Outcome of assisted reproductive technology in overweight and obese women

Abstract

Objective
The main objective of this study was to assess the prevalence of overweight and obesity among patients undergoing assisted reproductive technology (ART) in Latin America and its consequences on treatment outcomes.

Methods
We used the Latin American Registry of ART to obtain women's age and body mass index (BMI), cancellation rate, number of oocytes retrieved and embryos transferred, clinical pregnancy, live birth and miscarriage rates from 107.313 patients undergoing autologous IVF and ICSI during four years; a multivariable analysis was performed to determine the effect of BMI on cancellation, oocytes retrieved, pregnancy, live birth and miscarriage, adjusting for age, number of embryos transferred and embryo developmental stage upon embryo transfer, when appropriate.

Results
The prevalence of overweight and obesity was 16.1% and 42.4%, respectively; correcting for age of female partner, overweight and obesity were associated to an increase in the odds of cancellation and to a lower mean number of oocytes retrieved; after adjusting for age, number of embryos transferred and stage of embryo development at transfer, we found that the BMI category was not associated to a change in the likelihoods of pregnancy, live birth and miscarriage.

Conclusions
The prevalence of obesity among women seeking ART in Latin America is surprisingly high; however, BMI does not influence the outcome of ART performed in these women.

Full text

79
Received December 9, 2016
Accepted March 28, 2017
Original Article
Outcome of assisted reproductive technology in overweight and
obese women
Antonio MacKenna1,2, Juan Enrique Schwarze1,3, Javier A Crosby1,2, Fernando Zegers-Hochschild1,2,4
1Latin American Network of Assisted Reproduction
2Unit of Reproductive Medicine, Clinica Las Condes, Santiago, Chile
3Unit of Reproductive Medicine, Clinica Monteblanco, Santiago, Chile
4Program of Ethics and Public Policies in Human Reproduction, University Diego Portales, Santiago, Chile
ABSTRACT
Objective: The main objective of this study was to
assess the prevalence of overweight and obesity among
patients undergoing assisted reproductive technology
(ART) in Latin America and its consequences on treatment
outcomes.
Methods: We used the Latin American Registry of
ART to obtain women´s age and body mass index (BMI),
cancellation rate, number of oocytes retrieved and embryos
transferred, clinical pregnancy, live birth and miscarriage
rates from 107.313 patients undergoing autologous IVF
and ICSI during four years; a multivariable analysis was
performed to determine the eect of BMI on cancellation,
oocytes retrieved, pregnancy, live birth and miscarriage,
adjusting for age, number of embryos transferred and
embryo developmental stage upon embryo transfer, when
appropriate.
Results: The prevalence of overweight and obesity
was 16.1% and 42.4%, respectively; correcting for age
of female partner, overweight and obesity were associated
to an increase in the odds of cancellation and to a lower
mean number of oocytes retrieved; after adjusting for
age, number of embryos transferred and stage of embryo
development at transfer, we found that the BMI category
was not associated to a change in the likelihoods of
pregnancy, live birth and miscarriage.
Conclusions: The prevalence of obesity among women
seeking ART in Latin America is surprisingly high; however,
BMI does not inuence the outcome of ART performed in
these women.
Keywords: ART, BMI, obesity, clinical pregnancy, live
birth, miscarriage
JBRA Assisted Reproduction 2017;21(2):79-83
doi: 10.5935/1518-0557.20170020
INTRODUCTION
The prevalence of overweight and obesity, dened
by World Health Organization (WHO) as a body mass
index (BMI) of 25-30kg/m2 and ≥30kg/m2 (WHO, 2004),
respectively, is increasing worldwide as an epidemic, and
has become a serious health problem. Rivera et al. (2014)
reported that nearly 30% of the Latin American population
is obese. If current trends continue, it is estimated that by
the year 2030 up to 80% of the Latin American and the
Caribbean adult population could be overweight or obese
(Kelly et al., 2008).
It has been demonstrated that the time required
to achieve a spontaneous pregnancy is longer in obese
women (Gesink Law et al., 2007) and the probability of
pregnancy is reduced by 5% per unit of BMI exceeding
29kg/m2 (van der Steeg et al., 2008). Jungheim & Moley
(2010) suggested that obesity in women increases the
risk of infertility by impairing ovulation, oocyte quality,
fertilization, embryo quality and implantation. Due to
the relationship between higher BMI and infertility, many
overweight and obese women must undergo treatment
by assisted reproductive technologies (ART). Luke et al.
(2011) reported that 23.4% of the women undergoing
ART in the United States of America (USA) during 2007
were overweight and 16.5% were obese, and Provost
et al. (2016) showed a similar prevalence of overweight
(22.9%) and obesity (17.8%) within patients needing ART
in USA from 2008 to 2010.
The available evidence about the eects of BMI on the
outcome of ART is conicting. It has been suggested that
obese patients require higher doses of gonadotropins, have
a lower response to ovarian stimulation, higher cancellation
rates, reduced number of oocytes retrieved, poorer oocyte
quality, lower fertilization rates, less number of mature
oocytes and poorer embryo quality (Pandey et al., 2010).
DeUgarte et al. (2010) also showed that women with a BMI
≥ 35kg/m2 have lower implantation, pregnancy and live
birth rates than women with BMI < 35kg/m2. Moreover,
Luke et al. (2011) found reduced pregnancy rates with
autologous but not with donor oocytes in obese women,
suggesting impaired oocytes and poor embryo quality.
A recent report based on data from the Society for
Assisted Reproductive Technology Registry (SART) showed
that the prevalence of overweight and obesity was 22.9%
and 17.8%, respectively, and pregnancy outcomes were
more favorable in women with normal BMI, and it worsens
as BMI increases (Provost et al., 2016).
There are no studies regarding the prevalence of
overweight and obesity among women undergoing ART
in Latin America and its consequences on treatment
outcomes. The main objective of this study was to obtain
this missing evidence.
MATERIALS AND METHODS
Data was obtained from the Latin American Registry
of ART (RLA). The RLA collects information from centers
in fteen Latin American countries. Patients admitted for
autologous in vitro fertilization (IVF) and intra-cytoplasmic
sperm injection (ICSI) with fresh embryo transfer started
between January 1st, 2010 and December 31st, 2014, and
babies born up to September of 2015, were included in
this study.
As part of the accreditation process, all participating
institutions agreed to have their data registered and
published by the RLA (Zegers-Hochschild et al., 2016).
Data used for the current study were women´s ages,
weights and heights, cancellation rates, numbers of
oocytes retrieved, numbers of embryos transferred, clinical
pregnancy rates and live birth rates per initiated cycle,
and miscarriage rates (following RLA rules, there was no
missing information). We used the terminology published
by the International Committee Monitoring Assisted
Reproductive Technologies (ICMART) and the WHO 2009
glossary (Zegers-Hochschild et al., 2009).

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JBRA Assist. Reprod. | v.21 | no2| Apr-May-Jun/ 2017
BMI was calculated by dividing body mass (weight
in kilograms) by the square of body height in meters.
We stratied BMI in four categories, according to the
WHO classication (WHO, 2004): BMI ≤ 18.4kg/m2
(underweight), 18.5-24.9 kg/m2 (normal weight), BMI 25-
30kg/m2 (overweight) and BMI ≥ 30kg/m2 (obese).
The parametric data was described as means and
standard deviation, and non-parametric data by median
and ranges. To compare dierences in groups we used the
Chi square test and the Mann-Whitney-u test for categorical
and non-parametric variables, respectively.
We performed a multivariable analysis to determine the
eects of BMI on cancellation, number of oocytes retrieved,
pregnancy, live birth and miscarriage rates, adjusting
for age, number of embryos transferred and embryo
developmental stage upon embryo transfer (embryos at
cleavage stage or blastocysts), when appropriate. Results
from women with normal BMI were used as the reference
group. A p-value below 0.01 was considered statistically
signicant.
RESULTS
We analyzed a total of 107.313 patients admitted
for autologous IVF and ICSI, who underwent ovulation
induction for ART in Latin America during the study period.
All patients with initiated cycles were included in the study,
therefore some of them were cancelled previous oocyte
retrieval, other cancelled because lack of fertilization
or embryo development and the vast majority of them
reached fresh embryo transfer, either of cleavage stage
embryos or blastocysts (no frozen embryo transfers were
included). Their mean age (±SD) was 36.4±4.6 years
old and their prevalence rates regarding overweight and
obesity were 16.1% and 42.4%, respectively.
Table 1 shows the women´s ages, cancellation
rates, numbers of oocytes and the numbers of embryos
transferred in each BMI category. No signicant dierence
was found in age and number of embryos transferred
between the categories. Clinical pregnancy rates and live
birth rates per initiated cycle and miscarriage rates in each
BMI category are shown on table 2. If no adjustments are
made for women´s ages, numbers of embryos transferred
and the stages of embryo development at transfer, the
pregnancy and live birth rates become statistically lower in
obese patients when compared with women having normal
BMIs. Miscarriage rates varied from 15.9% to 18.4%,
without dierences according to BMI category.
Table 3 shows the outcomes of the multivariable
analyses. Correcting for age of the female partner,
overweight and obesity were associated to an increase in
the likelihood of cancellation and to a lower mean number
of oocytes retrieved, when compared to those with normal
BMIs. On the other hand, after adjusting for confounding
variables such as age, number of embryos transferred and
stage of embryo development upon transfer, we found that
the BMI category was not associated with changes in the
likelihoods of pregnancy, live birth and miscarriage.
DISCUSSION
We found that the proportion of overweight and
obese women treated with ART in Latin America between
2010 and 2014 reached 16.1% and 42.4%, respectively.
Intentionally, we decided to assess results per women
with initiated cycles, because such analysis oers better
epidemiological information for healthcare providers who
must counsel their patients. Consequently, we found
that an increase in BMI was associated to an increase in
cancellation and a reduced number of retrieved oocytes,
but did not aect the odds of clinical pregnancy, live birth
and miscarriage.
The main strength of our study is the large number
of cases and the thoroughness of the RLA database that
allows adjustment for the most relevant confounding
variables. It also represents results from dierent centers
located in dierent countries, thus conferring external
validity. However, potential limitations of the current study
are that we did not consider the possible eect of the male
partner and polycystic ovary syndrome, more commonly
diagnosed among obese women, on ART outcomes;
although Provost et al. (2016) recently suggested that it is
the BMI itself, rather than the underlying pathologies, that
contributes to the outcomes.
The prevalence of obese patients among Latin American
women undergoing ART is surprisingly higher than in any
other report published so far. Indeed, in the other large
multicentric studies, undertaken in the USA, only 16.5%
and 17.8% of patients undergoing ART were obese (Luke
et al., 2011; Provost et al., 2016). This issue could be
explained because of the rapid epidemiological changes
in most developing countries over the last decades, with
a nutritional transition, which impacts on the quality of
food, resulting in a declining of malnutrition rates, but an
increase in overweight and obesity (Rivera et al., 2004),
due to a change in dietary intake and energy expenditure,
inuenced by demographic, environmental, economic,
psychosocial and cultural factors (Barria & Amigo,
2006). Sedentary behavior and highly caloric diets, with
an increase intake of processed foods containing large
amounts of rened sugars and saturated fats, have been
described as the main causes of obesity in Latin America
and other developing countries (Pearson et al., 2014;
Popkin et al., 2012).
The group of overweight and obese women in our study
had signicantly more cycles cancelled. They also had
signicantly less oocytes retrieved, if compared with women
with normal BMI, and correcting by age, although this is of
little clinical signicance. Cancellation rates were four-fold
higher in obese patients than in women with a BMI < 30kg/
m2; however, this was much lower than cancellation rates
reported by Provost et al. (2016). Pinborg et al. (2011) also
showed an increase in the likelihood of cycle cancellation,
after adjusting for age. Moreover, Pinborg et al. (2011)
and Zander-Fox et al. (2012) also reported a signicantly
lower number of oocytes retrieved in obese patients.
In our study, after adjusting for known confounding
factors (age, number of embryos transferred and stage
of embryo development upon transfer), overweight and
obesity were not associated with a decrease in the odds
of pregnancy and live birth or an increase in the odds of
miscarriage. Several studies have reported that women
with overweight and obesity undergoing ART have lower
pregnancy and/or live birth rates, when compared with
patients with normal BMI (Tamer Erel & Senturk, 2009;
Orvieto et al., 2009; Bellver et al., 2010; Rittenberg et al.,
2011; Singh et al., 2012; Chavarro et al., 2012; Provost
et al., 2016). Moreover, the meta-analysis performed by
Rittenberg et al. (2011) also showed increased miscarriage
rates in obese patients undergoing ART. On the other
hand, other authors have reported no changes in ART
outcomes within dierent BMI categories (Sathya et al.,
2010; Vilarino et al., 2011; Zander-Fox et al., 2012).
However, none of these studies adjusted results for
known confounding factors, i.e. woman´s age, number
of embryos transferred and stage of embryo development
upon transfer. If the results from the current study are
analyzed without considering these variables, it also shows
a signicant dierence between women with normal weight
and obese patients, but this dierence disappears when
a multivariable analysis is performed to adjust results for
confounding variables.

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Women´s BMI and ART - MacKenna, A.
JBRA Assist. Reprod. | v.21 | no2| Apr-May-Jun/ 2017
BMI ≤18.4 18.5-24.9 25.0-29.9 ≥30.0
Nº cycles 1.436 43.130 17.247 45.500
Age (years) * 35.0±4.6 35.8±4.5 36.0±4.6 36.0±4.6 §
Cancellation rates (%) †2.14 2.08 (A) 2.51 5.7 (B)
Nº oocytes retrieved ‡9.1 (0-58) 8.9 (0-80) (C) 9.0 (0-70) 8.1 (0-73) (D)
Nº embryos transferred ‡2.1 (1-6) 2.1 (1-6) 2.1 (1-5) 2.1 (1-6) §
* Means±SD. (A) vs (B) p<0.0001; † Per initiated cycle.(C) vs (D) p<0.0001; ‡ Medians (ranges). § NS.
Table 1. Age, cancellation rates, number of oocytes retrieved and number of embryos transferred in women undergoing
107.313 cycles of autologous FIV/ICSI, according to BMI
BMI ≤18.4 18.5-24.9 25.0-29.9 ≥30
Nº cycles 1.436 43.130 17.247 45.500
Pregnancy rates (%) * 25.83 25.52 (A) 26.53 23.27 (B)
Live birth rates (%) * 21.24 20.55 (C) 21.32 18.68 (D)
Miscarriage rates (%) 15.90 17.98 18.40 18.33 †
Table 2. Clinical pregnancy, live birth and miscarriage rates in women undergoing 107.313 cycles of autologous FIV/ICSI,
according to BMI
* Per initiated cycle; (A) vs (B) p<0.0001; † NS.; (C) vs (D) p<0.0001.
Cancellation* Nº oocytes
retrieved †Pregnancy ‡Live birth ‡Miscarriage ‡
Underweight BMI
≤18.4(kg/m2)
OR 1.00 (0.68 to
1.46) p=0.995
β -0.27 (-0.62 to
0.08) p=0.695
OR 1.03 (0.91 to
1.18) p=0.629
OR 1.04 (0.91 to
1.20) p=0.552
OR 0.94 (0.79 to
1.26) p=0.695
Overweight BMI
25-29.9(kg/m2)
OR 1.18 (1.05 to
1.32 p=0.005
β 0.20 (0.08 to
0.31) p=0.001
OR 1.00 (0.96 to
1.05) p=0.811
OR 1.0 (0.95 to
1.05) p=0.927
OR 1.0 (0.92 to
1.10) p=0.881
Obesity BMI
≥30(kg/m2)
OR 2.78 (2.58 to
3.01) p<0.0001
β -0.79 (-0.88 to
0.70) p<0.0001
OR 0.96 (0.93 to
1.00) p=0.025
OR 0.96 (0.93 to
0.99) p=0.039
OR 1.01 (0.95 to
1.09) p=0.693
* Results are adjusted for age and presented as odd ratios (95% condence interval) and p-value. † Results are adjusted
for age and presented as coecient β of medians (95% condence interval) and p-value. ‡ Results are adjusted for age,
number of embryos transferred and embryo stage at embryo transfer and presented as odd ratios (95% condence interval)
and p-value.
Table 3. Multivariable analysis adjusting for age, number of embryos transferred and stage of embryo development upon
transfer on predictors of ART outcome, according to abnormal BMI categories in women undergoing 107.313 cycles of
autologous FIV/ICSI
Some authors have used multivariable analyses to
adjust results for confounding variables: Sneed et al.
(2008) adjusted results for age and showed that BMI did not
have a major eect on ART outcome; Pinborg et al. (2011)
corrected results for age, social class, diagnosis and duration
of infertility, demonstrating that pregnancy and live birth
rates were signicantly lower in obese women undergoing
their rst ART cycle; Petersen et al. (2013) adjusted results
for age and smoking, reporting reduced live birth rates as
BMI increased; and Schliep et al. (2015) corrected results
for age and parity, showing no dierences in ART success
among dierent BMI categories. Moreover, Veleva et al.
(2008) adjusting results for age, diagnosis and history
of miscarriage, reported an increased risk of miscarriage
in women with overweight and obesity. However, none of
these authors adjusted results for woman´s age, number
of embryos transferred and stage of embryo development
upon transfer together, as we did in our study.
Furthermore, Luke et al. (2011), Provost et al. (2016)
and Moragianni et al. (2012) used multivariable analyses to
correct results for several confounding variables including
age, number of embryos transferred and day of embryo
transfer. The rst two authors used data from the SART
registry and showed that an increased BMI was associated
with signicantly greater odds of failure to achieve clinical
intrauterine pregnancy and live birth. Provost et al. (2016)
also reported signicantly higher miscarriage rates with
increasing BMI categories. Using data from a single center,
Moragianni et al. (2012) showed that the odds of clinical
pregnancy and live births were lower and the odds of
miscarriage were higher in women with BMI ≥ 30kg/m2.
These authors concluded that higher BMI is associated
with a signicant impairment on ART outcomes. We could
not reach the same conclusions, which may be due to a
possible role of ethnicity on ART results. All these studies
were performed in the USA and Luke et al. (2011), the
only author reporting ethnicity, had 6% of Hispanic women
among their subjects, against most Hispanic women in our
study, which was not registered, for demographic reasons,
but expected. In a recent systematic review, performed
by Humphries et al. (2016), the authors concluded that
there are signicant disparities in pregnancy and live
birth rates after ART by ethnicity; however, most available
studies are limited by sample size, selection bias (dierent
denitions of race and ethnicity), extensive missing data
and inadequate adjustment for confounding variables.

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JBRA Assist. Reprod. | v.21 | no2| Apr-May-Jun/ 2017
On the other hand, given the high prevalence of obesity
among women undergoing ART in Latin America, patients
have to be aware of the maternal and neonatal risks derived
from obesity and should be advised to lose weight before
undergoing ART. Recently, a large cohort study showed
that relative risks of gestational diabetes, preeclampsia,
fetal macrosomia, cesarean delivery, blood loss, neonatal
hypoglycemia and respiratory distress syndrome increase
as BMI increases over 25kg/m2 (Schuster et al., 2016).
Moreover, Koning et al. (2010) suggested that overweight
and obesity in ovulatory infertile women leads to a 44%
and 70% increase in costs due to pregnancy complications,
respectively. A recently published study by Kaye et al.
(2016) suggested how relevant it is to develop reasonable
standards of care for obese patients, to encourage them
to lose weight before undergoing fertility treatment, giving
priority to safety and overall health status, although
patient’s autonomy must be balanced with non-malecence
and the avoidance of interventions that may be unsafe
both immediately and in the long run.
In summary, we found that BMI does not inuence the
outcomes of ART performed in Latin American women,
nevertheless, considering maternal and neonatal risks,
overweight and obese patients should be advised to
lose weight before undergoing ART. Future studies are
needed to assess the role of ethnicity on ART results and
the underlying causes of trans-ethnical dierences on
outcomes between women having similar BMI.
ACKNOWLEDGEMENTS
Thanks to Carolina Musri, the RLA administrator, and
all members of centers reporting to RLA for their eorts,
which enabled this study.
CONFLICT OF INTERESTS
The authors have no conict of interests to report.
Corresponding author:
Antonio MacKenna
Unit of Reproductive Medicine,
Clinica Las Condes
Santiago, Chile
E-mail: amackenn@clc.cl
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