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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

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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,

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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.


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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. -

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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)

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CI, confidence interval; IVF, in vitro fertilization; OR, odds ratio.


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