FERTILITY AND STERILITY威

VOL. 82, NO. 4, OCTOBER 2004

Copyright ©2004 American Society for Reproductive Medicine
Published by Elsevier Inc.
Printed on acid-free paper in U.S.A.

Treatment with piroxicam before embryo

transfer increases the pregnancy rate after
in vitro fertilization and embryo transfer
Hwa Sook Moon, M.D., Ph.D., Sea Hee Park, M.S., Ju Ok Lee, B.S.,
Kyung Seo Kim, M.D., and Bo Sun Joo, Ph.D.
Center for Reproductive Medicine and Infertility, Department of Obstetrics and Gynecology, Good Moon-Hwa
Hospital, Busan, Korea

Objective: To examine the effect of ␤-cyclodextrin piroxicam treatment for priming of the uterus on the
pregnancy outcome of IVF– embryo transfer (ET) programs.
Design: Prospective, randomized, double-blinded placebo-controlled clinical study.
Setting: Large urban medical center.
Patient(s): One hundred eighty-eight consecutive cycles of fresh IVF–ET and 78 cycles of frozen–thawed ET.
The patients underwent IVF because of tubal, male infertility, unexplained, or endometriosis factors. They
were randomly divided into treatment and control groups.
Intervention(s): In the treatment group, 94 cycles in fresh ET and 39 cycles in frozen–thawed ET the patients
received an oral dose of 10 mg of piroxicam. In the control group, the same number cycles corresponding to
the treatment group were treated with placebo. Both groups started piroxicam or placebo treatment 1–2 hours
before ET. Patients and staff were blinded to the treatment.
Main Outcome Measure(s): Implantation rate (IR) and pregnancy rate (PR).
Result(s): Piroxicam increased significantly IR (18.7%) and PR (46.8%) compared to the control group (8.6%
and 27.6%, respectively) in fresh cycles. With the exception of an unexplained factor, patients with the tubal,
male infertility, or endometriosis factor had significantly higher PR in the treatment group compared to the
control group. The beneficial effect of piroxicam was found in patients less than 40 years old, but was not
found in patients more than 40 years. In frozen–thawed cycles, there were statistically significant differences
between the treatment group and the control group in IR (9.4% vs. 2.3%) and PR (25.6% vs. 7.7%),
respectively.
Conclusion(s): Our study showed that piroxicam increases IR and PR after IVF–ET in both fresh and
frozen–thawed ET cycles. The beneficial effect seems to be more remarkable in patients less than 40 years old
with tubal, male infertility, or endometriosis factors. These results suggest that piroxicam treatment before ET
is very effective in the priming of a uterus suitable for embryo implantation. This is the first study to
investigate the possible consequence of piroxicam for improving the PR after IVF–ET. (Fertil Steril威 2004;
82:816 –20. ©2004 by American Society for Reproductive Medicine.)
Key Words: ␤-Cyclodextrin piroxicam, pregnancy outcome, uterine contractility

Received April 17, 2003;
revised and accepted
February 17, 2004.
Reprint requests: Bo Sun
Joo, Ph.D., Center for
Reproductive Medicine and
Infertility, Good Moon-Hwa
Hospital, 899-8 Bum-il
Dong, Busan 601-062,
Korea (FAX: 82-51-630-
0750; E-mail: bosunjoo@
hotmail.com).
0015-0282/04/$30.00
doi:10.1016/j.fertnstert.2004.
02.140
During the past 20 years numerous studies
have been made to improve the implantation
process. Most of their attempts have been
focused on the induction and selection of the
best quality embryos and the improvement of
uterus receptivity. Several developments in
controlled ovarian hyperstimulation (COH),
fertilization, and embryo culture techniques
have contributed to the improvement of the
quality of embryos available for ET. In con-
trast, little development has increased the
uterus receptivity.
Practical limitations in the evaluation and
improvement of uterine receptivity may be in-
fluenced by several factors. First, no one factor
was considered to play a critical determining
role in the establishment of uterus receptivity
for implantation because the events of implan-
tation are regulated by a complex morpholog-
ical and biochemical change of the endome-
trium (1). Thus all of these factors should be
investigated simultaneously to clearly assess
the receptivity status of the endometrium. Sec-
ond, tissue sampling for the direct assessment

816
of markers of uterine receptivity is inherently impossible in
the actual ET cycles.
Recently many researchers have focused on noninvasive
prognostic factors of uterine receptivity with the advent of
high resolution ultrasound probes, which permitted the direct
visualization of the uterine contractile activity (2, 3). The
uterus has typically three patterns of contractility throughout
the menstrual cycle that influence embryo implantation (4 –
7). Uterine contraction at the time of ET alters pregnancy
rates (PRs) after IVF (8). These results suggest that uterine
contractility can be an important factor in determining en-
dometrial receptivity as well as an alternative noninvasive
prognostic factor (9). In this respect, treatment of adjuvants,
such as uterine relaxants, should be considered to prime of a
uterus suitable for embryo implantation.
Prostaglandin, which is synthesized from arachidonic
acid by cyclooxygenase (COX), stimulates uterine contrac-
tion. Nonsteroidal anti-inflammatory drugs (NSAIDs) block
the action of COX and inhibit the production of prostaglan-
din (10). This result indicates that NSAIDs may cause the
reduction of uterine contractility. To date, no reports have
evaluated NSAIDs with the purpose of improving a preg-
nancy outcome after IVF–ET. Piroxicam is the most effec-
tive of all NSAIDs in the clinical relief of dysmenorrhea
(10). The aim of this study was to examine the effect of
piroxicam treatment for the priming of the uterus on the
pregnancy outcome in IVF–ET programs.
MATERIALS AND METHODS
This study was performed on 188 consecutive cycles of fresh
IVF–ET and 78 cycles of frozen–thawed ET from March
1998 to February 2000 at the Center for Reproductive Med-
icine of Good Moon-Hwa Hospital. The study included
women who underwent IVF because of tubal, male infertil-
ity, unexplained, or endometriosis factor. Written informed
consent was obtained from all patients. This study was
approved by the Institutional Review Board of the Human
Investigation Committee of Good Moon-Hwa Hospital.
Controlled Ovarian Hyperstimulation and
IVF Procedures
Controlled ovarian hyperstimulation (COH) was per-
formed by a long standard protocol with GnRH agonist
(GnRH-a; Lucrin, Johannesburg Abbott, France), hMG
(IVF-M; LG Inc., Iksan, Korea), and highly purified FSH
(hpFSH; Follimon, LG Inc.). In brief, GnRH-a was given
daily at a dose of 1 mg until a serum E2 level was obtained
to assess whether adequate suppression had been achieved.
When ovarian suppression was observed by serum E2 and
FSH levels on the third day of the menstrual cycle, GnRH-a
was given daily at a dose of 0.5 mg in the morning and one
or two ampules of 75 IU of hMG and hpFSH were given IM
in the evening, depending on the follicular development.
FERTILITY & STERILITY威
Follicular development was assessed by transvaginal ul-
trasonography. When at least two dominant follicles were 18
mm or larger, the serum E2 level was measured and 10,000
IU of hCG (IVF-C, LG Inc.) was administered.
Oocyte retrieval by transvaginal ultrasonographic guid-
ance was performed approximately 36 hours after the hCG
administration. Follicular aspirates were transferred into
60-mm tissue culture dishes (Falcon 3002; Becton Dickin-
son, Lincoln Park, NJ). Oocyte– cumulus cell complexes
were isolated under a dissecting microscope (SZH, Olym-
pus, Tokyo, Japan). The maturity and quality of each oo-
cyte– cumulus cell complex was graded under inverted phase
contrast microscope (Olympus IX 70, Olympus) by spread-
ing each oocyte– cumulus cell complex on one line of the
surface of 60-mm culture dishes. Oocytes with first polar
body and extensive cumulus cells were regarded as mature.
Four or five oocytes were placed into each organ culture
dish (Falcon 3037; Becton Dickinson) containing 0.9 mL of
glucose-free mHTF medium supplemented with 10% follic-
ular fluid (FF). Highly motile spermatozoa were collected by
a discontinuous three-layered percoll gradient (100%–90%–
50%) and suspended in glucose-containing HTF medium
with 10% FF. Then they were inseminated 4 –12 hours after
oocyte retrieval, depending on the oocyte maturity.
Fertilization was confirmed 16 –20 hours after insemina-
tion by visualization of two pronuclei. Fertilized oocytes
were transferred to fresh mHTF medium with 20% FF, and
then cultured for 24 hours or more, followed by co-culture
with autologous cumulus cells in glucose-containing HTF
with 20% FF. After co-culture, embryos were graded based
on the size of the blastomere and the presence of fragmen-
tation, using Bolton’s definition (11), just before ET. The ET
was performed with Embryon transfer catheter (Rocket med-
ical, Waterford, United Kingdom) 3 days after oocyte recov-
ery in fresh cycles and 3 days after ovulation in frozen–
thawed cycles.
Piroxicam Treatment
The 188 fresh IVF–ET cycles and 78 frozen–thawed ET
cycles were randomly divided into treatment and control
groups. In the fresh ET cycles, the treatment group (94
cycles) received an oral dose of 10 mg of piroxicam (Brexin;
Kolon Inc., Daejeon, Korea), and the control group (94
cycles) received a placebo. In the frozen–thawed ET cycles,
39 cycles received 10 mg of piroxicam orally (treatment
group) and 39 cycles were treated with placebo (control
group). Both groups started piroxicam or placebo treatment
1–2 hours before ET. Patients and staff were blinded to the
treatment.
Statistical Analysis
All data were presented as mean ⫾ SD. Statistical anal-
ysis was carried out using the unpaired Student’s t-test and
␹2-test. A P value ⬍.05 was considered statistically signif-
icant.
817
 TABLE 1 TABLE 3

Patient characteristics in the control and piroxicam Comparison of pregnancy rates according to the infertility
treatment groups. causes.
Control Piroxicam treatment Infertility causes Control Piroxicam treatment

No. of cases 94 94 Male 4/17 (23.5%) 7/16 (43.8%)a

Age (y) 32.7 ⫾ 4.3 33.2 ⫾ 4.7 Tubal 15/57 (26.3%) 24/50 (48.0%)a
Parity 0.1 ⫾ 0.3 0.2 ⫾ 0.5 Endometriosis 2/7 (28.5%) 5/10 (50.0%)a
Basal FSH (mIU/mL) 4.9 ⫾ 1.8 4.7 ⫾ 2.1 Unexplained 5/13 (38.5%) 8/18 (44.4%)
LH (mIU/mL) 2.9 ⫾ 1.8 3.0 ⫾ 1.2 a
P⬍.05 (vs. control group).
E2 (pg/mL) 38.7 ⫾ 23.5 35.4 ⫾ 19.8
E2 (pg/mL) on the hCG 2,937 ⫾ 1,678 3,726 ⫾ 1,834 Moon. Piroxicam increases pregnancy rate of IVF. Fertil Steril 2004.
administration
No. of oocytes retrieved 10.9 ⫾ 6.2 11.3 ⫾ 6.4
No. of embryos transferred 4.0 ⫾ 2.0 4.0 ⫾ 2.1 no beneficial effect of piroxicam was found in unexplained
No. of grade A embryoa 6.1 ⫾ 2.5 6.7 ⫾ 1.7 infertile patients (Table 3).
a
Grade A embryo is the best quality embryo with even-sized blastomere and
no fragmentation.
Piroxicam treatment resulted in a significant increase in
PR in patients less than 40 years old (P⬍.05), but not in
Moon. Piroxicam increases pregnancy rate of IVF. Fertil Steril 2004.
patients more than 40 years (Table 4).
Of 78 cycles of frozen–thawed ET, 39 cycles were treated
RESULTS with piroxicam. The number and quality of embryos trans-
ferred was similar in both groups. The implantation rate and
The mean age (⫾SD) of patients was 32.7 (⫾4.3) years in
clinical PR were 9.4% and 25.6% in the piroxicam-treated
the control group and 33.0 (⫾4.8) years in the piroxicam
group, which were significantly higher than in the control
treatment group. The mean number of retrieved oocytes was
group (2.3% and 7.7%, respectively) (P⬍.05; Table 5).
10 in the control group and 11 in the piroxicam treatment
group. The mean number of embryos transferred was four in
both groups. The woman’s age, parity, ovarian reserve, or E2 DISCUSSION
level on the day of hCG administration was not significantly This study shows higher rates of implantation and preg-
different in both groups. The number of oocytes retrieved, nancy with piroxicam treatment before ET. This is the first
number of embryos transferred, and the quality of embryo study to date that focused on the use of piroxicam for
transferred also showed no significant differences (Table 1). priming the uterus to improve the pregnancy rate after IVF–
ET.
The implantation rate and the clinical pregnancy rate
(PR) were 8.6% and 27.6% in the control group, and Piroxicam is a NSAID and is a risk factor C in pregnancy.
18.7% and 46.8% in the piroxicam treatment group. The The use of NSAIDs during pregnancy has not been associ-
implantation rate and PR were significantly higher in the ated with congenital malformations, preterm delivery, or low
piroxicam treatment group compared with the control birth weight, but two reports showed adverse effects of
group (P⬍.05; Table 2). NSAIDs during pregnancy. One states that NSAIDs block
blastocyst implantation by inhibiting blastocyst hatching (10,
When the PRs were compared according to the causes of
12). The other reports that the use of NSAIDs might be
infertility, piroxicam treatment increased about twice as
associated with spontaneous abortion (13). However, there
much in patients with tubal, male infertility, or endometrio-
are no reports concerning any adverse effects from one dose
sis factors compared to the control group (P⬍.05). However,

TABLE 4
TABLE 2
Comparison of pregnancy rate with the age of patients.
IVF–ET outcomes in the control and piroxicam treatment
groups. Age Control Piroxicam treatment

Control Piroxicam treatment ⱖ30 9/28 (32.1%) 19/36 (52.8%)a

31–35 14/48 (29.2%) 19/41 (46.3%)a
Implantation rate 8.6% 18.7%a 35–40 2/8 (25.0%) 5/11 (45.5%)a
Clinical pregnancy rate 27.6% (26/94) 46.8% (44/94)a ⱕ40 1/10 (10.0%) 1/6 (16.6%)
a a
P⬍.05 (vs. control group). P⬍.05 (vs. control group).
Moon. Piroxicam increases pregnancy rate of IVF. Fertil Steril 2004. Moon. Piroxicam increases pregnancy rate of IVF. Fertil Steril 2004.

818 Moon et al. Piroxicam increases pregnancy rate of IVF Vol. 82, No. 4, October 2004

TABLE 5
Pregnancy outcomes in frozen–thawed ET cycles.
Piroxicam
Control treatment
No. of cases 39 39
No. of embryos transferred 4.0 ⫾ 2.3 3.7 ⫾ 1.8
No. of grade A embryoa 2.7 ⫾ 0.5 2.8 ⫾ 0.2
Implantation rate 2.3% 9.4%b
Clinical pregnancy rate 7.7% (3 cases) 25.6% (10 cases)b
a
Grade A embryo is the best quality embryo with even sized blastomere and
no fragmentation.
b ation on uterine contractility is looked at in our present
P⬍.05 (vs. control group).
Moon. Piroxicam increases pregnancy rate of IVF. Fertil Steril 2004.
(10 mg) of piroxicam during the preimplantation period. Our
present study does not show any increase in spontaneous
abortion as well as malformation after piroxicam treatment
compared to the control group in IVF–ET.
The cause for this beneficial effect of piroxicam may be
postulated in two aspects. First, piroxicam treatment may re-
duce uterine contractility. IJland et al. (5) found that concep-
tional cycles had less endometrial wavelike activity compared
with nonconception cycles in spontaneous cycles. High fre-
quency contractions of uterus at the time of ET are associated
with poorer implantation (8) and poorer IVF–ET outcome (14).
These results mean that uterine contractility influences embryo
implantation.
Uterine contractility is stimulated by prostaglandins (PGs)
synthesized by COX (10). The NSAIDs block the action of
COX and inhibit the production of PGs (15), probably resulting
in the decrease of uterine contractility. In this respect, the one
time oral treatment with piroxicam on the day of ET seems to
increase the implantation of human blastocyst by calming uter-
ine contraction rather than inhibiting embryo development and
blastocyst hatching.
Second is the increase of uterine blood flow with piroxi-
cam treatment. A few studies used aspirin, another inhibitor
of PG, to improve the pregnancy outcome of IVF–ET. They
concluded that low-dose aspirin improved implantation rates
and PRs in IVF patients (16 –18). Rubinstein et al. (18)
explained that the effect of aspirin is attributable to an
increase in uterine blood flow.
Studies similar to ours were conducted by Fanchin (19)
and Ayoubi (20) and their colleagues. Uterine contractions
are increased by rising E2 levels during the follicular phase
(21–23) and are reduced by P exerted during the luteal phase
(21, 24, 25). These researchers administered vaginal P start-
ing on the day of oocyte retrieval to relax uterine contrac-
tility at the time of ET. As a result, they found a decrease in
uterine contraction frequency on the day of ET, suggesting
that a uterine relaxation effect by P administration before ET
is likely to improve IVF–ET outcome.
FERTILITY & STERILITY威
Uterine contractility follows three characteristic pat-
terns according to the phase of the menstrual cycle. Uter-
ine contractility during the early follicular phase (menses,
antegrade: fundus-to-cervix) increases progressively to a
maximum activity at midcycle (retrograde: cervix-to-fun-
dus), and declines gradually throughout the luteal phase
(quiescence) (4, 25–27). Dyskinetic alterations in this
process may be responsible for infertility, especially with
endometriosis (28, 29). The uterine contraction amplitude
is three times higher in women with endometriosis than in
women without endometriosis (30). The finding that en-
dometriosis is intimately associated with dyskinetic alter-
study, which shows that the PR in women with endome-
triosis who had the piroxicam treatment increased about
twice as much as in control women. We hypothesize that
this increased PR may be a result of the normalization of
uterine contractility by piroxicam treatment.
However, our present study did not show the significant
improvement of PR by piroxicam treatment in the patient
group with an unexplained infertility factor. One explanation
of this unexpected finding is an unknown factor of unex-
plained infertility may surpass the calming effect of piroxi-
cam on the uterine contractility. Therefore, further study to
seek the effect of NSAIDs on the uterine contractility and PR
is necessary. Also, in the present study, the beneficial effect
of piroxicam was not expressed in older women, notably
patients more than 40 years. This result implies that the
calming effect of piroxicam does not seem to overcome the
age-related fertility declines.
In conclusion, this study is the first to investigate the
possible consequence of piroxicam to improve the preg-
nancy outcome of IVF–ET, and shows that the treatment
with piroxicam increases the implantation rate and PR after
IVF–ET in both fresh and frozen–thawed cycles. These
results suggest that administration of piroxicam just before
ET is very effective in the priming of the uterus to be suitable
for embryo implantation. However, our study did not eval-
uate whether piroxicam calms the uterus by reducing uterine
contractions or if it increases uterine blood flow. Further
study is needed to elucidate the mechanism of the action of
piroxicam.
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Vol. 82, No. 4, October 2004