mentioned the potential risks for both the woman and fetus. The data on the chances of conceiving from OC were presented as based on the clinic’s experience in only 12.5% of the private clinics and 15.8% of the university-affiliated clinics. The detailed scoring and a comparison between private and university-affiliated clinics are shown in Table 2. Data on the number of IVF cycles performed were available in 132 of the 147 clinics that offer SOC. There was no statistical difference in the average score between clinics that perform >500 cycles a year and clinics that perform less (P ¼ .12). There was also no difference in the distribution of the score categories (i.e., poor, moderate, and excellent; P ¼ .37). Larger clinics were more likely to state the chances of success according to the patient’s age than smaller clinics, but this difference was not significant after correction for multiple comparisons. Looking at the number of annually performed IVF cycles as a continuous scale, there was a significant positive correlation between the number of cycles performed and clinic website scores (Pearson correlation ¼ 0.274, P< .001). The detailed scoring and a comparison between clinics performing <500 or 500 or more cycles are shown in Table 3. Although we assumed that clinics performing more cycles per year would have more experience and data to publish, the mean website scores were similar between the groups; the only difference being that larger clinics provided more accurate information regarding the efficacy of conceiving according to patient age (P< .03).
DISCUSSION
Flow diagram showing process for identifying SART-member clinics offering SOC. Avraham. SOC in SART member clinics, websites. Fertil Steril 2014.
224
This study is, to the best of our knowledge, the first study to assess systematically the quality of information on SOC services presented on the internet by SART member fertility clinics. Our results indicate that the majority of websites do not follow the guidelines published by SART/ASRM on OC and related advertising. Although not recommended by SART (3), SOC was offered on the websites of 38% of the clinics registered as members of SART. University-affiliated clinics were significantly more likely to offer on their websites OC for medical indications only but overall failed to fulfill ASRM guidelines when SOC was offered, similar to most of the private clinics. The guidelines VOL. 101 NO. 1 / JANUARY 2014
Fertility and Sterility®
TABLE 2 Website scores and information provided by university-affiliated and private IVF units that offer SOC. Private IVF units (n [ 128) Web score, mean SD (range) Is the name of the clinic clearly mentioned? Is contact information given? Is an explanation of the safety of the oocyte freezing process given? Is explicit explanation of the oocyte freezing process given (graphic, tables)? Are explanations of success rates given? Are the source and date of the data accurately provided? Are the data based on the clinic’s experience? Are the success rates based on autologous oocytes? Is the efficacy of conceiving from frozen oocytes accurately stated according to the patient’s age? Is the cost of the procedure given?
3.4 2 (2–11) 128 (100) 127 (99) 1 point: 15 (11.7); 2 points: 4 (3.1)
University-affiliated IVF units (n [ 19) P value 3.8 2.9 (2–11) 19 (100) 19 (100) 1 point: 2 (10.5); 2 points: 0 (0)
14 (10.9) 1 point: 25 (19.5); 2 points: 15 (11.7) 22 (17.2)
3 (15.8) 1 point: 3 (15.8); 2 points: 4 (21.1) 4 (21.2)
16 (12.5) 5 (3.9) 9 (7) 1 point: 16 (12.5); 2 points: 10 (7.8)
3 (15.8) 3 (15.8) 2 (10.5) 1 point: 1 (5.3); 2 points: 3 (15.8)
.98 1.00 1.00 1.00 .46 .49 .75 .71 .07 .64 .43
Note: The Wilcoxon test was performed to test for difference in score means. Per question, the number of websites is presented and the percentage from the total is in parentheses. Fisher’s exact test was performed to test dependency on unit type; no significance was found. Avraham. SOC in SART member clinics, websites. Fertil Steril 2014.
aim to protect women from false hopes by recommending that clinics include information on the woman’s age and its possible impact on success, as well as clinic-specific success rates, risks, and costs. All of these parameters were mentioned by very few of the websites, regardless of their affiliation. Websites of clinics with >500 cycles per year tended to give more age-specific success rates, but no statistical significance was noted after correction for multiple comparisons. We found a positive correlation between the number of cycles performed per year and score on a continuous scale, but with a relatively weak Pearson coefficient. These results resemble data from a recent analysis by Keehn et al. (14) on clinic and agency websites’ adherence to ASRM guidelines on egg donors’ recruitment online. They found that most of the websites did not present risks, either short or long term. Although in the case of egg donation the patients receive a financial benefit and face a different decision-making process, SOC involves an invasive procedure for a nonguaranteed ‘‘insur-
ance premium’’ payout (15). A study that evaluated websites of clinics on the Centers for Disease Control provider list showed that websites where preimplantation genetic diagnosis (PGD) was noted tended to describe the benefits of PGD more than the risks involved (16). Before making a decision regarding SOC, interested women need to obtain reliable information to make a balanced risk-benefit decision. One could claim that such women are likely to be referred to a fertility specialist who would provide this information. However, there is evidence that only a minority of patients in need of specific health information consult their physician before first going online (17). In regard to SOC, this may bias the patients in choosing a clinic, for example, one that does not highlight the risks or a clinic that cites the best success rates. The importance of counseling regarding accurate success rates on the decision-making process in relation to SOC can be estimated from data gathered in an online survey among
TABLE 3 Website information and score according to the number of cycles per year reported to SART (2012).
Web score, mean SD (range) Is an explanation of the safety of the oocyte freezing process given? Is graphic explanation of the oocyte freezing process given? Are explanations of success rates given? Are the source and date of the data accurately provided? Are the data based on the clinic’s experience? Are the success rates based on autologous oocytes? Is the efficacy of conceiving from frozen oocytes accurately stated according to the patient’s age? Is the cost of the procedure given?
£500 cycles (n [ 81)
>500 cycles (n [51)
P value
3.2 1.8 (2–11) 1 point: 11 (13.6); 2 points: 2 (2.5)
3.8 2.4 (2–11) 1 point: 4 (7.8); 2 points: 2 (3.9)
.12 .58
8 (15.7)
.26
1 point: 10 (19.6); 2 points: 10 (19.6) 12 (23.5)
.26 .16
9 (17.6) 5 (9.8) 7 (13.7)
.17 .11 .03
1 point: 8 (15.7); 2 points: 3 (5.9)
.43
7 (8.6) 1 point: 16 (19.8); 2 points: 8 (9.9) 11 (13.6) 7 (8.6) 2 (2.5) 2 (2.5) 1 point: 7 (8.6); 2 points: 8 (9.9)
Note: The Student’s t-test was performed to test for difference in score means. Per question, the number of websites is presented and the percentage from the total is in parentheses. Fisher’s exact test was performed to test dependency on the unit cycles category; no significance was found after correction for multiple comparisons. Avraham. SOC in SART member clinics, websites. Fertil Steril 2014.
VOL. 101 NO. 1 / JANUARY 2014
225
ORIGINAL ARTICLE: FERTILITY PRESERVATION female university students in northern California (18). Fiftythree percent of the students said they would consider SOC if informed that their ovarian reserve was very low. Only 29% of the participants said they would consider stopping educational or professional pursuits to focus on conceiving. Participants believed that the decline in ovarian reserve starts later than it actually does and that infertility treatments were highly effective regardless of how severe the depletion of egg supply. It is apparent that lack of reported success rates or even presenting general success rates that are not age related on the clinics’ websites, in combination with the low awareness, might encourage women to falsely believe they can indefinitely delay childbearing through OC. More specific presentation of success rates according to age could help women to make an informed assessment and make the right decision at the right time. The methodology of the present study has several limitations. Scoring of websites may vary because of the heterogeneous way that information is presented. The accuracy of the search may occasionally be affected owing to a website’s multilayer structure that can require data mining that may lead to increased inter- and intraobserver variability. This variability is an innate default in a quality-based scoring system, even in some of the most widely accepted scoring systems, such as the Apgar score for infant assessment (19). We tried to minimize this variability by scoring all sites by two independent researchers and limiting the search time to 10 minutes. The 10-minute time frame was decided after a pilot analysis by the researchers. Our scoring system can be used in future studies to assess websites that are present on free search engines such as Google or Bing, which might be those websites that are visited by the average patient. We assume that a free search would present less regulated clinics that may be less compliant with ASRM guidelines, as was demonstrated in a study by Marriott and colleagues (12). Our findings suggest that SART member clinics should make a greater effort to ensure that the content of their websites complies with the published ASRM/SART guidelines. Future studies should determine the quality of the data provided on the web by non-SART member clinics, agencies, and egg banks. In conclusion, to our knowledge this is the first study to evaluate information provided on the internet by SART member clinics. We found that most of the clinics do not follow the guidelines provided by SART/ASRM. Since SOC is becoming more widely used and is currently offered by many regulated and nonregulated ART units, there is an urgent need to continue monitoring the quality of the information provided to women considering SOC.
2. 3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
REFERENCES 1.
226
Cobo A, Diaz C. Clinical application of oocyte vitrification: a systematic review and meta-analysis of randomized controlled trials. Fertil Steril 2011;96:277–85.
19.
Sheldon T. Dutch medical associations support freezing oocytes for nonmedical reasons. Br Med J 2010;341:c4823. The practice committees of the American Society for Reproductive Medicine and the Society for Assisted Reproductive Technology. Mature oocyte cryopreservation: a guideline. Fertil Steril 2013;99:37–43. Sole M, Santalo J, Boada M, Clua E, Rodriguez F, Martinez F, et al. How does vitrification affect oocyte viability in oocyte donation cycles? A prospective study to compare outcomes achieved with fresh versus vitrified sibling oocytes. Hum Reprod 2013;28:2087–92. Borini A, Levi Setti PE, Anserini P, De Luca R, De Santis L, Porcu E, et al. Multicenter observational study on slow-cooling oocyte cryopreservation: clinical outcome. Fertil Steril 2010;94:1662–8. Ubaldi F, Anniballo R, Romano S, Baroni E, Albricci L, Colamaria S, et al. Cumulative ongoing pregnancy rate achieved with oocyte vitrification and cleavage stage transfer without embryo selection in a standard infertility program. Hum Reprod 2010;25:1199–205. Cil AP, Banq H, Oktay K. Age-specific probability of live birth with oocyte cryopreservation: an individual patient data meta-analysis. Fertil Steril 2013; 100:492–9. Chang CC, Elliott TA, Wright G, Shapiro DB, Toledo AA, Nagy ZP. Prospective controlled study to evaluate laboratory and clinical outcomes of oocyte vitrification obtained in in vitro fertilization patients aged 30 to 39 years. Fertil Steril 2013;99:1891–7. Chain RC, Huang JY, Tan SL, Lucena E, Saa A, Rojas A, et al. Obstetric and perinatal outcome in 200 infants conceived from vitrified oocytes. Reprod Biomed Online 2008;16:608–10. The Practice Committee of the Society for Assisted Reproductive Technology and the American Society for Reproductive Medicine. Guidelines for advertising by ART programs. Fertil Steril 2004;82(Suppl 1):s3. Abusief ME, Hornstein MD, Jain T. Assessment of United States fertility clinic websites according to the American Society for Reproductive Medicine(ASRM)/Society for Assisted Reproductive Technology (SART) guidelines. Fertil Steril 2007;87:88–92. Marriott JV, Stec P, El-Toukhy T, Khalaf Y, Braude P, Coomarasamy A. Infertility information on the World Wide Web: a cross-sectional survey of quality of infertility information on the internet in the UK. Hum Reprod 2008;23: 1520–5. Society for Assisted Reproductive Technology. IVF success rates. SART national summary. Available at: http://www.sart.org/find_frm.html. Last accessed October 9, 2013. Keehn J, Holwell E, Abdul-Karim R, Chin LJ, Leu CS, Sauer MV, Klitzman R. Recruiting egg donors online: an analysis of in vitro fertilization clinic and agency websites’ adherence to American Society for Reproductive Medicine guidelines. Fertil Steril 2012;98:995–1000. Lockwood GM. Social egg freezing: the prospect of reproductive ‘‘immortality’’ or a dangerous delusion? Reprod Biomed Online 2011; 23:334–40. Klitzman R, Zolovska B, Folberth W, Sauer MV, Chung W, Appelbaum P. Preimplantation Genetic Diagnosis (PGD) on IVF websites: presentation of risks, benefits and other information. Fertil Steril 2009;92:1276–86. Hesse BW, Nelson DE, Kreps GL, Croyle RT, Arora NK, Rimer BK, et al. Trust and sources of health information: the impact of the internet and its implications for health care providers: findings from the first Health information National Trends Survey. Arch Intern Med 2005;165:2618–24. Bavan B, Porziq E, Baker VL. An assessment of female university students’ attitudes toward screening technologies for ovarian reserve. Fertil Steril 2011;96:1195–9. O’Donnell CP, Kamlin CO, Davis PG, Carlin JB, Morley CJ. Interobserver variability of the 5-minute Apgar score. J Pediatr 2006;149:486–9.
VOL. 101 NO. 1 / JANUARY 2014
What is the quality of information on social oocyte cryopreservation provided by websites of Society for Assisted Reproductive Technology member fertility clinics? Sarit Avraham, M.D.,a Ronit Machtinger, M.D.,a Tal Cahan, M.D.,a Amit Sokolov, B.Sc.,b Catherine Racowsky, Ph.D.,c and Daniel S. Seidman, M.D., M.M.Sc.a a IVF Unit, Department of Obstetrics and Gynecology, the Chaim Sheba Medical Center, and the Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel; b Department of Statistics and Operations Research, the Raymond and Beverly Sackler Faculty of Exact Sciences, Tel Aviv University, Tel Aviv, Israel; and c Department of Obstetrics, Gynecology and Reproductive Biology, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts
Objective: To evaluate adequacy and adherence to American Society for Reproductive Medicine (ASRM) guidelines of internet information provided by Society for Assisted Reproductive Technology (SART)-affiliated clinics regarding social oocyte cryopreservation (SOC). Design: Systematic evaluation of websites of all SART member fertility clinics. Setting: The internet. Patient(s): None. Intervention(s): All websites offering SOC services were scored using a 0–13 scale, based on 10 questions designed to assess website quality and adherence to the ASRM/SART guidelines. The websites were analyzed independently by two authors. Whenever disagreement occurred, a third investigator determined the score. Main Outcome Measure(s): Scores defined website quality as excellent, R9; moderate, 5–8; or poor, %4 points. Result(s): Of the 387 clinics registered as SART members, 200 offered oocyte cryopreservation services for either medical or social reasons; 147 of these advertised SOC. The average website scores of those clinics offering SOC was 3.4 2.1 (range, 2–11) points. There was no significant difference in scores between private versus academic clinics or clinics performing more or less than 500 cycles per year. Conclusion(s): The majority of the websites do not follow the SART/ASRM guidelines for SOC, indicating that there is a need to improve the type and quality of information provided on SOC Use your smartphone by SART member websites. (Fertil SterilÒ 2014;101:222–6. Ó2014 by American Society for to scan this QR code Reproductive Medicine.) and connect to the Key Words: Nonmedical oocyte cryopreservation, internet, websites Discuss: You can discuss this article with its authors and with other ASRM members at http:// fertstertforum.com/avrahams-oocyte-cryopreservation-internet-websites-sart/
T
he ability to cryopreserve oocytes efficiently has greatly improved over the last few years with the introduction of new techniques such as vitrification (1). Consequently, the
clinical use of oocyte cryopreservation (OC) has been on the rise. The use of OC for fertility preservation of women with unique medical problems (e.g., cancer), as well as within ovum dona-
Received June 10, 2013; revised and accepted September 6, 2013; published online October 17, 2013. S.A. has nothing to disclose. R.M. has nothing to disclose. T.C. has nothing to disclose. A.S. has nothing to disclose. C.R. has nothing to disclose. D.S.S. has nothing to disclose. Reprint requests: Daniel S. Seidman, M.D., M.M.Sc., Department of Obstetrics and Gynecology, Chaim Sheba Medical Center, 52621 Tel-Hashomer, Israel (E-mail: [email protected]). Fertility and Sterility® Vol. 101, No. 1, January 2014 0015-0282/$36.00 Copyright ©2014 American Society for Reproductive Medicine, Published by Elsevier Inc. http://dx.doi.org/10.1016/j.fertnstert.2013.09.008 222
discussion forum for this article now.*
* Download a free QR code scanner by searching for “QR scanner” in your smartphone’s app store or app marketplace.
tion programs and for surplus oocyte storage, is widely accepted (1). However, the use of OC for fertility preservation among women desiring to extend their fertile years (i.e., social oocyte cryopreservation [SOC]) has remained a more controversial issue (2). The recent reports showing improved fertilization and pregnancy rates of cryopreserved mature oocytes when vitrified and warmed led the practice committees of the American Society for Reproductive Medicine VOL. 101 NO. 1 / JANUARY 2014
Fertility and Sterility® (ASRM) and the Society for Assisted Reproductive Technology (SART) to state that this technique should no longer be considered experimental (3). However, it is emphasized in the new guidelines that most of the data reported so far were derived from the experience of a few clinics with healthy young oocyte donors and limited vitrification duration (3, 4). Therefore, it is assumed that these data cannot be readily extrapolated to all clinics, different patient populations, and diverse cryopreservation protocols. Several studies suggest that success rates appear to decline with maternal age via either slow freeze or vitrification (5–7). A very recent prospective study compared IVF outcomes with vitrified oocytes versus sibling fresh oocytes in women aged 30–39 (8). The researchers showed that maternal age seemed to be the determining factor for treatment success instead of the vitrification process or the stimulation protocol, with clear advantages for younger patients. The younger group presented a statistically significant higher number of goodquality embryos and a trend towards higher implantation and clinical pregnancy rates, which was limited by the small sample size. Despite the limited number of deliveries, it seems that there is no increased risk of congenital anomalies or differences in birth weight among those born from oocyte vitrification compared with those born from fresh IVF (9). However, long-term data on developmental outcomes and safety data in diverse populations are missing. The ASRM/ SART committees concluded that in cases of elective cryopreservation to defer childbearing, the data on the safety, efficacy, cost-effectiveness, and emotional risks are insufficient to recommend SOC. Moreover, it is noted in the ASRM/SART guidelines that marketing of this technology for social purposes may give women false hope and encourage them to delay childbearing. These patients should be carefully counseled about age and clinic-specific success rates, risks, costs, and alternatives to using this approach. Earlier guidelines from the ASRM/SART practice committee in regard to advertising and marketing by assisted reproductive technology (ART) programs (10) suggest that claims made in advertising must be supported by reliable data, ‘‘success rates’’ should include live-birth data if available to avoid misleading patients, and outcomes of all initiated cycles in a specific category must be reported. In 2007, Abusief et al. (11) evaluated the compliance of SART member fertility clinic websites with ASRM/SART guidelines for general advertising of fertility treatments on websites. Adherence to guidelines was low in all categories in both private and academic clinics. General criteria for website quality assessment usually include content (reliability and accuracy), design and aesthetics (layout and interactivity), currency of information, and disclosure of author and sponsors (12). The aim of the present study was to evaluate the way SOC services are presented on the internet by SART-affiliated clinics. These regulated clinics must have accredited laboratories and report their data annually to the U.S. government through SART. We established a scoring system that assesses the main issues noted in the ASRM/SART guidelines and applied it to appraise the current quality of data presented VOL. 101 NO. 1 / JANUARY 2014
on the websites of all SART member ART clinics that offer SOC services.
MATERIALS AND METHODS During November–December 2012, we systematically evaluated all SART member fertility clinic websites, as registered in the SART official website (13). If no website was identified for a clinic, we searched the web using Google and confirmed the clinic by the name of the medical director as reported to SART. The clinics were assessed for offering OC services for medical indications, social indications, or both. In addition, we noted whether the clinic was private or had an academic affiliation and the number of cycles performed per year, as reported to SART. When OC services were not noted in the main services page of the website, we used the keywords ‘‘cryopreservation,’’ ‘‘egg freezing,’’ and ‘‘fertility preservation’’ in the website’s search engine, when available, to assure that we did not miss the availability of OC treatment. These keywords were obtained after random sites navigation. The websites that offer SOC were scored using a 0–13 point scale (Table 1), which was based on 10 questions designed to assess the quality of websites for those clinics that offer SOC services and their adherence to the ASRM guidelines described
TABLE 1 Clinic scoring system for oocyte cryopreservation services. Question
Possible score
Is the name of the clinic clearly mentioned? Is contact information given? Is graphic explanation of the oocyte freezing process given? Is an explanation of the safety of the oocyte freezing process given?
1 point
Are the source and date of the data accurately provided? Are explanations of success rates given? Are the data based on the clinic’s experience? Are the success rates based on autologous oocytes? Is the efficacy of conceiving from frozen oocytes accurately stated according to the patient’s age? Is the cost of the procedure given?
1 point
Explanation of scoring
1 point 1 point 2 points
2 points
Showing potential risks to the woman or the fetusa; presenting the potential risks to both the woman and the fetus
Pregnancy rate; live birth rate
1 point 1 point 1 point
2 points
Global pricing; elaborate pricing
a Risks to the woman: ovarian hyperstimulation syndrome must be mentioned in order to receive 1 point; risks to the fetus: it must be declared that long-term developmental risks are unknown to receive 1 point.
Avraham. SOC in SART member clinics, websites. Fertil Steril 2014.
223
ORIGINAL ARTICLE: FERTILITY PRESERVATION above. This questionnaire was discussed by all authors before evaluation of the websites and was first checked for 10 pilot websites. Each website was analyzed independently by two of the authors (S.A., T.C.). Whenever disagreement occurred, a third investigator (R.M.) evaluated the score, and the score was given according to the majority (2:1). A clinic’s website was considered excellent, in regard to SOC, if it received a score of 9 points or above; moderate if the score was 5–8; and poor if it accumulated only 4 points or less. The scores were also analyzed according to whether a clinic was private or university affiliated and by the number of cycles performed per year. Medical OC was reported according to the website selfinformation. Although this term was mostly used for cancer patients, the exact inclusion criteria for medical conditions for medical OC were not always reported.
Statistics Categorical data are presented as numbers and percentages; continuous data include mean and SDs. For categorical comparisons we used Fisher’s exact test. For continuous data of two categories we used Wilcoxon rank test or t-test when normality could be assumed; as well as Pearson’s correlation. For continuous data with three or more categories, we used analysis of variance. P< .05 was considered statistically significant; to control for increased chance of type l error due to multiple comparisons, we used Bonferroni correction.
RESULTS We identified 387 clinics registered as SART member clinics from the official site as provided by SART; 293 were private clinics and 86 were university affiliated. Of the 387 clinics, 98% had an active website, and 200 clinics offered OC services (both medical and social): 151 private and 49 with academic affiliation. Of those clinics, 147 clinics advertised SOC (Fig. 1). There was no statistical difference between the proportion of private versus academic clinics that offer some type of OC (51.5% and 57.0%, respectively). Private clinics were significantly more likely to offer SOC compared with
FIGURE 1
university-affiliated clinics, which were more likely to offer OC for medical indications only (P< .0001). Approximately 5% of both private and academic clinics failed to specify whether they offered OC for social versus medical reasons. Of the 200 websites that were evaluated, disagreement between the two investigators was found in six cases (3%). The disagreement did not exceed 1 point. The average website score of all clinics that offer SOC was 3.4 2.13 points (range, 2–11 points). Only seven (4.8%) clinics achieved an ‘‘excellent’’ (R9) score, and 21 (14.3%) reached a ‘‘moderate’’ (5–8) score. The rest of the clinics were in the ‘‘poor’’ (%4) score category. There was no significant difference in the score categories between private and university-affiliated clinics (P ¼ .345) or in the total scores (P ¼ .98). In general, most of the websites achieved relatively low scores regardless of being universityaffiliated or private clinics. For example, only 3.1% of the private clinics and none of the university-affiliated clinics mentioned the potential risks for both the woman and fetus. The data on the chances of conceiving from OC were presented as based on the clinic’s experience in only 12.5% of the private clinics and 15.8% of the university-affiliated clinics. The detailed scoring and a comparison between private and university-affiliated clinics are shown in Table 2. Data on the number of IVF cycles performed were available in 132 of the 147 clinics that offer SOC. There was no statistical difference in the average score between clinics that perform >500 cycles a year and clinics that perform less (P ¼ .12). There was also no difference in the distribution of the score categories (i.e., poor, moderate, and excellent; P ¼ .37). Larger clinics were more likely to state the chances of success according to the patient’s age than smaller clinics, but this difference was not significant after correction for multiple comparisons. Looking at the number of annually performed IVF cycles as a continuous scale, there was a significant positive correlation between the number of cycles performed and clinic website scores (Pearson correlation ¼ 0.274, P< .001). The detailed scoring and a comparison between clinics performing <500 or 500 or more cycles are shown in Table 3. Although we assumed that clinics performing more cycles per year would have more experience and data to publish, the mean website scores were similar between the groups; the only difference being that larger clinics provided more accurate information regarding the efficacy of conceiving according to patient age (P< .03).
DISCUSSION
Flow diagram showing process for identifying SART-member clinics offering SOC. Avraham. SOC in SART member clinics, websites. Fertil Steril 2014.
224
This study is, to the best of our knowledge, the first study to assess systematically the quality of information on SOC services presented on the internet by SART member fertility clinics. Our results indicate that the majority of websites do not follow the guidelines published by SART/ASRM on OC and related advertising. Although not recommended by SART (3), SOC was offered on the websites of 38% of the clinics registered as members of SART. University-affiliated clinics were significantly more likely to offer on their websites OC for medical indications only but overall failed to fulfill ASRM guidelines when SOC was offered, similar to most of the private clinics. The guidelines VOL. 101 NO. 1 / JANUARY 2014
Fertility and Sterility®
TABLE 2 Website scores and information provided by university-affiliated and private IVF units that offer SOC. Private IVF units (n [ 128) Web score, mean SD (range) Is the name of the clinic clearly mentioned? Is contact information given? Is an explanation of the safety of the oocyte freezing process given? Is explicit explanation of the oocyte freezing process given (graphic, tables)? Are explanations of success rates given? Are the source and date of the data accurately provided? Are the data based on the clinic’s experience? Are the success rates based on autologous oocytes? Is the efficacy of conceiving from frozen oocytes accurately stated according to the patient’s age? Is the cost of the procedure given?
3.4 2 (2–11) 128 (100) 127 (99) 1 point: 15 (11.7); 2 points: 4 (3.1)
University-affiliated IVF units (n [ 19) P value 3.8 2.9 (2–11) 19 (100) 19 (100) 1 point: 2 (10.5); 2 points: 0 (0)
14 (10.9) 1 point: 25 (19.5); 2 points: 15 (11.7) 22 (17.2)
3 (15.8) 1 point: 3 (15.8); 2 points: 4 (21.1) 4 (21.2)
16 (12.5) 5 (3.9) 9 (7) 1 point: 16 (12.5); 2 points: 10 (7.8)
3 (15.8) 3 (15.8) 2 (10.5) 1 point: 1 (5.3); 2 points: 3 (15.8)
.98 1.00 1.00 1.00 .46 .49 .75 .71 .07 .64 .43
Note: The Wilcoxon test was performed to test for difference in score means. Per question, the number of websites is presented and the percentage from the total is in parentheses. Fisher’s exact test was performed to test dependency on unit type; no significance was found. Avraham. SOC in SART member clinics, websites. Fertil Steril 2014.
aim to protect women from false hopes by recommending that clinics include information on the woman’s age and its possible impact on success, as well as clinic-specific success rates, risks, and costs. All of these parameters were mentioned by very few of the websites, regardless of their affiliation. Websites of clinics with >500 cycles per year tended to give more age-specific success rates, but no statistical significance was noted after correction for multiple comparisons. We found a positive correlation between the number of cycles performed per year and score on a continuous scale, but with a relatively weak Pearson coefficient. These results resemble data from a recent analysis by Keehn et al. (14) on clinic and agency websites’ adherence to ASRM guidelines on egg donors’ recruitment online. They found that most of the websites did not present risks, either short or long term. Although in the case of egg donation the patients receive a financial benefit and face a different decision-making process, SOC involves an invasive procedure for a nonguaranteed ‘‘insur-
ance premium’’ payout (15). A study that evaluated websites of clinics on the Centers for Disease Control provider list showed that websites where preimplantation genetic diagnosis (PGD) was noted tended to describe the benefits of PGD more than the risks involved (16). Before making a decision regarding SOC, interested women need to obtain reliable information to make a balanced risk-benefit decision. One could claim that such women are likely to be referred to a fertility specialist who would provide this information. However, there is evidence that only a minority of patients in need of specific health information consult their physician before first going online (17). In regard to SOC, this may bias the patients in choosing a clinic, for example, one that does not highlight the risks or a clinic that cites the best success rates. The importance of counseling regarding accurate success rates on the decision-making process in relation to SOC can be estimated from data gathered in an online survey among
TABLE 3 Website information and score according to the number of cycles per year reported to SART (2012).
Web score, mean SD (range) Is an explanation of the safety of the oocyte freezing process given? Is graphic explanation of the oocyte freezing process given? Are explanations of success rates given? Are the source and date of the data accurately provided? Are the data based on the clinic’s experience? Are the success rates based on autologous oocytes? Is the efficacy of conceiving from frozen oocytes accurately stated according to the patient’s age? Is the cost of the procedure given?
£500 cycles (n [ 81)
>500 cycles (n [51)
P value
3.2 1.8 (2–11) 1 point: 11 (13.6); 2 points: 2 (2.5)
3.8 2.4 (2–11) 1 point: 4 (7.8); 2 points: 2 (3.9)
.12 .58
8 (15.7)
.26
1 point: 10 (19.6); 2 points: 10 (19.6) 12 (23.5)
.26 .16
9 (17.6) 5 (9.8) 7 (13.7)
.17 .11 .03
1 point: 8 (15.7); 2 points: 3 (5.9)
.43
7 (8.6) 1 point: 16 (19.8); 2 points: 8 (9.9) 11 (13.6) 7 (8.6) 2 (2.5) 2 (2.5) 1 point: 7 (8.6); 2 points: 8 (9.9)
Note: The Student’s t-test was performed to test for difference in score means. Per question, the number of websites is presented and the percentage from the total is in parentheses. Fisher’s exact test was performed to test dependency on the unit cycles category; no significance was found after correction for multiple comparisons. Avraham. SOC in SART member clinics, websites. Fertil Steril 2014.
VOL. 101 NO. 1 / JANUARY 2014
225
ORIGINAL ARTICLE: FERTILITY PRESERVATION female university students in northern California (18). Fiftythree percent of the students said they would consider SOC if informed that their ovarian reserve was very low. Only 29% of the participants said they would consider stopping educational or professional pursuits to focus on conceiving. Participants believed that the decline in ovarian reserve starts later than it actually does and that infertility treatments were highly effective regardless of how severe the depletion of egg supply. It is apparent that lack of reported success rates or even presenting general success rates that are not age related on the clinics’ websites, in combination with the low awareness, might encourage women to falsely believe they can indefinitely delay childbearing through OC. More specific presentation of success rates according to age could help women to make an informed assessment and make the right decision at the right time. The methodology of the present study has several limitations. Scoring of websites may vary because of the heterogeneous way that information is presented. The accuracy of the search may occasionally be affected owing to a website’s multilayer structure that can require data mining that may lead to increased inter- and intraobserver variability. This variability is an innate default in a quality-based scoring system, even in some of the most widely accepted scoring systems, such as the Apgar score for infant assessment (19). We tried to minimize this variability by scoring all sites by two independent researchers and limiting the search time to 10 minutes. The 10-minute time frame was decided after a pilot analysis by the researchers. Our scoring system can be used in future studies to assess websites that are present on free search engines such as Google or Bing, which might be those websites that are visited by the average patient. We assume that a free search would present less regulated clinics that may be less compliant with ASRM guidelines, as was demonstrated in a study by Marriott and colleagues (12). Our findings suggest that SART member clinics should make a greater effort to ensure that the content of their websites complies with the published ASRM/SART guidelines. Future studies should determine the quality of the data provided on the web by non-SART member clinics, agencies, and egg banks. In conclusion, to our knowledge this is the first study to evaluate information provided on the internet by SART member clinics. We found that most of the clinics do not follow the guidelines provided by SART/ASRM. Since SOC is becoming more widely used and is currently offered by many regulated and nonregulated ART units, there is an urgent need to continue monitoring the quality of the information provided to women considering SOC.
2. 3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
REFERENCES 1.
226
Cobo A, Diaz C. Clinical application of oocyte vitrification: a systematic review and meta-analysis of randomized controlled trials. Fertil Steril 2011;96:277–85.
19.
Sheldon T. Dutch medical associations support freezing oocytes for nonmedical reasons. Br Med J 2010;341:c4823. The practice committees of the American Society for Reproductive Medicine and the Society for Assisted Reproductive Technology. Mature oocyte cryopreservation: a guideline. Fertil Steril 2013;99:37–43. Sole M, Santalo J, Boada M, Clua E, Rodriguez F, Martinez F, et al. How does vitrification affect oocyte viability in oocyte donation cycles? A prospective study to compare outcomes achieved with fresh versus vitrified sibling oocytes. Hum Reprod 2013;28:2087–92. Borini A, Levi Setti PE, Anserini P, De Luca R, De Santis L, Porcu E, et al. Multicenter observational study on slow-cooling oocyte cryopreservation: clinical outcome. Fertil Steril 2010;94:1662–8. Ubaldi F, Anniballo R, Romano S, Baroni E, Albricci L, Colamaria S, et al. Cumulative ongoing pregnancy rate achieved with oocyte vitrification and cleavage stage transfer without embryo selection in a standard infertility program. Hum Reprod 2010;25:1199–205. Cil AP, Banq H, Oktay K. Age-specific probability of live birth with oocyte cryopreservation: an individual patient data meta-analysis. Fertil Steril 2013; 100:492–9. Chang CC, Elliott TA, Wright G, Shapiro DB, Toledo AA, Nagy ZP. Prospective controlled study to evaluate laboratory and clinical outcomes of oocyte vitrification obtained in in vitro fertilization patients aged 30 to 39 years. Fertil Steril 2013;99:1891–7. Chain RC, Huang JY, Tan SL, Lucena E, Saa A, Rojas A, et al. Obstetric and perinatal outcome in 200 infants conceived from vitrified oocytes. Reprod Biomed Online 2008;16:608–10. The Practice Committee of the Society for Assisted Reproductive Technology and the American Society for Reproductive Medicine. Guidelines for advertising by ART programs. Fertil Steril 2004;82(Suppl 1):s3. Abusief ME, Hornstein MD, Jain T. Assessment of United States fertility clinic websites according to the American Society for Reproductive Medicine(ASRM)/Society for Assisted Reproductive Technology (SART) guidelines. Fertil Steril 2007;87:88–92. Marriott JV, Stec P, El-Toukhy T, Khalaf Y, Braude P, Coomarasamy A. Infertility information on the World Wide Web: a cross-sectional survey of quality of infertility information on the internet in the UK. Hum Reprod 2008;23: 1520–5. Society for Assisted Reproductive Technology. IVF success rates. SART national summary. Available at: http://www.sart.org/find_frm.html. Last accessed October 9, 2013. Keehn J, Holwell E, Abdul-Karim R, Chin LJ, Leu CS, Sauer MV, Klitzman R. Recruiting egg donors online: an analysis of in vitro fertilization clinic and agency websites’ adherence to American Society for Reproductive Medicine guidelines. Fertil Steril 2012;98:995–1000. Lockwood GM. Social egg freezing: the prospect of reproductive ‘‘immortality’’ or a dangerous delusion? Reprod Biomed Online 2011; 23:334–40. Klitzman R, Zolovska B, Folberth W, Sauer MV, Chung W, Appelbaum P. Preimplantation Genetic Diagnosis (PGD) on IVF websites: presentation of risks, benefits and other information. Fertil Steril 2009;92:1276–86. Hesse BW, Nelson DE, Kreps GL, Croyle RT, Arora NK, Rimer BK, et al. Trust and sources of health information: the impact of the internet and its implications for health care providers: findings from the first Health information National Trends Survey. Arch Intern Med 2005;165:2618–24. Bavan B, Porziq E, Baker VL. An assessment of female university students’ attitudes toward screening technologies for ovarian reserve. Fertil Steril 2011;96:1195–9. O’Donnell CP, Kamlin CO, Davis PG, Carlin JB, Morley CJ. Interobserver variability of the 5-minute Apgar score. J Pediatr 2006;149:486–9.
VOL. 101 NO. 1 / JANUARY 2014