Upload
agus-prima
View
215
Download
0
Embed Size (px)
Citation preview
7/25/2019 1-s2.0-S0002937814005109-main
1/5
GYNECOLOGY
Embryo transfer by reproductive endocrinologyfellows vs attending physicians: are live
birth rates comparable?Jennifer L. Eaton, MD, MSCI; Xingqi Zhang, PhD; Randall B. Barnes, MD
OBJECTIVE:To compare live birth rates following ultrasound-guided
embryo transfer (ET) by reproductive endocrinology and infertility fel-
lows versus attending physicians.
STUDY DESIGN: Women who underwent their first day-3, fresh,
nondonor ET between Oct. 1, 2005, and April 1, 2011, at our ac-
ademic center were included in this retrospective cohort study.
Embryos were designated high quality if they had 8 cells, less than
10% fragmentation, and no asymmetry. ET was performed with the
afterload technique under ultrasound guidance. Categorical vari-
ables were evaluated with the c2 test and continuous variables with
the Studentttest. Logistic regression was performed to assess the
relationship between ET physician and live birth rate while adjusting
for potential confounders.
RESULTS:Seven hundred sixty women underwent ET by an attending
physician, and 104 by a fellow. Baseline characteristics were similar
between the groups. The live birth rate was 31% following ET by an
attending physician, compared with 34% following ET by a fellow (P
.65). Logistic regression adjusting for potential confounders demon-
strated no significant association between ET physician and live birth rate.
CONCLUSION: This retrospective study demonstrated no significant
difference in live birth rates following ultrasound-guided ET by fellows vs
attending physicians at our institution. These data suggest that academicpractices using the afterload method and ultrasound guidance can train
fellows to perform ET without compromising success rates.
Key words: assisted reproductive technology, embryo transfer, in vitro
fertilization
Cite this article as: Eaton JL, Zhang X, Barnes RB. Embryo transfer by reproductive endocrinology fellows vs attending physicians: are live birth rates comparable? Am J
Obstet Gynecol 2014;211:494.e1-5.
E mbryo transfer (ET) is a critical stepin the process of in vitro fertiliza-tion (IVF). Existing literature suggeststhat ET outcomes are inuenced by
several factors, including patient age,1,2
embryo quality,3 the type of transfer
catheter used,4,5 the use of ultrasound
guidance,6-8 and ET provider.9-12 Despitethe importance of proper ET technique, a
recent survey of current fellows and
recent fellowship graduates indicatedthat almost half of reproductive endo-crinology and infertility (REI) fellows do
not perform ET while in training.13
Although that study was limited by alow response rate of 39%, the ndings
suggest that many REI fellowship grad-
uates perform their rst ETs as attending
physicians.
13
Several explanations havebeen suggested for the lack of experience
in ET. Many programs restrict ET toattending physicians based on historical
precedent or concerns about patient
satisfaction.13 Alternatively, programsmay fear that pregnancy rates will be
compromised by allowing fellows to
perform ET, despite a lack of supportingevidence. Finally, signicant heteroge-neity exists among the various training
methods.14-16 As an alternative to real
ET, many programs train fellows withmock ET or intrauterine insemination
(IUI). Other programs require fellows to
perform a minimal number of IUIs prior
to performing ET. In a recent study,however, fellow and attending physician
ET pregnancy rates were comparableboth before and afterthe institution of a
minimal IUI policy.16 In addition, a
survey of recent fellowship graduatesrevealed that those who did not per-
form ET as a fellow were more likely to
require additional ET training aftergraduation.17 Therefore, there is a criticalneed for development of a training
method that will allow fellows to perform
ET while not compromising programs
success rates.
At our academic institution, fellows
perform embryo transfer under directultrasound guidance by the attending
physician. All providers use the afterloadmethod, in which the outer sheath of the
transfer catheter is left in place to
maintain access to the uterine cavity.Embryos are loaded into the inner
sheath only after proper placement of
the outer sheath is conrmed by the
attending physician, thereby minimizingthe time from loading to transfer and
From the Division of Reproductive Endocrinology and Infertility, Department of Obstetrics andGynecology, Feinberg School of Medicine, Northwestern University School of Medicine, Chicago, IL.DrEaton is now afliated with the Division of Reproductive Endocrinology and Fertility, Department ofObstetrics and Gynecology, Duke University School of Medicine, Durham, NC.
Received March 11, 2014; revised May 8, 2014; accepted May 27, 2014.
The authors report no conict of interest.
Presented in oral format at the 68th annual meeting of the American Society for ReproductiveMedicine, San Diego, CA, Oct. 20-24, 2012.
Corresponding author: Jennifer L. Eaton, MD, [email protected]
0002-9378/$36.00 2014 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajog.2014.05.042
494.e1 American Journal of Obstetrics &Gynecology NOVEMBER 2014
Research ajog.org
mailto:[email protected]://dx.doi.org/10.1016/j.ajog.2014.05.042http://ajog.org/http://ajog.org/http://ajog.org/http://dx.doi.org/10.1016/j.ajog.2014.05.042mailto:[email protected]7/25/2019 1-s2.0-S0002937814005109-main
2/5
ensuring optimal catheter positioning.Given the high degree of attending
control over the ET process at our in-
stitution, we hypothesized that ourtraining model allows fellows to perform
ET without compromising success rates.
Our objective was to examine the rela-tionship between trainee status and live
birth rate after ET while controlling forpotential confounders.
MA T E R I A L S A N D METHODS
The study was approved by the North-
western University Institutional ReviewBoard. All women who underwent day 3,
fresh, nondonor embryo transfer be-
tween Oct. 1, 2005, and April 1, 2011, atour academiccenter wereidentied. This
study period was chosen based on theinception of our institutions fellowship
program in 2005. Only rst IVF cycles
were included in the analysis. Two hun-dred twenty-one cycles lacking complete
data on embryo quality, ET physician, or
birth outcomes were excluded.Patients underwent one of the fol-
lowing ovarian stimulation protocols:luteal phase leuprolide acetate suppres-
sion (Lupron; Abbott Laboratories,
Abbott Park, IL) with or without oral
contraceptive pretreatment; microdoseLupron are; or GnRH antagonist pre-
vention of premature ovulation withcetrorelix (Cetrotide; EMD Serono,Rockland, MA) or ganirelix (Antagon;
Organon, Roseland, NJ). Controlled
ovarian hyperstimulation was achievedby administration of once or twice daily
injections of follicle-stimulating hor-
mone (FSH) (Follistim; Organon,Roseland, NJ or Gonal-F; EMD Serono)
or FSH plus luteinizing hormone (LH)
(Menopur; Ferring Pharmaceuticals,Parsippany, NJ) at total daily doses
ranging from 75 through 600 IU. In theantagonist protocol, the GnRH antago-
nist was added when a lead follicle
measured 14 mm or the estradiolexceeded 500 pg/mL. Cycles weremonitored with serum estradiol levels
and transvaginal ultrasounds beginning
on stimulation day 5 and every 1-2 daysthereafter. When at least 3 follicles
reached a mean diameter of 16 mm, 250m
g recombinant human chorionicgonadotropin (hCG) (Ovidrel; EMD
Serono) were administered subcutane-ously. Ultrasound-guided oocyte re-
trieval was performed 36 hours later.
Luteal phase support with 50 mg intra-muscular progesterone in oil was initi-
ated the day of oocyte retrieval.
Embryos were inseminated 4-6 hoursafter retrieval by culture with motile
sperm or by intracytoplasmic sperm in-jection. Fertilization was veried by the
presence of 2 pronuclei 15 to 18 hours
after insemination. Embryos were cul-tured in 40 mL droplets of culture me-
dium at 37 C in a humidied 5% O2,5% CO2, and 90% N atmosphere until
day 3. Embryos were deemed highquality on day 3 if they contained 8 cells
with less than 10% fragmentation and
no asymmetry.Embryo transfer was performed on
day 3. Five fellows and 4 attending phy-
sicians performed ET. There was nooverlap between fellows and attendings.
In general, fellows performed 1-5 intra-uterine inseminations and observed 1-5
embryo transfers before performing a
transfer; however, there was no mini-mum requirement for inseminations or
observed transfers. The 4 attending
physicians each had 15-20 years experi-
ence with ET and historically had com-parable success rates. Fellows typicallyperformed transfers on 1-2 assigned days
per week. The number of embryos totransfer was based on American Society
for Reproductive Medicine guidelines
and institutional protocols. All ETswere performed with a Wallace catheter
(Smiths Medical, Dublin, OH) under
direct transabdominal ultrasound guid-ance. Attending physicians performed
the ultrasound guidance for all fellow
ETs. The afterload technique was usedaspreviously described by Neithardt et al.18
Briey, the cervix was washed with em-bryo culture media and a Wallace cath-
eter was then introduced into the uterine
cavity until the outer sheath passed theinternal os. The inner catheter wasremoved and discarded, and the em-
bryo(s) loaded into a new inner catheter
by the embryologist. This inner catheterwas then placed through the outer
catheter and the embryo(s) was/were
transferred approximately 1 to 1.5 cmfrom the top of the uterine cavity.
Pregnancy was conrmed with apositive serum hCG 10 days following
ET, and a repeat hCG 48 hours later if
the initial hCG was positive. Clinicalpregnancy was veried by fetal cardiac
activity on a transvaginal ultrasound at
6 to 7 weeks gestational age. Clinicalpregnancy rate, live birth rate, and
multiple birth rate were calculated asfollows: (N/total number of ETs) 100.
Because of the retrospective studydesign, sample size was determined by
the study period. Previous studies have
reported that pregnancy rates with dif-ferentET providers vary signicantly. For
example, Hearns-Stokes et al10 dem-onstrated pregnancy rates rangingfrom
17.0% to 54.3% and Karande et al11 re-
ported a range of 13.2% to 37.4%. Forthe current analysis, post hoc power
calculations were performed with SPSS
Sample Power 3 (IBM Corporation,Armonk, NY). The overall live birth rate
for attending physicians and fellowsduring our study period was 31.7%. For
the purpose of power calculations, we
hypothesized that the live birth ratewould be higher for attending physicians.
Assuming a live birth rate of 32% for
attending physicians, a sample size of 104
participants per group would provide83% power at5% type I error to detect anabsolute difference of 17% in live birth
rates (ie, 32% for attending physiciansand 15% for fellows). Assuming an even
higher live birth rate for attending phy-
sicians, 35%, the same sample size wouldstill provide 80% power at 5% type I er-
ror to detect the same absolute difference
(ie, 35% for attending physicians and18% for fellows).
Statistical analysis was performed
with SPSS Statistics 19 (IBM Corpora-tion). The c2 test was used for categor-
ical variables, and Student t test forcontinuous variables. Crude odds ratios
(ORs) and 95% condence intervals
(95% CIs) were determined. Logisticregression was performed to examinethe association of trainee status with
live birth rate while controlling for the
effects of potential confounders,including maternal age, gravidity, par-
ity, day 3 FSH, number of oocytes
retrieved, number of oocytes fertilized,use of intracytoplasmic sperm injection,
ajog.org Gynecology Research
NOVEMBER 2014 American Journal of Obstetrics &Gynecology 494.e2
http://ajog.org/http://ajog.org/7/25/2019 1-s2.0-S0002937814005109-main
3/5
use of assisted hatching, number of
embryos transferred, and the number ofhigh quality embryos transferred. Only
signicant predictors of live birth were
included in the nal regression model. A2-tailedPvalue of< .05 was considered
statistically signicant.
RESULTS
Seven hundred sixty embryo transfers
were performed by attending physicians
and 104 by fellows. Baseline patientcharacteristics were similar between the
2 groups (Table 1). There were no sig-nicant differences in stimulation pa-
rameters, laboratory techniques used, or
the number of embryos transferred(Table 2). Embryo quality was similar
between the 2 groups (Table 2). There
were no signicant associations betweentrainee status and IVF outcomes. Live
birth rates, clinical pregnancy rates, and
multiple birth rates were comparable
between the 2 groups (Table 3). Onlyyoung maternal age and the number of
high quality embryos transferred were
predictors of live birth when all potentialconfounders were included in a logistic
regression model (P < .001). After
adjusting for the effects of maternal ageand number of high quality embryostransferred, the odds of live birth
remained statistically indistinguishable
following ET by an attending physicianvs ET by a fellow (Table 3).
COMMENT
This retrospective study demon-
strated similar live birth rates followingultrasound-guided ET by REI fellows and
attending physicians using the afterload
technique at our academic institution.The ndings were unchanged after
adjusting for potential confounders.
Previous studies have demonstratedthe feasibility of ET by nonphysician
providers. Specically, 2 studies com-
pared pregnancy rates with ET by nursesvs physicians. The rst, by Barber et al,19
demonstrated a 36% pregnancy rate
following ET by nurses, compared with29% with physician ET. Although there
was a trend toward increased pregnancyrates with ET by nurses, this difference
was not statistically signicant and therewas no power analysis to support the
authors conclusionof a high compa-
rable success rate.19 Unlike REI fellows,who are still trainees, the nurses in this
study had previously been trained andcertied competent by a senior doc-
tor.19 Details of the training, however,
were not discussed. The authors notedthat difcult transfers were typically
performed by physicians, and that
straightforward transfers were associatedwith the highest pregnancy rates.
Therefore, their ndings were inuencedby selection bias. Furthermore, the
analysis did not control for embryo
quality or the number of embryostransferred. The second study, by Sin-
clair et al,20 compared pregnancy rates
after ET by nurses vs physicians. Preg-
nancy rates were similar between the 2groups (40.2% vs 41%), and implanta-tion rates were also comparable (16.9%
vs 17%). Nurses were trained byobserving at least 5 ETs and performing
at least 5 ETs. As in the rst study, doc-
tors were called for difcult transfers,resulting in selection bias. Furthermore,
1 of the 4 physicians had never per-
formed ET before the study period.Finally, the study lacked a power calcu-
lation. Given the limitations of these
preliminary studies, the only conclusionthat can be drawn is that select,
straightforward ETs by nurses werenot associated with different pregnancy
outcomes at the authorsinstitutions.
Few studies have specically examinedthe inuence of training on pregnancyrates following ET. Barber et al21
demonstrated a higher pregnancy rate
following ET by 3 experienced nursescompared with ET by 3 nurses who were
undergoing training (29.5% vs 19.5%).
In contrast to our study, however, ul-trasound guidance was used only for
TABLE 1
Patient characteristics
CharacteristicAttending physiciansn[ 760
Fellowsn[ 104 Pvalue
Age, y 36.4 (36.1e36.7) 36.0 (35.2e36.7) .32
Gravidity 0.9 (0.8e
0.9) 1.0 (0.7e
1.3) .27
Parity 0.2 (0.2e0.3) 0.3 (0.1e0.4) .70
D3 FSH (mIU/mL) 7.5 (7.3e7.8) 7.5 (6.9e8.1) .91
Values represent mean (95% CI). Pvalues determined with Student ttest.
CI, confidence interval; D3 FSH, day 3 follicle-stimulating hormone.
Eaton. Live birth rates following embryo transfer by fellows vs attending physicians. Am J Obstet Gynecol 2014.
TABLE 2
IVF cycle parameters
ParameterAttending physiciansn[ 760
Fellowsn[ 104 Pvalue
Number of oocytes retrieved 10.1 (9.7e
10.6) 10.8 (9.6e
12.1) .29
Number of oocytes fertil ized 6.0 (5.7e6.3) 6.0 (5.2e6.8) .99
Number (%) of cycles with ICSI 626 (82) 81 (78) .27
Number (%) of cycles withassisted hatching
459 (60) 57 (55) .28
Number of embryos transferred 2.2 (2.2e2.3) 2.2 (2.1e2.3) .64
Number of high quality embryostransferred
0.7 (0.6e0.7) 0.8 (0.6e1.0) .31
Values represent mean (95% CI) or n (%). Pvalues determined by c2 test for categorical variables and Student t test forcontinuous variables.
CI, confidence interval; ICSI, intracytoplasmic sperm injection.
Eaton. Live birth rates following embryo transfer by fellows vs attending physicians. Am J Obstet Gynecol 2014.
Research Gynecology ajog.org
494.e3 American Journal of Obstetrics &Gynecology NOVEMBER 2014
http://ajog.org/http://ajog.org/7/25/2019 1-s2.0-S0002937814005109-main
4/5
difcultETs.21 Ultrasound guidance islikely an important component of ET
training, as catheter placement is directly
observed by the attending physician.More recently, Papageorgiou et al14
examined the inuence of experience
on pregnancy rates following ET by 5REI fellows. When cumulative preg-
nancies were plotted over time for eachfellow, pregnancy rates appeared lower
for the rst 25 ETs as compared with
the second 25 ETs. Therefore, the au-thors divided each fellows training
period in half and compared pregnancy
rates between the 2 periods. They
demonstrated a trend toward improvedpregnancy rates over time (39% for ET1-25 vs 52% for ET 26-50); however,
statistical signicance was not ach-ieved. The authors also reported that
the fellowsoverall pregnancy rate was
comparable to that of experiencedproviders (45.5% vs 47.3%), in agree-
ment with the ndings from our study.
When comparing rates of fellows andexperienced providers, however, the
analysis did not control for potential
confounders such as patient age, em-bryo quality, and number of embryos
transferred. Therefore, although thestudy provided interesting information
regarding ET learning curves among
fellows, it was not designed to drawconclusions regarding equivalence ofthe pregnancy rates between fellows
and experienced providers.
A study from France used a statisticaltool to estimate the number of transfers
necessary for prociency.22 The authors
demonstrated signi
cant heterogeneityamong the trainees; between 11 and
99 embryo transfers were necessary. Inanother French study, Desparoir et al15
compared clinical pregnancy rates
among 2 attending physicians withgreater than 20 years of experience, 3
assistant physicians with 2-5 years of
experience, and 3 resident physicianswith less than 6 months of experience.
Pregnancy rates were 29.9% for attendingphysicians, 28.2% for assistant physicians,
and 19.1% for resident physicians. Their
ndings were potentially confounded bythe use of different catheters. In addition,
ultrasound guidance was not used and the
analysis did not control for other poten-
tial confounders, such as embryo qualityor the number of embryos transferred.Therefore, direct comparisons of preg-
nancy rates among the 3 groups cannotbe made.
In a recent study by Shah et al,16
pregnancy rates were comparable be-tween fellows and attending physicians
both before and after the implementa-
tion of a mandatory requirement of 100IUIs. As noted by the authors, their
analysis may have been underpowered to
detect a small increase in pregnancyrates.16 A learning curve for ETs was also
demonstrated. Seventy to 100 ETs werenecessary for fellowspregnancy rates to
exceed the attending physiciansmedian
pregnancy rate.16 Ultrasound guidanceand the afterload technique were typi-cally used only for difcult transfers.16
The present study was strengthened
by the consistent use of one embryotransfer technique. Furthermore, fellows
have always been allowed to perform ETs
since the institution of our program in2005. Therefore, the attending and
fellow ETs were synchronous in time.Additional strengths include the use of
live birth as the main outcome measure,
as well as the fact that the statisticalanalysis controlled for potential con-
founders such as patient age and the
number of high quality embryos trans-ferred. Anal strength was the inclusion
of onlyrst cycles, eliminating the needto adjust for prior failed cycles or mul-
tiple cycles experienced by the same
woman.Limitations of the present study in-
clude its retrospective design and re-latively small sample size. The study did
not have adequate power to detect smalldifferences in live birth rates between the
2 groups. Because data were analyzed
retrospectively, we were unable to con-trol for difculty of transfer. It is possible
that attending physicians were more
likely to perform difcult transfers;however, these data were not available. In
general, the assignment of an ET to anattending or fellow wasbasedon the day of
the week that the procedure was per-
formed. In addition, our study was per-formed at 1 academic center with a
relatively small number of attending phy-
sicians and fellows. Therefore, the external
validity of our study may be questioned.Finally, our study does not present dataregarding the effects of fellow-performed
ET on patient satisfaction. This is a po-tential area for future research.
In conclusion, live birth rates are
similar following ultrasound-guided em-bryo transfer with the afterload method
by attending physicians and REI fellows
at our academic institution. Our ndingssuggest that with appropriate supervision
and consistent technique, REI fellows
may obtain hands-on experience in ETwithout compromising a programs suc-
cess rates. -
REFERENCES
1. Hughes EG, King C, Wood EC.A prospectivestudy of prognostic factors in in vitro fertilizationand embryo transfer. Fertil Steril 1989;51:838-44.2. Padilla SL, Garcia JE. Effect of maternal ageand number of in vitro fertilization procedures onpregnancyoutcome.Fertil Steril1989;52:270-3.3. Roseboom TJ, Vermeiden JP, Schoute E,
et al. The probability of pregnancy after embryotransfer is affected by the age of the patient,
TABLE 3
IVF outcomes
Outcome
Attendingphysiciansn[ 760
Fellowsn[ 104
Crude OR(95% CI)
Adjusted OR(95% CI)
Clinical pregnancy 292 (38%) 40 (38%) 1.00 (0.66e1.53) 1.10 (0.71e1.71)
Live birth 239 (31%) 35 (34%) 0.90 (0.59e1.40) 0.99 (0.63e1.55)
Multiple birth 48 (6%) 7 (7%) 0.93 (0.41e2.12) 1.05 (0.45e2.44)
Values represent n (%) or OR (95% CI). ORs adjusted for maternal age and number of high quality embryos transferred.
CI, confidence interval; IVF, in vitro fertilization; OR, odds ratio.
Eaton. Live birth rates following embryo transfer by fellows vs attending physicians. Am J Obstet Gynecol 2014.
ajog.org Gynecology Research
NOVEMBER 2014 American Journal of Obstetrics &Gynecology 494.e4
http://refhub.elsevier.com/S0002-9378(14)00510-9/sref1http://refhub.elsevier.com/S0002-9378(14)00510-9/sref1http://refhub.elsevier.com/S0002-9378(14)00510-9/sref1http://refhub.elsevier.com/S0002-9378(14)00510-9/sref1http://refhub.elsevier.com/S0002-9378(14)00510-9/sref2http://refhub.elsevier.com/S0002-9378(14)00510-9/sref2http://refhub.elsevier.com/S0002-9378(14)00510-9/sref2http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://ajog.org/http://ajog.org/http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref2http://refhub.elsevier.com/S0002-9378(14)00510-9/sref2http://refhub.elsevier.com/S0002-9378(14)00510-9/sref2http://refhub.elsevier.com/S0002-9378(14)00510-9/sref1http://refhub.elsevier.com/S0002-9378(14)00510-9/sref1http://refhub.elsevier.com/S0002-9378(14)00510-9/sref1http://refhub.elsevier.com/S0002-9378(14)00510-9/sref17/25/2019 1-s2.0-S0002937814005109-main
5/5
cause of infertility, number of embryos trans-ferred and the average morphology score, asrevealed by multiple logistic regression analysis.Hum Reprod 1995;10:3035-41.4. Wisanto A, Janssens R, Deschacht J, et al.Performance of different embryo transfer cath-eters in a human in vitro fertilization program.Fertil Steril 1989;52:79-84.5. Gonen Y, Dirnfeld M, Goldman S, et al. Doesthe choice of catheter for embryo transfer inu-ence the success rate of in-vitro fertilization?Hum Reprod 1991;6:1092-4.6. Tang OS, Ng EH, So WW, et al. Ultrasound-guided embryo transfer: a prospective ran-domized controlled trial. Hum Reprod 2001;16:2310-5.7. Sallam HN, Sadek SS. Ultrasound-guidedembryo transfer: a meta-analysis of randomizedcontrolled trials. Fertil Steril 2003;80:1042-6.8. Buckett WM. A meta-analysis of ultrasound-guided versus clinical touch embryo transfer.Fertil Steril 2003;80:1037-41.
9. Angelini A, Brusco GF, Barnocchi N, et al.Impact of physician performing embryo transferon pregnancy rates in an assisted reproductiveprogram. J Assist Reprod Genet 2006;23:329-32.
10. Hearns-Stokes RM, Miller BT, Scott L, et al.Pregnancy rates after embryo transfer dependon the provider at embryo transfer. Fertil Steril2000;74:80-6.11. Karande VC, Morris R, Chapman C, et al.Impact of the physician factor on pregnancyrates in a large assisted reproductive technologyprogram: do too many cooks spoil the broth?
Fertil Steril 1999;71:1001-9.12. Yao Z, Vansteelandt S, Van der Elst J, et al.
The efcacy of the embryo transfer catheter inIVF and ICSI is operator-dependent: a random-ized clinical trial. Hum Reprod 2009;24:880-7.13. Wittenberger MD, Catherino WH,
Armstrong AY. Role of embryo transfer infellowship training. Fertil Steril 2007;88:1014-5.14. Papageorgiou TC, Hearns-Stokes RM,Leondires MP, et al. Training of providers inembryotransfer: what is theminimum number oftransfers required for prociency? Hum Reprod2001;16:1415-9.15. Desparoir A, Capelle M, Banet J, et al. Does
the experience of the provider affect pregnancyrates after embryo transfer? J Reprod Med2011;56:437-43.16. Shah DK, Missmer SA, Correia KF, et al.Efcacy of intrauterine inseminations as a
training modality for performing embryo transferin reproductive endocrinology and infertilityfellowship programs. Fertil Steril 2013;100:386-91.17. Bishop L, Brezina PR, Segars J. Training inembryo transfer: how should it be done? FertilSteril 2013;100:351-2.18. Neithardt AB, Segars JH, Hennessy S, et al.
Embryo afterloading: a renement in embryotransfer technique that may increase clinicalpregnancy. Fertil Steril 2005;83:710-4.19. Barber D, Egan D, Ross C, et al. Nursesperforming embryo transfer: successfuloutcome of in-vitro fertilization. Hum Reprod1996;11:105-8.20. Sinclair L, MorganC, LashenH, et al.Nursesperforming embryo transfer: the developmentand results of the Birmingham experience. HumReprod 1998;13:699-702.21. Barber D, Barlow D, Balen A. Fertility nursesdoing embryo transfers what is the impact oftraining? Hum Fertil (Camb) 2000;3:181-5.
22. Dessolle L, Freour T, Barriere P, et al. Howsoon can I be procient in embryo transfer?Lessons from the cumulative summation test forlearning curve (LC-CUSUM). Hum Reprod2010;25:380-6.
Research Gynecology ajog.org
494.e5 American Journal of Obstetrics &Gynecology NOVEMBER 2014
http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref4http://refhub.elsevier.com/S0002-9378(14)00510-9/sref4http://refhub.elsevier.com/S0002-9378(14)00510-9/sref4http://refhub.elsevier.com/S0002-9378(14)00510-9/sref4http://refhub.elsevier.com/S0002-9378(14)00510-9/sref5http://refhub.elsevier.com/S0002-9378(14)00510-9/sref5http://refhub.elsevier.com/S0002-9378(14)00510-9/sref5http://refhub.elsevier.com/S0002-9378(14)00510-9/sref5http://refhub.elsevier.com/S0002-9378(14)00510-9/sref5http://refhub.elsevier.com/S0002-9378(14)00510-9/sref5http://refhub.elsevier.com/S0002-9378(14)00510-9/sref6http://refhub.elsevier.com/S0002-9378(14)00510-9/sref6http://refhub.elsevier.com/S0002-9378(14)00510-9/sref6http://refhub.elsevier.com/S0002-9378(14)00510-9/sref6http://refhub.elsevier.com/S0002-9378(14)00510-9/sref7http://refhub.elsevier.com/S0002-9378(14)00510-9/sref7http://refhub.elsevier.com/S0002-9378(14)00510-9/sref7http://refhub.elsevier.com/S0002-9378(14)00510-9/sref8http://refhub.elsevier.com/S0002-9378(14)00510-9/sref8http://refhub.elsevier.com/S0002-9378(14)00510-9/sref8http://refhub.elsevier.com/S0002-9378(14)00510-9/sref9http://refhub.elsevier.com/S0002-9378(14)00510-9/sref9http://refhub.elsevier.com/S0002-9378(14)00510-9/sref9http://refhub.elsevier.com/S0002-9378(14)00510-9/sref9http://refhub.elsevier.com/S0002-9378(14)00510-9/sref9http://refhub.elsevier.com/S0002-9378(14)00510-9/sref10http://refhub.elsevier.com/S0002-9378(14)00510-9/sref10http://refhub.elsevier.com/S0002-9378(14)00510-9/sref10http://refhub.elsevier.com/S0002-9378(14)00510-9/sref10http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref12http://refhub.elsevier.com/S0002-9378(14)00510-9/sref12http://refhub.elsevier.com/S0002-9378(14)00510-9/sref12http://refhub.elsevier.com/S0002-9378(14)00510-9/sref12http://refhub.elsevier.com/S0002-9378(14)00510-9/sref12http://refhub.elsevier.com/S0002-9378(14)00510-9/sref12http://refhub.elsevier.com/S0002-9378(14)00510-9/sref13http://refhub.elsevier.com/S0002-9378(14)00510-9/sref13http://refhub.elsevier.com/S0002-9378(14)00510-9/sref13http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref15http://refhub.elsevier.com/S0002-9378(14)00510-9/sref15http://refhub.elsevier.com/S0002-9378(14)00510-9/sref15http://refhub.elsevier.com/S0002-9378(14)00510-9/sref15http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref17http://refhub.elsevier.com/S0002-9378(14)00510-9/sref17http://refhub.elsevier.com/S0002-9378(14)00510-9/sref17http://refhub.elsevier.com/S0002-9378(14)00510-9/sref18http://refhub.elsevier.com/S0002-9378(14)00510-9/sref18http://refhub.elsevier.com/S0002-9378(14)00510-9/sref18http://refhub.elsevier.com/S0002-9378(14)00510-9/sref18http://refhub.elsevier.com/S0002-9378(14)00510-9/sref18http://refhub.elsevier.com/S0002-9378(14)00510-9/sref18http://refhub.elsevier.com/S0002-9378(14)00510-9/sref19http://refhub.elsevier.com/S0002-9378(14)00510-9/sref19http://refhub.elsevier.com/S0002-9378(14)00510-9/sref19http://refhub.elsevier.com/S0002-9378(14)00510-9/sref19http://refhub.elsevier.com/S0002-9378(14)00510-9/sref20http://refhub.elsevier.com/S0002-9378(14)00510-9/sref20http://refhub.elsevier.com/S0002-9378(14)00510-9/sref20http://refhub.elsevier.com/S0002-9378(14)00510-9/sref20http://refhub.elsevier.com/S0002-9378(14)00510-9/sref21http://refhub.elsevier.com/S0002-9378(14)00510-9/sref21http://refhub.elsevier.com/S0002-9378(14)00510-9/sref21http://refhub.elsevier.com/S0002-9378(14)00510-9/sref21http://refhub.elsevier.com/S0002-9378(14)00510-9/sref21http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://ajog.org/http://ajog.org/http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://refhub.elsevier.com/S0002-9378(14)00510-9/sref22http://refhub.elsevier.com/S0002-9378(14)00510-9/sref21http://refhub.elsevier.com/S0002-9378(14)00510-9/sref21http://refhub.elsevier.com/S0002-9378(14)00510-9/sref21http://refhub.elsevier.com/S0002-9378(14)00510-9/sref20http://refhub.elsevier.com/S0002-9378(14)00510-9/sref20http://refhub.elsevier.com/S0002-9378(14)00510-9/sref20http://refhub.elsevier.com/S0002-9378(14)00510-9/sref20http://refhub.elsevier.com/S0002-9378(14)00510-9/sref19http://refhub.elsevier.com/S0002-9378(14)00510-9/sref19http://refhub.elsevier.com/S0002-9378(14)00510-9/sref19http://refhub.elsevier.com/S0002-9378(14)00510-9/sref19http://refhub.elsevier.com/S0002-9378(14)00510-9/sref18http://refhub.elsevier.com/S0002-9378(14)00510-9/sref18http://refhub.elsevier.com/S0002-9378(14)00510-9/sref18http://refhub.elsevier.com/S0002-9378(14)00510-9/sref18http://refhub.elsevier.com/S0002-9378(14)00510-9/sref17http://refhub.elsevier.com/S0002-9378(14)00510-9/sref17http://refhub.elsevier.com/S0002-9378(14)00510-9/sref17http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref16http://refhub.elsevier.com/S0002-9378(14)00510-9/sref15http://refhub.elsevier.com/S0002-9378(14)00510-9/sref15http://refhub.elsevier.com/S0002-9378(14)00510-9/sref15http://refhub.elsevier.com/S0002-9378(14)00510-9/sref15http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref14http://refhub.elsevier.com/S0002-9378(14)00510-9/sref13http://refhub.elsevier.com/S0002-9378(14)00510-9/sref13http://refhub.elsevier.com/S0002-9378(14)00510-9/sref13http://refhub.elsevier.com/S0002-9378(14)00510-9/sref12http://refhub.elsevier.com/S0002-9378(14)00510-9/sref12http://refhub.elsevier.com/S0002-9378(14)00510-9/sref12http://refhub.elsevier.com/S0002-9378(14)00510-9/sref12http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref11http://refhub.elsevier.com/S0002-9378(14)00510-9/sref10http://refhub.elsevier.com/S0002-9378(14)00510-9/sref10http://refhub.elsevier.com/S0002-9378(14)00510-9/sref10http://refhub.elsevier.com/S0002-9378(14)00510-9/sref10http://refhub.elsevier.com/S0002-9378(14)00510-9/sref9http://refhub.elsevier.com/S0002-9378(14)00510-9/sref9http://refhub.elsevier.com/S0002-9378(14)00510-9/sref9http://refhub.elsevier.com/S0002-9378(14)00510-9/sref9http://refhub.elsevier.com/S0002-9378(14)00510-9/sref9http://refhub.elsevier.com/S0002-9378(14)00510-9/sref8http://refhub.elsevier.com/S0002-9378(14)00510-9/sref8http://refhub.elsevier.com/S0002-9378(14)00510-9/sref8http://refhub.elsevier.com/S0002-9378(14)00510-9/sref7http://refhub.elsevier.com/S0002-9378(14)00510-9/sref7http://refhub.elsevier.com/S0002-9378(14)00510-9/sref7http://refhub.elsevier.com/S0002-9378(14)00510-9/sref6http://refhub.elsevier.com/S0002-9378(14)00510-9/sref6http://refhub.elsevier.com/S0002-9378(14)00510-9/sref6http://refhub.elsevier.com/S0002-9378(14)00510-9/sref6http://refhub.elsevier.com/S0002-9378(14)00510-9/sref5http://refhub.elsevier.com/S0002-9378(14)00510-9/sref5http://refhub.elsevier.com/S0002-9378(14)00510-9/sref5http://refhub.elsevier.com/S0002-9378(14)00510-9/sref5http://refhub.elsevier.com/S0002-9378(14)00510-9/sref4http://refhub.elsevier.com/S0002-9378(14)00510-9/sref4http://refhub.elsevier.com/S0002-9378(14)00510-9/sref4http://refhub.elsevier.com/S0002-9378(14)00510-9/sref4http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3http://refhub.elsevier.com/S0002-9378(14)00510-9/sref3