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Embryo transfer techniques: an American Society for Reproductive Medicine survey of current Society for Assisted Reproductive Technology practices

      Objective

      To better understand practice patterns and opportunities for standardization of ET.

      Design

      Cross-sectional survey.

      Setting

      Not applicable.

      Patient(s)

      Not applicable.

      Intervention(s)

      An anonymous 82-question survey was emailed to the medical directors of 286 Society for Assisted Reproductive Technology member IVF practices. A follow-up survey composed of three questions specific to ET technique was emailed to the same medical directors. Descriptive statistics of the results were compiled.

      Main Outcome Measure(s)

      The survey assessed policies, protocols, restrictions, and specifics pertinent to the technique of ET.

      Result(s)

      There were 117 (41%) responses; 32% practice in academic settings and 68% in private practice. Responders were experienced clinicians, half of whom had performed <10 procedures during training. Ninety-eight percent of practices allowed all practitioners to perform ET; half did not follow a standardized ET technique. Multiple steps in the ET process were identified as “highly conserved;” others demonstrated discordance. ET technique is divided among [1] trial transfer followed immediately with ET (40%); [2] afterload transfer (30%); and [3] direct transfer without prior trial or afterload (27%). Embryos are discharged in the upper (66%) and middle thirds (29%) of the endometrial cavity and not closer than 1–1.5 cm from fundus (87%). Details of each step were reported and allowed the development of a “common” practice ET procedure.

      Conclusion(s)

      ET training and practices vary widely. Improved training and standardization based on outcomes data and best practices are warranted. A common practice procedure is suggested for validation by a systematic literature review.

      Key Words

      Discuss: You can discuss this article with its authors and with other ASRM members at https://www.fertstertdialog.com/users/16110-fertility-and-sterility/posts/12493-22790
      In a health care environment increasingly attentive to quality surveillance, assisted reproductive technology (ART) has been an innovative leader in outcomes reporting. Following the Fertility Clinic Success Rate and Certification Act of 1992, all clinics involved with IVF are required to provide pregnancy outcome data to the Centers for Disease Control and Prevention (CDC). Since 1987 when Society for Assisted Reproductive Technology (SART) and 1997 when the CDC began to report these outcomes, success rates for various types of clinics—large, small, academic, private—have improved significantly (
      • Sunderam S.
      • Kissin D.M.
      • Crawford S.B.
      • Folger S.G.
      • Jamieson D.J.
      • Warner L.
      • et al.
      Assisted reproductive technology surveillance—United States, 2013.
      ). The last 30 years have borne witness to significant advances in the field of assisted reproduction, with many portions of the process having undergone improvement. However, ET, the critical final step in an IVF cycle, has remained largely technically unchanged since first described in 1984 (
      • Edwards R.G.
      • Fishel S.B.
      • Cohen J.
      • Fehilly C.B.
      • Purdy J.M.
      • Slater J.M.
      • et al.
      Factors influencing the success of in vitro fertilization for alleviating human infertility.
      ).
      The goal of a successful ET is to deliver the embryo(s) atraumatically to a location within the endometrial cavity that maximizes the chance of implantation. In general, there is no universal protocol for ET. While there has been much effort to study the association between various steps and specifics to ET with pregnancy outcomes (
      • Mansour R.
      • Aboulghar M.
      • Serour G.
      Dummy embryo transfer: a technique that minimizes the problems of embryo transfer and improves the pregnancy rate in human in vitro fertilization.
      ,
      • Englert Y.
      • Puissant F.
      • Camus M.
      • Van Hoeck J.
      • Leroy F.
      Clinical study on embryo transfer after human in vitro fertilization.
      ,
      • Tomás C.
      • Tikkinen K.
      • Tuomivaara L.
      • Tapanainen J.S.
      • Martikainen H.
      The degree of difficulty of embryo transfer is an independent factor for predicting pregnancy.
      ,
      • Lesny P.
      • Killick S.R.
      • Tetlow R.L.
      • Robinson J.
      • Maguiness S.D.
      Embryo transfer—can we learn anything new from the observation of junctional zone contractions?.
      ,
      • Fanchin R.
      • Righini C.
      • Olivennes F.
      • Taylor S.
      • de Ziegler D.
      • Frydman R.
      Uterine contractions at the time of embryo transfer alter pregnancy rates after in-vitro fertilization.
      ,
      • Strickler R.C.
      • Christianson C.
      • Crane J.P.
      • Curato A.
      • Knight A.B.
      • Yang V.
      Ultrasound guidance for human embryo transfer.
      ,
      • Brown J.
      • Buckingham K.
      • Buckett W.
      • Abou-Setta A.M.
      Ultrasound versus “clinical touch” for catheter guidance during embryo transfer in women.
      ), there has been little consensus within the scientific community regarding evidence-based guidelines to optimize ET success.
      Much of the published data on prognostic factors of success after ET are conflicting, inconclusive, or confounded by variables due to differing techniques that are unable to be controlled in a reliable manner. In addition, while a systematic literature review is being reported by the American Society for Reproductive Medicine (ASRM) for the steps of ET for which data exist, there are a wide variety of opinions regarding best practices for many other parts of ET and there are few data assessing what practice patterns for ET are actually in use in this country currently (
      Practice Committee of the American Society for Reproductive Medicine
      Performing the embryo transfer: a guideline.
      ). The purpose of this study was to evaluate specific practice patterns of ET nationally and identify potential opportunities for standardization of ET. The goal was to identify a common practice protocol that could be tested by a systematic literature review.

      Materials and methods

      An anonymous 82-question survey was developed by the ASRM Embryo Transfer Advisory Panel of 12 ART experts in the United States to assess the recommendations, policies, restrictions, and specifics to the technique of ET for practices and individuals. The panel members were presented a draft survey, and all participants made comments for changes, additions, deletions, and reformatting of questions. The changed survey was then completed by all of the Advisory Panel members followed by an in-person 3-hour meeting with them at which time the results of the validation survey were reviewed and each question was analyzed for clarity. Changes were made, and the survey was finalized. The survey was structured to cover the following eight sections: [1] fellow and physician training and current practice, [2] determining outcomes and satisfaction with ET technique, [3] techniques and instrumentation, [4] difficult transfers, [5] ET technique/strategies, [6] patient and physician preparation,; [7] embryo expulsion, and [8] improving outcomes. Question types included categorical and yes/no questions as well as multiple choice questions and opportunities for respondents to input free text for their answers. The survey was sent by email to the medical directors of all SART member IVF practices throughout the country who had an active email address and had not previously opted out of optional electronic surveys. The survey was sent on one occasion (April 10, 2015) and was kept open for 1 month to allow time for reply with several reminder emails sent in the interim.
      An additional survey of three questions specifically assessing aspects of transfer technique that were not asked on the initial survey was sent by email on one occasion (January 18, 2016) and was kept open for 4 weeks. In particular, respondents were asked which type of ET they most commonly performed: trial with transfer, afterload, or direct. The following descriptions were given of these procedures. For trial with transfer, the procedure begins with passage of a trial catheter up to or just through the internal os. The embryo(s) are then loaded into the same or a different catheter and the transfer is performed. For afterload, the inner catheter is placed approximately 1 cm beyond the outer sheath; the outer and inner sheaths are then advanced together until the leading tip reaches or is just beyond the level of the internal os; the inner catheter is removed; the loaded catheter is then passed through the outer sheath to the desired location within the endometrial canal. For direct ET, the catheter is immediately loaded with embryo(s) and advanced directly through the internal os to the desired place within the endometrial cavity. A mock transfer is typically not performed, and the outer sheath is not typically left within the cervical canal before transferring a loaded catheter. In addition, in this second survey, the respondents were asked about the location within the endometrial cavity where they plunged the embryos.
      Data were collected and analyzed using SurveyMonkey, an anonymous online survey tool. Descriptive statistics were compiled. The study was submitted to and exempted by the Partners Healthcare Institutional Review Board.

      Results

       Demographics

      Table 1 outlines the detailed demographics taken at the first survey and practice characteristics as reported by respondents. Of the 286 total surveys sent nationwide to SART medical directors, there were 117 (41%) responses from the initial survey. Of the follow-up survey there were 135 (47%) respondents. Demographics of the main survey demonstrate that the respondents are experienced, with all but one performing ETs for over 5 years and 79 (68%) performing more than 100 ETs yearly. Most of them are in private practice (79, or 78%), although all type of practices are represented. These data also demonstrate that of those programs that train fellows, 14 (45%) reported never allowing fellows to perform transfers, and only three (10%) reported allowing fellows to perform between 50% and 100% of total transfers. Thirty (26%) respondents performed fewer than 10 unassisted ETs during their own fellowship; 30 (26%) performed only mock transfers.
      Table 1Demographics and practice characteristics of respondents.
      Demographicsn%
      One hundred seventeen total responses received; every respondent did not necessarily answer every question; percentage per total number of respondents who answered the question.
      Total surveys sent286
      Responses received11740.9
      Type of IVF practice
       Academic with fellows2218.8
       Academic without fellows1613.7
       Private practice affiliated with academic program with fellows76.0
       Private practice without fellows in training7261.5
      If you train fellows, what percent of transfers do fellows perform?
       None1414.0
       < 101010.0
       10–5044.0
       50–10033.0
       NA (practice does not train fellows)6969.0
      Physicians in practice
       13025.6
       2–34235.9
       4–83832.5
       9–1543.4
       >1532.6
      ETs performed personally by respondent, yearly
       <5076.0
       50–1003126.5
       100–2004135.0
       >2003832.5
      Unassisted ETs performed during fellowship training
       Fellowship training limited only to mock transfers3026.1
       <103026.1
       10–503127.0
       50–100108.7
       >10097.8
       NA (respondent not fellowship trained)54.3
      Practice keeps track of each practitioner's ET success rate
       Yes10994.0
       No76.0
      Frequency the practice reviews individual practitioners' ET success rates
       Every 1–2 y or longer76.2
       Yearly3026.5
       Twice a year1614.2
       Quarterly or 3 times a year5548.7
       NA (respondent practice does not keep track of success rates)54.4
      Basis of ET success rate
      Respondent could select more than one answer; percentage per total number of respondents who answered the question.
       Positive hCG4137.0
       Clinical pregnancy rate6558.6
       Implantation rate2219.8
       Live-birth rate1917.1
       NA (respondent practice does not keep track of success rates)43.6
      Estimated typical ET success rate for women <35 y of age per transfer (%)
       <2010.9
       20–3021.7
       30–3565.2
       35–402219.1
       ≥408473.0
      Estimated clinical pregnancy rates for all practitioners performing ET in your practice (%)
      Respondent could select more than one answer; percentage per total number of respondents who answered the question.
       <2000.0
       20–3054.9
       30–403534.0
       40–505048.5
       >503433.0
      Presence of standard technique for ET within practice
       Standard technique5950.9
       Individual choice of practitioner5749.1
      Satisfaction with current ET technique
       Completed satisfied5749.1
       Mostly satisfied but interested in improvement5950.9
       Not satisfied00.0
      Note: ET = embryo transfer; hCG = human chorionic gonadotropin; NA = not applicable.
      a One hundred seventeen total responses received; every respondent did not necessarily answer every question; percentage per total number of respondents who answered the question.
      b Respondent could select more than one answer; percentage per total number of respondents who answered the question.
      Fifty-nine respondents (51%) indicated the enforcement of a standard ET technique within their practice. When evaluating embryo technique, the majority of practices (65, or 59%) used clinical pregnancy rate as the basis of ET success, followed by positive hCG (41, or 37%), implantation rate (22, or 20%), and live-birth rate (19, or 17%). Fifty-five (49%) respondent practices review individual practitioners’ ET success rates quarterly or 3 times per year; only five (4%) do not keep track of individual success rates.

       Physician and Patient Preparation for Transfer

      Table 2 outlines the detailed survey responses for physician and patient preparation for ET. A few of the key points show both consensus and variation. Fifty-five respondents (54%) report no usage of a patient relaxant medication. Of the 47 (46%) who use a relaxant, most respondents use diazepam (2–10 mg). Ninety-two practitioners (88%) wash their hands with soap and water or use an antibacterial hand lotion, while only seven (7%) prepare with a sterile surgical scrub, and six (6%) engage in no specific sanitization before ET. Sixty-four (62%) use a surgical mask, and 93 (89%) use sterile gloves. When performing the ET, 100 (97%) providers sit for the transfer, 56 (54%) use a warmed speculum, and 35 (34%) use a lubricant on the speculum, which, when specified, varied mostly between culture media, 24 (51%), and saline, 20 (43%). Essentially all respondents cleanse the cervix before transfer, with more of them using media, 78 (78%), and the minority using normal saline, 17 (17%). While 77 (75%) remove mucus from the endocervical canal if encountered, there was minimal consensus to the approach to removing mucus, with 25 (26%) using a cotton swab, 19 (20%) using a flush, 29 (31%) using both, and six (6.3%) using aspiration. Fifty-eight (56%) would clear bleeding in the endocervical canal, if encountered, with a cotton swab, 17 (17%) would flush, 13 (13%) would wait and observe before proceeding. Only 15 (15%) would do nothing.
      Table 2Physician and patient preparation.
      Characteristic/stepn%
      One hundred seventeen total responses received; every respondent did not necessarily answer every question; percentage per total number of respondents who answered the question.
      Use of patient relaxant medication
       Yes4746.1
       No5553.9
      Hand sanitization preparation
       Standard sterile surgical scrub76.7
       Wash hands7268.6
       Antibacterial hand lotion2019.0
       No specific sanitization65.7
      Use of a surgical mask
       Yes6461.5
       No4038.5
      Use of sterile gloves
       Yes9389.4
       No1110.6
      Change of gloves after preparation of the cervix
       Yes3534.3
       No6765.7
      Illumination of the perineum during the transfer
       Yes8178.6
       No2221.4
      Position of physician for transfer
       Seated10097.1
       Not seated32.9
      Use of a warmed speculum
       Yes5654.4
       No4745.6
      Use of lubricant to speculum
       Yes3534.0
       No6866.0
      Type of lubricant used
       Culture media2451.1
       Normal saline2042.6
       Sterile water24.3
       US gel12.1
      Cleanse cervix before transfer
       Yes10096.2
       No43.9
      Fluid used to cleanse the cervix
       Normal saline1717.0
       Media from embryology lab7878.0
       NA (do not cleanse cervix)33.0
       Other22.0
      Instrument used to cleanse the cervix
       Cotton swab6667.3
       Gauze sponge on forceps3131.6
       NA (do not cleanse cervix)11.0
      Removal of mucus from the endocervical canal
       Yes7774.8
       No2624.2
      Approach to removing mucus from the endocervical canal
       Cotton swab2526.3
       Flush1920.0
       Both cotton swab and flush2930.5
       NA (mucus not removed)1616.8
       Aspirate66.3
      Approach to bleeding in the endocervical canal
       Clear with cotton swab or Q-tip5856.3
       Flush until bleeding stops before transferring embryo1716.5
       Wait and observe before proceeding1312.6
       Do nothing1514.6
      Use of US guidance for ET
       Always9893.3
       Never32.9
       Selectively43.6
      Primary reason for using US guidance for ET
       To improve success rates7676.8
       For physician reassurance1313.1
       For patient reassurance1010.1
      Person performing US guidance
      Respondent could select more than one answer; percentage per total number of respondents who answered the question.
       US technician2624.8
       Nurse5047.6
       Allied health provider (nurse practitioner, physician's assistant, etc.)1817.1
       Another clinician/fellow1211.4
       Other1110.5
       NA (do not use US guidance)43.8
      Approach to encountering fluid in the endometrial cavity
       Cancel the transfer6159.8
       Aspirate fluid then proceed with transfer3231.4
       Do nothing (proceed with transfer)32.9
       Other65.9
      Approach to bleeding in the endometrial cavity
       Cancel and freeze embryo(s)4746.5
       Do nothing (proceed with transfer)1211.9
       NA (has never occurred)4241.6
      Routine performance of first mock transfer
       Yes9084.9
       No1615.1
      Timing of initial mock transfer
       Before cycle begins8489.4
       During stimulation11.1
       At time of oocyte retrieval66.4
       Immediately before actual transfer33.2
      Note: ET = embryo transfer; NA = not applicable; US = ultrasound.
      a One hundred seventeen total responses received; every respondent did not necessarily answer every question; percentage per total number of respondents who answered the question.
      b Respondent could select more than one answer; percentage per total number of respondents who answered the question.
      Ultrasound (US) guidance for the ET occurs in essentially all practices either with all transfers, 98 (93%), or selectively, four (4%). The primary reason for using US guidance was to improve success rates (76, or 77%), for physician reassurance (13, or 13%), and for patient reassurance (10, or 10%). In 50 respondent practices (48%), US guidance is performed by a registered nurse, less commonly by an US technician (26, or 25%) or an allied health provider such as a physician assistant/nurse practitioner (18, or 17%), another clinician/fellow (11, or 11%) and others, including medical assistants and residents (12, or 11%). In addition to guidance of the transfer, US data may influence the performance of the ET. If fluid is encountered in the endometrial cavity, 61 (60%) would cancel the transfer and 32 (31%) would aspirate the fluid before proceeding with ET; three (3%) would do nothing. If bleeding is noted in the endocervical canal, 57 (56%) would clear it with a cotton swab; alternatively, 17 (17%) would flush it until it stopped; 15 (15%) would do nothing. If bleeding were encountered in the endometrial cavity, 47 (47%) would cancel the transfer and 12 (12%) would do nothing and proceed with the transfer.
      Table 2 also presents tabulated data regarding the timing of the first mock embryo transfer (MET). Eighty-four (89%) do so before the cycle begins. In addition, data regarding the MET at the time of the transfer are tabulated in Table 3, with 70 (92%) of respondents always performing a trial transfer immediately before or during the actual ET procedure, including 40 (52%) as a trial followed by transfer and 30 (40%) performed as a part of the afterload procedure.
      Table 3Instrumentation and transfer technique.
      Characteristic/stepn%
      One hundred seventeen total responses received; every respondent did not necessarily answer every question; percentage per total number of respondents who answered the question.
      The predominant technique used when performing ET
      These questions were assessed in the subsequent three-question survey sent out on a separate occasion; 135 total responses were received with various response rates for each question.
       Trial with transfer technique5239.7
       Afterload technique4030.5
       Direct technique3526.7
      Routine performance of a trial transfer immediately before or at some time during actual ET procedure
       Never4240.0
       Always4441.9
       Selectively1918.1
      Frequency of placing a bend in the catheter or outer sheath before placement in the endocervical canal
       Never76.7
       Always2624.8
       20%–50% of the time4542.9
       >50% of the time1918.1
       The catheter is already bent87.6
      Angle of curve of bent catheter (degrees)
       15–306060.6
       30–453636.4
       45–6033.0
       60–9000.0
      Frequency of transfers using a stylette
       All the time1312.4
       50% of the time21.9
       20%–30% of the time32.9
       <20% of the time6965.7
       Never1817.1
      Frequency of transfers using a tenaculum or cervical suture
       Never3533.7
       Several times in my career4038.5
       <10% of the time2423.1
       10%–25% of the time21.9
       25%–50% of the time32.9
      Frequency of advancing the outer sheath over the inner catheter
       <20% of the time4746.1
       25% of the time2221.6
       30% of the time1110.8
       >50% of the time2221.6
      Approximate location within endometrial canal where tip of catheter is aimed
      These questions were assessed in the subsequent three-question survey sent out on a separate occasion; 135 total responses were received with various response rates for each question.
       Upper third8965.9
       Middle third3928.9
       Lower third75.2
      If aiming for the upper third of the endometrial canal, the closest from the uterine fundus the catheter tip is aimed to be placed (cm)
      These questions were assessed in the subsequent three-question survey sent out on a separate occasion; 135 total responses were received with various response rates for each question.
       0.587.0
       1.05447.0
       1.54539.1
       2.087.0
      Who pushes the plunger once the embryo catheter is in place
       Physician7673.8
       Embryologist2726.2
      Speed and process of plunge
       As slowly as possible1514.6
       Slow with steady pressure6260.2
       Moderately fast with steady pressure2625.2
       As quickly as possible00.0
      Do you leave the outer sheath in place until embryologist checks for retained embryo?
       Yes1110.7
       No6361.2
       Only for difficult transfers2928.2
      Approach to retained embryos in catheter
       Retransfer in same catheter3432.7
       Reload into new catheter7067.3
      Frequency of retained embryos (%)
       <17874.3
       1–52422.9
       5–1521.9
       15–2011.0
       >2000.0
      Time after embryos expelled into the cavity before removing catheter
       Immediately remove catheter3130.7
       Wait 5–10 sec3332.7
       Wait 30 sec2221.8
       Wait 1 min1211.9
       Other33.0
      Direction for catheter removal
       Straight4948.0
       Rotate as removed5352.0
      Patient remains supine after the transfer (time supine)
       Gets up immediately3331.7
       5–10 min1312.5
       10–15 min1312.5
       15–30 min2826.9
       30 min to 1 h1514.4
       > 1 h21.9
      a One hundred seventeen total responses received; every respondent did not necessarily answer every question; percentage per total number of respondents who answered the question.
      b These questions were assessed in the subsequent three-question survey sent out on a separate occasion; 135 total responses were received with various response rates for each question.

       Instrumentation and Transfer Technique

      Table 3 tabulates instrumentation and transfer technique data as reported by survey respondents. A bend is placed in the catheter or outer sheath always by 26 (25%), with the angle of the curve placed in the catheter most commonly reported as 15°–30° (60, or 61%). Additional data presented in Table 3 include the rare use and indications for a stylette and tenaculum or cervical suture.
      The additional survey specifically assessed practitioners’ predominant technique used when performing transfers. These were separated into three categories: trial with transfer, afterload, and direct transfer techniques performed by 40%, 31%, and 27% of 131 respondents, respectively. The majority of practitioners place the tip of the catheter in either the upper third (89, or 66%) or middle third (39, or 29%) of the endometrial cavity. When targeting the upper third of the endometrial canal, the vast majority of providers aim to get no closer than 1–1.5 cm to the fundus (99, or 86%).
      Plunging the embryos is performed in the majority of practices by the physician (76, or 74%) and less frequently by the embryologist (27, or 26%). More variation is seen in the characteristics of the plunge and the time and technique for withdrawal of the catheter: 75% push in the plunger slowly; nearly 2/3 withdraw the catheter either immediately or at 5–10 seconds; and the catheter is withdrawn either straight or in a rotating fashion, approximately 50/50. The presence of retained embryos is reported by the majority of practices as a rare occurrence (<1%). Techniques employed while waiting for the embryologist's report and for retransfer of embryos, if found, are also reported in Table 3. Almost one third of patients will get up immediately after transfer, while 26 (25%) spend 5–15 minutes supine, 28 (27%) spend 15–30 minutes supine, and 17 (16%) spend greater than 30 minutes supine. When asked to name the two most important components of a successful transfer besides the skill of the practitioner, 85 practitioners (83%) chose “final location of tip of catheter in uterine cavity” and 47 (46%) chose prevention of uterine bleeding.

       Troubleshooting Difficult Transfers

      Table 4 outlines the possible steps in troubleshooting difficult ETs as reported by survey respondents. Eighty-nine (84%) practices report that in the case of a difficult ET, once the catheter is loaded, they would return the embryos to the incubator if needed. When asked how long would one attempt a difficult transfer before returning embryos to the incubator, 32 (32%) responded 1 minute, 26 (26%) 2 minutes, seven (7%) 3 minutes, and six (6%) 5 minutes. Nineteen (19%) answered “no fixed time limit,” which is consistent with the number of respondents who also reported they would not return embryos to the incubator. Additional strategies employed for difficult transfers are displayed in Table 4 and include taking a break (32, or 31%), asking another clinician to try the transfer (35 respondents or 33%, but rarely), and using anesthesia or conscious sedation (67, or 63%, <10% of time). The most commonly used techniques to troubleshoot difficult transfers included varying the amount of urine in the bladder first (i.e., fill or empty depending on situation), 35 (40%); using a stylet, 31 (34%); changing the type of transfer catheter, 26 (30%); and using a relaxant and attempting again after a break, 9 (14%). When asked which strategies were the most likely to be used when scheduling an IVF cycle for a patient with a known difficult transfer, 34 (33%) were most likely to perform a mock transfer to “map out the ET course.” Twenty-two (22%) perform dilation before the start of stimulation, 21 (21%) perform cervical dilation at the time of egg retrieval, nine (9%) hysteroscopically manage the patient, nine (9%) schedule the transfer under anesthesia, and seven (7%) responded with other techniques including laminaria overnight, relaxant medications, and cervical suture. When asked to describe the strategies employed for difficult transfers not previously surveyed, the following qualitative responses were reported: varying the patient position (most commonly knee-chest position), using an os finder for slight dilation, precycle laminaria, dilation/hysteroscopy, and/or misoprostol several days before transfer. When asked to describe the most common cause of difficult transfers, 41 physicians (49%) responded with acute flexion of the uterus (25, or 30% answering acute anteflexion and 16, or 19% answering acute retroflexion). Twenty-one (24%) felt a tortuous cervical canal most commonly contributed to a difficult transfer, and 16 (20%) felt either ridges or false tracts in the cervical canal were most likely to blame.
      Table 4Troubleshooting difficult transfers.
      Characteristic/stepn%
      One hundred seventeen total responses received; every respondent did not necessarily answer every question; percentage per total number of respondents who answered the question.
      For difficult transfers once the catheter is loaded, will you return embryos to incubator
       Yes8984.0
       No1716.0
      How long in minutes will you continue with a difficult transfer before returning embryos to the incubator?
       13231.7
       22625.7
       376.9
       565.9
       >500.0
       No fixed time limit1918.8
       NA (will not return embryos to incubator)1110.9
      When the embryos are returned, do you use fresh media to reincubate them
       Yes1818.6
       No6668.0
       NA (will not reincubate embryos)1313.4
      With difficult transfers, will you let the patient take a break and try again later
       Yes3230.5
       No7369.5
      How frequently do you ask another provider to try a transfer that is difficult for you? (% of the time)
       Never6763.2
       Several times in career3533.0
       <543.8
       >500.0
      Frequency of performing difficult transfers under anesthesia or conscious sedation (% of the time)
       Never4239.6
       <106157.6
       10–2511.0
       >2521.9
      Frequency of freezing embryos with plan to transfer at a later date for difficult transfers (% of the time)
       Never6763.2
       <103835.9
       10–2500.0
       25–5010.9
       >5000.0
      Strategy used when scheduling cycle for a known difficult transfer
       Perform mock transfer in cycle to map out course3433.3
       Perform dilation before start of stimulation2221.6
       Perform cervical dilation at time of oocyte retrieval2120.6
       Hysteroscopic management98.8
       Schedule transfer under anesthesia98.8
       Other76.9
      Perform difficult transfer under anesthesia/sedation less than 10% of the time99.1
      Note: NA = not applicable.
      a One hundred seventeen total responses received; every respondent did not necessarily answer every question; percentage per total number of respondents who answered the question.
      All steps/characteristics of the ET procedure addressed in this survey were analyzed for concordance among the respondents. Of the 48 total steps and characteristics of ET practice analyzed, 10 of them were considered highly conserved with at least 85% of respondents having the same answer. They are [1] tracking of each practitioner's ET success rate; [2] use of hand sanitization preparation and [3] sterile gloves; [4] cleansing of cervix; [5] seated physician position; [6] US guidance for ET; [7] timing of first mock transfer; [8] trial at transfer (including afterload]; [9] never asking another provider to try a difficult transfer; and [10] performing a difficult transfer under anesthesia or sedation less than 10% of time. There were five steps of the ET procedure in which respondents indicated highly discordant practice patterns occurring among 40%–56% of respondents: [1] presence of standard ET protocol; [2] universal use of patient relaxant medication of ET; [3] use of warmed speculum; [4] straight versus rotating direction of catheter removal; and [5] patient remaining supine for less than or greater than 15 minutes after ET.

      Discussion

      This study represents the first published survey from SART member centers across the country that specifically assesses ET techniques and common practices. It identified the steps of ET with the highest respondent consensus, demonstrating the most conserved steps of ET on a national basis. While some of these steps have been previously studied, others have not, such as the use of hand sanitization before ET, use of sterile gloves, and a cervical cleanse before transfer. Interestingly, similar to recently published data that support US guidance over clinical touch technique (
      • Strickler R.C.
      • Christianson C.
      • Crane J.P.
      • Curato A.
      • Knight A.B.
      • Yang V.
      Ultrasound guidance for human embryo transfer.
      ,
      • Brown J.
      • Buckingham K.
      • Buckett W.
      • Abou-Setta A.M.
      Ultrasound versus “clinical touch” for catheter guidance during embryo transfer in women.
      ,
      Practice Committee of the American Society for Reproductive Medicine
      Performing the embryo transfer: a guideline.
      ,
      • Buckett W.M.
      A meta-analysis of ultrasound-guided versus clinical touch embryo transfer.
      ), 93% of those surveyed always use US for guidance. Timing of a mock transfer before cycle start was also conserved for 89% of respondents (
      • Katariya K.O.
      • Bates G.W.
      • Robinson R.D.
      • Arthur N.J.
      • Propst A.M.
      Does the timing of mock embryo transfer affect in vitro fertilization implantation and pregnancy rates?.
      ). In addition, a trial transfer was performed by 92% of respondent practices either as a trial followed by a transfer after removal of the trial catheter or as a part of an afterload procedure. Highly conserved ET practices such as these may be instructive in identifying steps that the vast majority of reproductive endocrinologists consider critical to a successful ET. They may serve as instruction for trainees, for new IVF practices seeking “best practices,” or for practices seeking to develop their own standard ET technique to be used by all of their practitioners. In contrast, for others, determining that their ET practice includes one or more of the steps that is rarely performed by IVF practitioners may help identify an area for performance improvement.
      This survey also identified areas of discordance in ET technique, which highlight where practices are most varied. As an example of nearly equal discordance, the use of patient relaxant medication is practiced in 46% of the surveyed population; there have been no published reports on benefits or drawbacks of this practice. In regards to removal of the catheter after transfer, 48% of respondents remove the transfer catheter in a straight direction, while 52% rotate during removal. As a final example, patient positioning after the transfer is another contested area, in which 57% of providers have patients get up immediately or within 15 minutes, while 43% have patients remain supine for greater than 15 minutes after transfer. This represents an area of change, as historically patients may have been placed on bedrest for longer than 24 hours after ET. More recent studies have suggested that even brief bedrest does not offer any benefit compared with immediate ambulation (
      • Purcell K.J.
      • Schembri M.
      • Telles T.L.
      • Fujimoto V.Y.
      • Cedars M.I.
      Bed rest after embryo transfer: a randomized controlled trial.
      ), but this survey shows provider practices continue to differ.
      In addition to the identified steps with near 50/50 discordance, there are still other steps with wide variation (Table 3). This demonstrates that the practice of ET is highly diverse. There exists a variety of opinions and practices that are employed nationally with this single procedure. This may have some effect on the published literature on outcomes after ET. As with any procedure, highly variable inputs and absence of process standardization make it increasingly difficult to control for confounders and study outcomes (such as clinical pregnancy or live-birth rates). Review of the ET literature demonstrates numerous inconclusive studies or results that vary from one study to another. The absence of process standardization could be one such reason underlying these findings (
      • Mains L.
      • Van Voorhis B.J.
      Optimizing the technique of embryo transfer.
      ).
      The results of this survey highlight a need to develop a standardized ET procedure. With the data presented here, a common practice procedure can be proposed and these steps analyzed for legitimacy by the ASRM systematic review of the literature where data exist (
      Practice Committee of the American Society for Reproductive Medicine
      Performing the embryo transfer: a guideline.
      ). Based on the most common practice, we propose the following “common practice procedure” that includes the standard time-out process during which the patient is matched with the embryos.
      • 1.
        Patient preparation for procedure (relaxant when deemed necessary).
      • 2.
        Physician preparation for procedure to include some form of handwashing and sterile latex-free gloves.
      • 3.
        Time-out process with identification and matching of patient and embryos.
      • 4.
        Use of abdominal US for view of the endometrial cavity and other pelvic structures and guidance of the ET; alternatively, selective use of abdominal US for potentially difficult ET.
      • 5.
        Place speculum.
      • 6.
        Flush or cleanse cervix/vagina with cotton swab or gauze sponge using media or saline solution.
      • 7.
        Remove mucus from endocervical canal.
      • 8.
        Load the ET catheter and traverse the cervix using one of three techniques: trial followed by transfer, afterload transfer, or direct transfer.
      • 9.
        Place the tip of the catheter at the upper or middle third of the endometrial catheter and no closer than 1–1.5 cm to the fundus; expel the embryos, and remove the catheter.
      • 10.
        Check the catheter for retained embryo(s).
      • 11.
        Patient leaves the room.
      We propose that the ASRM systematic review of the literature be used to further refine these usual practice steps, either supporting or refuting their use (
      Practice Committee of the American Society for Reproductive Medicine
      Performing the embryo transfer: a guideline.
      ). While there has been a significant effort to monitor IVF outcomes on the national level, process standardization has not yet been part of the equation. This phenomenon is not limited to the practice of IVF. Despite its success in other industries, process standardization has been more difficult to adopt within health care. While there have been increasing efforts on a global level to use standardization in part to improve health care delivery, the attention has been mostly focused on basic patient safety issues such as correct surgery and medication reconciliation (
      • Leotsakos A.
      • Zheng H.
      • Croteau R.
      • Loeb J.M.
      • Sherman H.
      • Hoffman C.
      • et al.
      Standardization in patient safety: the who high 5s project.
      ). Process standardization may be a difficult goal for IVF given the number of variable inputs that qualify ET as often more of an “art” than a science (
      • Hall J.M.
      • Johnson M.E.
      When should a process be art, not science?.
      ). That said, benefits of a standardized operating protocol might include a reduction in system variation, promotion of efficiency and quality control, assistance in standardizing research across multiple sites, facilitation of trainee education and proficiency, and ultimately success rates.
      A significant aspect of these survey results is the information gathered on trainee involvement in ET. Over half of the medical directors surveyed reported that they either never performed or did fewer than 10 ETs during their own fellowship training; presumably their skill was either self-taught or influenced by fellow practitioners in early practice. There are currently 44 American Board of Obstetrics and Gynecology–approved fellowship programs in the country. Of the SART medical directors who responded to our survey, 29 work at IVF centers associated with fellowship programs. This represents 66% of all the fellowship programs nationally. Fourteen of the 29 (48%) surveyed IVF centers with fellow training do not allow fellows to perform any transfers during their training. Small studies have suggested that ET by fellow versus attending has no significant difference in live-birth rate (
      • Eaton J.L.
      • Zhang X.
      • Barnes R.B.
      Embryo transfer by reproductive endocrinology fellows vs attending physicians: Are live birth rates comparable?.
      ). While it has been reported that a relatively low number of ETs is necessary to achieve competence (
      • López M.J.
      • Garcia D.
      • Rodriguez A.
      • Colodron M.
      • Vassena R.
      • Vernaeve V.
      Individualized embryo transfer training: timing and performance.
      ), a more standardized training approach may be helpful for practitioners in the early stages of their career. If many providers are self-taught or are only exposed to one particular center's ET protocol, there may be utility in pursuing a standardized protocol for new providers to learn. In addition, a number of studies have demonstrated variation of the ET pregnancy rates among practitioners within practices (
      • Angelini A.
      • Brusco G.F.
      • Barnocchi N.
      • El-Danasouri I.
      • Pacchiarotti A.
      • Selman H.A.
      Impact of physician performing embryo transfer on pregnancy rates in an assisted reproductive program.
      ,
      • Hearns-Stokes R.M.
      • Miller B.T.
      • Scott L.
      • Creuss D.
      • Chakraborty P.K.
      • Segars J.H.
      Pregnancy rates after embryo transfer depend on the provider at embryo transfer.
      ,
      • Karande V.C.
      • Morris R.
      • Chapman C.
      • Rinehart J.
      • Gleicher N.
      Impact of the “physician factor” on pregnancy rates in a large assisted reproductive technology program: do too many cooks spoil the broth?.
      ). Standardization may help to reduce the variation and increase success rates from practitioner to practitioner, even for those who have performed ETs for more than 5 years.
      Of late, there has been increasing attention on simulation as a method of trainee involvement in learning ET technique. Recently, ASRM partnered with Virtamed, a company dedicated to building high-fidelity surgical simulators for medical education, to develop a simulator for the training of ET and IUI (
      • Sunderam S.
      • Kissin D.M.
      • Crawford S.B.
      • Folger S.G.
      • Jamieson D.J.
      • Warner L.
      • et al.
      Assisted reproductive technology surveillance—United States, 2013.
      ). Results from this survey may help guide the analysis of ET technique and the development of a training protocol to be used nationwide (
      • Gambone J.C.
      • Segars J.H.
      • Cedars M.
      • Schlaff W.D.
      Fellowship training and board certification in reproductive endocrinology and infertility.
      ).
      Limitations of this study include its subjective nature, which is intrinsic to survey studies. While its response rate of 41% (and 47% for the additional survey) is relatively high for an elective survey of its length, our respondents might not be a representative sample of the IVF centers across the nation. An additional limitation is that given the length of the survey, a respondent was not required to answer every question in order to submit their response. Thus there were slightly differing response rates from question to question. These results are qualitative and should be interpreted accordingly as the aim of the study is to elucidate overall practice patterns and highlight opportunities for further discussion surrounding potential standardization. Finally, to limit the length of the survey, some areas were not included such as the use of transvaginal US for ET, the type of catheter used, the amount of media injected with embryos, and the use of air “bubbles” along with the media.
      Strengths of the study include its national scope as well as the comprehensive nature in which the survey assessed each specific step of ET. From this study, the first of its kind, one can infer the most important, critical, conserved, and also discordant steps of ET. The results provide a breadth of qualitative information regarding the national practice patterns of ET. For any one individual or practice that may be interested in learning about others’ perspectives and practice of ET, this survey demonstrates what medical directors of SART member IVF programs across the country believe are critical to their success.
      In summary, the current study examined attitudes toward and practice patterns of ET among experienced providers throughout the nation. It identified areas that providers felt to be most critical to successful ET; the results also detect steps in which providers had the most divergent opinions. These findings may have significant implications on future research, trainee development, and clinical outcomes reporting. Further, the survey results highlight the discussion surrounding potential process standardization of ET in the setting of improving patient outcomes and advancing the field of assisted reproduction.

      Acknowledgments

      In addition to the authors, other members of the ASRM Embryo Transfer Advisory Panel involved in development of the survey include Owen K. Davis, M.D., Robin N. Fogle, M.D., David Frankfurter, M.D., Jamie A. Grifo, M.D., Julie D. Lamb, M.D., Andrew R. La Barbera, Ph. D., Alan S. Penzias, M.D., John A. Schnorr, M.D., Richard T. Scott, M.D., Andrew A. Toledo, M.D., and Eric A. Widra, M.D.

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