Role of acupuncture in the treatment of female infertility
Raymond Chang, M.D.[a,b] Pak H. Chung, M.D.[b] and Zev
Rosenwaks, M.D.[c]
The Institute of East-West Medicine and the Center for
Reproductive Medicine and Infertility, Weill Medical College
of Cornell University, New York, New York
Received June 24, 2002; revised and accepted July 19, 2002.
Reprint requests: Pak H. Chung, M.D., The Center for Reproductive
Medicine and Infertility, Weill Medical College of Cornell
University, 505 East 70 Street, New York, New York 10021
(FAX: 212-746-8208; E-mail: pakchu@med.cornell.edu).
[a]The Institute of East-West Medicine. [b]The Department
of Internal Medicine, Weill Medical College of Cornell Unversity.
[c]The Center for Reproductive Medicine and Infertility.
0015-0282/02/$22.00
PII S0015-0282(02)04348-0
Objective: To review existing scientific rationale
and clinical data in the utilization of acupuncture in the
treatment of female infertility.
Design: A MEDLINE computer search was performed
to identify relevant articles.
Result(s): Although the understanding of acupuncture
is based on ancient medical theory, studies have suggested
that certain effects of acupuncture are mediated through
endogenous opioid peptides in the central nervous system,
particularly ß-endorphin. Because these neuropeptides
influence gonadotropin secretion through their action on
GnRH, it is logical to hypothesize that acupuncture may
impact on the menstrual cycle through these neuropeptides.
Although studies of adequate design, sample size, and appropriate
control on the use of acupuncture on ovulation induction
are lacking, there is only one prospective randomized controlled
study examining the efficacy of acupuncture in patients
undergoing IVF. Besides its central effect, the sympathoinhibitory
effects of acupuncture may impact on uterine blood flow.
Conclusion(s): Although the definitive role of acupuncture
in the treatment of female infertility is yet to be established,
its potential impact centrally on the hypothalamic-pituitary-ovarian
axis and peripherally on the uterus needs to be systemically
examined. Prospective randomized controlled studies are
needed to evaluate the efficacy of acupuncture in the female
fertility treatment. (Fertil Steril® 2002;78:1149-53.
©2002 by American Society for Reproductive Medicine.
Key Words: Acupuncture, female infertility, in vitro
fertilization
Acupuncture as a therapeutic intervention has been extensively
studied and is increasingly practiced in the United States.
A recent survey of acupuncture released by an NIH Consensus
Development panel (1) indicated that although there are
inherent problems of design, sample size, and appropriate
controls in the acupuncture literature, promising data exist
for the use of acupuncture in treating nausea and vomiting
(2), postoperative pain (3-5), addiction (6-9), and general
pain syndromes (10-12). As a medical technique, acupuncture
has also been reported as an adjunct in the treatment of
various gynecologic problems (13-15).
Although conventional treatment options for female infertility
have been well established, there have been few systematic
reviews of complementary or alternative approaches to the
treatment of infertility. In light of an increasing trend
in the use of complementary and alternative medicine (16)
and common inquiry and utilization of such approaches by
patients suffering from infertility, we intend to review
the existing scientific rationale and clinical data based
on which acupuncture may exert an influence on the outcome
of female fertility.
In examining the potential usefulness of acupuncture in
enhancing female fertility, it is appropriate first to give
some theoretical background for acupuncture. Although the
theory of acupuncture stems from underlying traditional
Chinese medicine premises that would define etiologies for
infertility in terms of energy disturbance of imbalances,
or organ deficiencies and excesses, we intend to review
the existing literature by examining modern medical aspects
of the central and peripheral modes of action of acupuncture
as they impact on the hypothalamic-pituitary-ovarian axis
and the pelvic organs, respectively. Moreover, the effect
of acupuncture on anxiety and stress and ensuing potential
indirect effects on female fertility will also be discussed.
Background
Acupuncture is the manipulation of thin metallic needles
inserted into anatomically defined locations on the body
to affect bodily function. The US Food and Drug Administration
has recently removed acupuncture needles from the category
of experimental medical devices and now regulates them just
like it does other devices, such as surgical scalpels and
hypodermic needles, under good manufacturing practices and
single-use standard of sterility (1).
The general theory of acupuncture is based on the premise
that there are patterns of energy flow (Qi) through the
body, which are essential for health. Disruption of this
flow is believed to be responsible for disease. Acupuncture
can correct imbalances of flow at identifiable points close
to the skin.
According to the proposed international acupuncture nomenclature
by The World Health Organization in 1991 (17), the meridian
system consists of 20 meridians interconnecting about 400
acupoints. These acupoints correspond to specific areas
on the surface of the body, which demonstrate higher electrical
conductance because of the presence of higher density of
gap junctions along cell borders. They act as converging
points (or sinks) for electromagnetic fields. A higher metabolic
rate, temperature, and calcium ion concentration, are also
observed at these points. In principle, positive (anode)
pulse stimulation of a point inhibits the organ function,
whereas negative (cathode) pulse stimulation enhances that
function (18). This forms the basis of electroacupuncture,
which applies small electrical needles inserted in specific
acupoints.
Effects of acupuncture on the hypothalamic-pituitary-ovarian
axis and menstrual cycle
Although traditional Chinese medicine understanding of
acupuncture is based on ancient medical theory, a modern
and scientific neuroendocrine perspective has begun to evolve
in the past two decades. Mayer et al. (19) first reported
that acupuncture analgesia was induced through endorphin
production and antagonized by the narcotic antagonist naloxone.
Other studies similarly suggested that certain effects of
acupuncture are mediated through the nervous system, within
which ß-endorphin and other neuropeptides have been
implicated (20-22).
Acupuncture was shown by Petti et al. (20) to cause a significant
increase in ß-endorphin levels during treatment, which
lasted for up to 24 hours. ß-endorphin is derived
from its precursor protein pro-opiomelanocortin, which is
present in abundant amounts in neuronal cells of the arcuate
nucleus of the hypothalamus, pituitary, medulla, and in
peripheral tissues including intestines and ovaries (23-25).
Pro-opiomelanocortin cleaves to form adrenocorticotropic
hormone and ß-lipoprotein. Further cleavage of ß-lipoprotein
yields neuropeptides including ß-endorphin. Aleem
et al. (26, 27) demonstrated the presence of immunoreactive
ß-endorphin in follicular fluids of both normal and
polycystic ovaries.
The influence on gonadotropin secretion and the menstrual
cycle by endogenous opioid peptides is believed to be mediated
by their action on GnRH secretion (28). The hypothalamic
ß-endorphin center and the GnRH pulse generator, in
fact, are both situated within the arcuate nucleus. Quigley
et al. (29) first reported an increased opioid inhibition
of LH secretion in hyperprolactinemic patients with pituitary
microadenomas. Ching (30) and Orstead and Spics (31), respectively,
showed that opioid peptides suppress GnRH release in rats
and rabbits.
The role of these neuropeptides, including ß-endorphin,
in the regulation of GnRH secretion in humans has recently
been reviewed by Kalra et al. (32) and Pau and Spies (33).
Rossmanith et al. (34) demonstrated the role of opioid peptides
in the initiation of the mid-cycle LH surge in normal cycling
women. Meanwhile, measurement of ß-endorphin in ovarian
follicular fluid of healthy ovulatory women revealed much
higher levels than that in circulating plasma (35). The
highest level of ß-endorphin was noted to be in the
preovulatory follicle.
Because acupuncture treatment impacts on ß-endorphin
levels, which in turn affect GnRH secretion and the menstrual
cycle, it is logical to hypothesize that acupuncture may
influence ovulation and fertility. Animal studies have revealed
that acupuncture treatment normalized GnRH secretion and
affected peripheral gonadotropin levels (36, 37). Various
investigators have shown that in normally ovulatory or anovulatory
women, acupuncture also influenced plasma levels of FSH,
LH, E2, and P (38-40). Acupuncture as a surrogate for hCG
in ovulation induction was successfully used by Cai (41).
Chen and Yu (42) showed that electroacupuncture normalized
they hypothalamic-pituitary-ovarian axis, and in another
study Chen (43) reported that 6 of 13 anovulatory cycles
responded to acupuncture treatment.
A series published from the University of Heidelberg in
Germany (44) used auricular acupuncture on 45 infertile
women suffering from ovulatory dysfunction such as oligomenorrhea
and luteal phase defect. The control group received medical
treatment including bromocriptine, dexamethasone, levothyroxine,
clomiphene citrate (CC), and gonadotropin. Although the
investigators concluded that resumption of ovulatory cycles
occurred significantly more often in the acupuncture group
compared to the control group, pregnancy rates were not
different between the two groups. However, interpretation
of study data was very difficult due to the heterogeneity
of the patient population and treatment modalities. Moreover,
seven pregnancies in the acupuncture group were actually
achieved with hormone treatment 6 months after acupuncture
was stopped.
Another study by Stenver-Victorin et al. (45) evaluated
the use of electroacupuncture for ovulation induction on
24 oligo/amenorrheic women with polycycstic ovarian syndrome
(PCOS). The percentage of ovulatory cycles in all subjects
was shown to improve from 15% (in a total of 3 months before
treatment) to 66% up to 3 months after treatment. Responsive
patients were noted to have significantly lower body mass
index (BMI), waist-to-hip circumference ratio, serum T concentration,
serum T/sex hormone-binding globulin ratio, and serum basal
insulin level. They suggested that, in these selected patients
with PCOS, acupuncture could be considered as an alternative
or adjunct to pharmacological ovulation induction.
A recent prospective randomized controlled study by Paulus
et al. (46) compared pregnancy rates in a total of 160 patients
undergoing IVG. Acupuncture was performed in 80 patients
25 minutes before and after ET. After controlling confounding
variables, clinical pregnancy rate for the acupuncture group
(42.5%) was significantly higher than the control group
(26.3%).
Peripheral effects of acupuncture
In addition to the central modulation of the hypothalamic-pituitary-ovarian
axis, the effects of acupuncture on the autonomic nervous
system have been well documented (47). In the early 1980s,
Yao et al. (48) reported long-lasting cardiovascular depression
induced by acupuncture stimulation of the sciatic nerve
in unanesthetized hypertensive rats. In the human, acupuncture
was also shown to be sympathoinhibitory. After acupuncture,
sympathetic nerve activity as measured by norepinephrine
level, skin temperature, blood pressure, and pain tolerance
threshold was shown to be decreased (49).
Endometrial thickness, morphology, and uterine artery blood
flow have been implicated as important parameters for success
of implantation of human embryos (50-57). Despite conflicting
results in the utilization of these parameters during various
stages of treatment to predict outcome in IVF, it is generally
believed that adequate endometrial thickness is required
to optimize pregnancy rate. Because endometrial thickness
is a function of uterine artery blood flow, Sher and Fisch
(58) reported a novel method of using vaginal sildenafil
in an attempt to improve uterine artery blood flow and endometrial
development in patients undergoing IVF.
With its central sympathoinhibitory effect, acupuncture
may contribute to reduce uterine artery impedance and therefore,
increase blood flow to the uterus. In fact, Sterner-Victorin
et al. (59) demonstrated this when they performed acupuncture
in 10 infertile women who were down-regulated by GnRH analog
to avoid the effect of endogenous hormone on the uterine
artery blood flow.
Pulsatility index in the uterine artery and skin temperature
(on the forehead and lumbosacral area) were evaluated in
three time periods-before, right after, and 2 weeks after
acupuncture treatment (twice a week for 4 weeks). Pulsatility
index and skin temperatures were found to be significantly
decreased and increased, respectively, both right after
and 14 days after acupuncture treatment. This effect was
hypothesized to be caused by central inhibition of sympathetic
activity.
Acupuncture and stress reduction
It has been well documented that infertility causes stress
(60-65), and stress reduction may, in turn, improve fertility
(66). However, the relationship between stress and infertility
is that of a vicious cycle. Social stigmatization, decreased
self-esteem, unmet reproductive potential of sexual relationship,
physical and mental burden of treatment, and the lack of
control on treatment outcome are just some of the factors
that can lead to psychological stress in any couple pursuing
infertility treatment. In turn, stress may lead to the release
of stress hormones and influence mechanisms responsible
for a normal ovulatory menstrual cycle through its impact
on the hypothalamic-pituitary-ovarian axis.
The use of acupuncture for reducing anxiety and stress
possibly through its sympathoinhibitory property and impact
on ß-endorphin levels has been reviewed (67, 68),
and the efficacy of acupuncture in depression has also been
studied (69). Because the pharmacological side effects of
anxiolytic and antidepressant drugs on infertility treatment
outcome are largely unknown, acupuncture may provide an
excellent alternative for stress reduction in women undergoing
infertility treatment.
Discussion
The practice of acupuncture to treat identifiable patho-physiological
conditions has been a subject of intense research. The underlying
physiologic mechanisms of acupuncture such as the release
of opioids and other peptides in the central peripheral
nervous system, and its inhibition of the sympathetic nervous
system have been increasingly established. Promising results
from credible trials have emerged for the use of acupuncture
in treating various pain syndromes, substance abuse, and
chemotherapy-induced nausea and vomiting.
Although the definitive role of acupuncture in the treatment
of female infertility is yet to be established, its neuroendocrine
effect on the hypothalamic-pituitary-ovarian axis and the
preliminary clinical data reviewed here justifies further
clinical trials to systematically examine the efficacy of
acupuncture in treating various conditions related to female
infertility such as ovulatory dysfunction associated with
PCOS. The peripheral impact of acupuncture in improving
uterine artery blood flow and hence endometrial thickness
also provides encouraging data regarding its potential positive
effect on implantation.
Whether these potential beneficial effects of acupuncture
on the reproductive system can be translated into improving
infertility treatment outcomes will eventually mandate randomized
controlled studies of adequate design. Because acupuncture
is nontoxic and relatively affordable, its indications as
an adjunct in assisted reproduction or as an alternative
for women who are intolerant, ineligible, or contraindicated
for conventional hormone induction of ovulation deserves
serious research and exploration.
Appropriate training, credentialing, and certification
of acupuncture practitioners by state agencies can facilitate
the integration of acupuncture into the treatment of female
infertility, and healthcare in general. The NIH Consensus
Conference (1) agreed that this is necessary to allow the
public and other health practitioners to identify qualified
acupuncture practitioners. With the help of the US Department
of Education, issues of training and licensure of non-physician
and physician practitioners have been addressed. There is
sufficient evidence to acupuncture's value to expand its
use into conventional medicine and treatment of female infertility,
and to encourage further studies of its underlying mechanisms
as well as to establish its clinical value.
References
1. NIH Consensus Development Panel of Acupuncture. Acupuncture.
JAMA 1998;280:1518-24.
2. Dundee JW, Ghaly RG, Lynch GA, Fitzpatrick KT, Abram
WP. Acupuncture prophylaxis of cancer chemotherapy-induced
sickness. J R Soc Med 1989;82:268-71.
3. Christiansen PA, Noreng M, Andersen PE, Nielsen JW. Electroacupuncture
and postoperative pain. Br J Anaesth 1989;62:258-62.
4. Martelete M, Fiori AMC. Comparative study of analgesic
effect of transcutaneous nerve stimulation (TNS), electroacupuncture
(EA), and meperidine in the treatment of postoperative pain.
Acupunct Electrother Res 1985;10:183-93.
5. Lao L, Bergman S, Langenberg P, Wong RH, Berman B. Efficacy
of Chinese acupuncture on postoperative oral surgery pain.
Oral Surg Med Oral Path Oral Radiol Endod 1995;79:423-8.
6. Bullock ML, Culliton PD, Olander RT. Controlled trial
of acupuncture for severe recidivist alcoholism. Lancet
1989;1:1435-39.
7. Clavel-Chapelon F, Paoletti C, Banhamou S. Smoking cessation
rates 4 years after treatment by nicotine gum and acupuncture.
Prev Med 1997;26:25-8.
8. He D, Berg JE, Hostmark AT. Effects of acupuncture on
smoking cessation or reduction for motivated smokers. Pev
Med 1997;26:208-14.
9. Margolin A, Avants SK, Chang P, Kosten TR. Acupuncture
for the treatment of cocaine dependence in methadone-maintained
patients, Am J Addict 1993;2:194-201.
10. Patel M, Gutzwiller F, Paccaud F, Marazzi A. A meta-analysis
of acupuncture for chronic pain. Int J Epidemiol 1989;18:900-6.
11. Shlay JC, Chaloner K, Max MB, Flaws B, Reichelderfer
P, Wentworth D, et al. Acupuncture and amitriptyline for
pain due to HIV-related peripheral neuropathy: a randomized
control trial. JAMA 1998;280:1590-5.
12. Tier Riet G, Kleijnen J, Knipschild P. Acupuncture and
chronic pain: a criteria based meta-analysis. J Clin Epidemiol
1990;43:1191-9.
13. Chez RA, Jonas WB. Complementary and alternative medicine.
Part II: Clinical studies in gynecology. Obstet Gynecol
Surv 1997;52:709-16.
14. Wu XJ, Cui YL, Yang BY, Zhou QM, Observations on the
effect of He-Ne laser acupoint radiation in chronic pelvic
inflammation. J Tradit Chin Med 1987;7:263-5.
15. Beal MW. Acupuncture and acupressure. Applications to
women's reproductive health care. J Nurse Midwifery 1999;44:217-30.
16. Eisenberg DM, Davis RB, Ettner SL, Appel S, Wilkey S,
Van Rompay M, et al. Trends in alternative medicine use
in the United States, 1990-1997: results of a follow-up
national survey. JAMA 1998;280:1569-75.
17. World Health Organization. A proposed standard international
acupuncture nomenclature: report of a WHO scientific group.
Geneva, Switzerland: World Health Organization, 1991.
18. McCaig CD. Sinal neurite reabsorption and regrowth in
vitro depend on the polarity of an applied electric field.
Development 1987;100:31-41.
19. Mayer DJ, Price DD, Rafil A. Antagonism of acupuncture
analgesia in man by the narcotic antagonist naloxone. Brain
Res 1977;121:368-72.
20. Petti F, Bangrazi A, Liguori A, Reale G, Ippoliti F.
Effects of acupuncture on immune response related to opioids-like
peptides. J Tradit Chin Med 1998;18:55-63.
21. Ulett GA, Han S, Han JS. Electroacupuncture: mechanisms
and clinical application, Biol Psychiatry 1998;44:129-38.
22. Ku Y, Chang Y. Beta-endorphin and GABA-mediated depressor
effect of specific electroacupuncture surpasses pressor
response of emotional circuit. Peptides 2001;22:1465-70.
23. Facchinetti F, Storchi AR, Petraglia F, Volpe A, Genazzani
AR. Expression of proopiomelanocortin-related eptides in
human follicular fluid. Peptides 1988;9:1089-92.
24. Gallinelli A, Garuti G, Matteo ML, Genazzani AR, Facchinetti
F. Expression of proopiomelanocortin gene in human ovarian
tissue. Hum Reprod 1995;10:1085-9.
25. DeBold CD, Menefee JK, Nicholson WE, Orth DN. Proopiomelanocortin
gene is expressed in many normal human tissues and intumors
not associated with ectopic adrenocorticotropin syndrome.
Mol Endocrinol 1988;2:862-70.
26. Aleem FA, Eltabbakh GH, Omar RA, Couthren AL. Ovarian
follicular fluid beta-endorphin levels in normal and polycystic
ovaries. Am J Obstet Gynecol 1987;156:1197-200.
27. Aleem FA, Omar RA, Eltabbakh GH. Immunoreative beta-endorphin
in human ovaries. Fertial Steril 1986;45:507-11.
28. Ferin M, Van de Wiele RL. Endogenous opioid peptides
and the control of the menstrual cycle. Eur J Obstet Gynecol
Repro Biol 1984;10:365-73.
29. Quigley ME, Sheeham KL, Casper RF, Yen SSC. Evidence
for an increased opioid inhibition of luteinizing hormone
secretion in hyperprolactinemic patients with pituitary
microadenoma. J Clin Endocrinol Metabol 1980;50:427-46.
30. Ching M. Morphine suppresses the proestrous surge of
GnRH in pituitary portal plasma of rats. Endocrinology 1983;112:2209-11.
31. Orstead KM, Spics HG. Inhibition of hypothalamic gonadotropin
releasing hormone release by endogenous opioid peptides
in the female rabbit. Neuroendocrinology 1987;46:14-23.
32. Kalra SP, Horvath T, Naftolin F, Xu B, Pu S, Kalra PS.
The interactive language of the hypothalamus for the gonadotropin
releasing hormone (GNRH) system. J Neuroendocrinol 1997;9:569-76.
33. Pau KY, Spies HG. Neuroendocrine signals in the regulation
of gonadotropin-releasing hormone secretion. Chin J Physiol
1997;40:181-96.
34. Rossmanith WG, Mortola JF, Yen SSC. Role of endogenous
opioid peptides in the initiation of the mid-cycle luteinizing
hormone surge in normal cycling women. J Clin Endocrinol
Metab 1988;67:695-700.
35. Petraglia F, DiMeo G, Storchi R, Segre A, Facchinette
F, Szalay S, et al. Proopiomelanocortin-related peptides
and methionine enkephalin in human follicular fluid: changes
during the menstrual cycle. Am J Obstet Gynecol 1987;157:142-6.
36. Lin JH, Liu SH, Chan WW, Wu LS, Pi WP. Effects of electroacupuncture
and gonadotropin-releasing hormone treatments on hormone
changes in anoestrous sows. Am J Chin Med 1988;16:117-26.
37. Yang SP, Yu J, He L. Release of gonadotropin-releasing
hormone (GnRH) from the medio-basal hypothalamus induced
by electroacupuncture in conscious female rabbits. Acupunct
Electrother Res 1994;19:19-27.
38. Aso T, Motohashi T, Murata M, Nishimura T, Kakizaki
K. The influence of acupuncture stimulation on plasma levels
of LH, FSH, progesterone and estradiol in normally ovulating
women. Am J Chin Med 1976;4:391-401.
39. Yu J, Zheng HM, Ping SM. Changes in serum FSH, LH and
ovarian follicular growth during electroacupuncture for
induction of ovulation [Chinese]. Chung His I Chieh Ho Tsa
Chih 1989;9:199-202.
40. Mo X, Li D, Pu Y, Xi G, Le X, Fu Z. Clinical studies
on the mechanism of acupuncture stimulation of ovulation.
J Trad Chin Med 1993;13:115-9.
41. Cai X. Substitution of acupuncture for human chorionic
gonadortropin in ovulation induction. J Tradit Chin Med
1997;17:119-21.
42. Chen BY, Yu J. Relationship between blood radioimmunoreactive
beta-endorphin and hand skin temperature during the electro-acupuncture
induction of ovulation. Acupunct Electrother Res 1991;16:1-5.
43. Chen BY. Acupuncture normalizes dysfunction of hypothalamic-pituitary-ovarian
axis. Acupunct Electrother Res 1997;22:97-108.
44. Gerhard I, Postneek F. Auricular acupuncture in the
treatment of female infertility. Gynecol Endocrinol 1992;6:171-81.
45. Stener-Victorin E. Waldenstrom U, Tagnfors U, Lundeberg
T, Lundstedt G, Janson PO. Effects of electro-acupuncture
on anovulation in women with polycycstic ovary syndrome.
Acta Obstet Gynecol Scand 2000;79:180-8.
46. Paulus WE, Zhang M, Strehler E, El-Danasouri I, Sterzik
K. Influence of acupuncture on the pregnancy rate inn patients
who undergo assisted reproduction therapy. Fert Steril 2002;77:721-4.
47. Haker E, Egekvist H, Bjerring P. Effect of sensory stimulation
(acupuncture) on sympathetic and parasympathetic activities
in healthy subjects. J Automomic Nerv Sys 2000;79:52-9.
48. Yao T, Andersson S, Thoren P. Long-lasting cardiovascular
depression induced by acupuncture-like stimulation of the
sciatic nerve in unanaesthetized spontaneously hypertensive
rats. Brain Res 1982;240:77-85.
49. Knardahl S, Elam M, Olausson B, Wallin BG. Sympathetic
nerve activity after acupuncture in humans. Pain 1998;75:19-25.
50. Noyes N, Liu HC, Sultan K, Schattman G, Rosenwaks Z.
Endometrial thickness appears to be a significant factor
in embryo implantation in thickness appears to be a significant
factor in embryo implantation in-vitro fertilization. Hum
Reprod 1995;10:919-22.
51. Schild RL, Knoblock C, Dorn C, Fimmers R, van der Ven
H, Hansmann M. Endometrial receptivity in an in vitro fertilization
program as assessed by spiral artery blood flow, endometrial
thickness, endometrial volume, and uterine artery blood
flow. Fertil Steril 2001;75:361-6.
52. Chiang CH, Hsieh TT, Chang MY, Shiau CS, Hou HC, Hsu
JJ, et al. Prediction of pregnancy rate of in vitro fertilization
an embryo transfer in women aged 40 and over with basal
uterine artery pulsatility index. J Assist Reprod Genet
2000;17:409-14.
53. Engmann L. Sladkevicius P, Agrawal R, Bekir J, Campbell
S, Tan SL. The pattern of changes in ovarian stromal and
uterine artery blood flow velocities during in vitro fertilization
treatment and its relationship with outcome of the cycle.
Ultrasound Obstet Gynecol 1999;13:26-33.
54. Salle B, Bied-Damon V, Benchaib M, Desperes S, Gaucherand
P, Rudigoz RC. Preliminary report of an ultrasonography
and colour Doppler uterine score to predict uterine receptivity
in an in-vitro fertilization programme. Hum Reprod 1998;13:1669-73.
55. Aytoz A, Ubaldi F, Tournaye H, Nagy ZP, Van Steirteghem
A, Devroey P. The predictive value of uterine artery blood
flow measurements for uterine receptivity in an intracytoplasmic
sperm injection program. Fertil Steril 1997;68:935-7.
56. Friedler S, Schenker JG, Herman A, Lewin A. The role
of ultrasonography in the evaluation of endometrial receptivity
following assisted reproductive treatments: a critical review.
Hum Reprod Update 1996; 2:323-35.
57. Zaidi J, Pittrof R, Shaker A, Kyei-Mensah A, Campbell
S, Tan SL. Assessment of uterine artery blood flow on the
day of human chorionic gonadotropin administration by transvaginal
color Doppler ultrasound in an in vitro fertilization program.
Fertil Steril 1996;65:377-81.
58. Sher G, Fisch JD. Vaginal sildenifil (Viagra): a preliminary
report of a novel method to improve uterine artery blood
flow and endometrial development in patients undergoing
IVF. Hum Reprod 2000;15:806-9.
59. Stener-Victorin E, Waldenstrom U, Andersson SA, Wikland
M. Reduction of blood flow impedance in the uterine arteries
of infertile women with electro-acupuncture. Hum Reprod
Biol 1996;11:1314-7.
60. Schenker JG, Meirow D, Schenker E. Stress and human
reproduction. Eur J Obstet Gynecol Reprod Biol 1992;45:1-8.
61. Eugster A, Vingerhoets AJ. Psychological aspects of
in vitro fertilization: a review. Soc Sci Med 1999;48:575-89.
62. Domar AD, Broome A, Zuttermeister PC, Seibel M. Friedman
R. The prevalence and predictability of depression in infertile
women. Fertil Steril 1992;58:1158-63.
63. Domar AD, Zuttermeister PC, Friedman R. The psychological
impact of infertility: a comparison with patients with other
medical conditions. J Psychosom Obstet Gynaecol 1993;14:45-52.
64. Mahlstedt PP, Macduff S, Bernstein J. Emotional factors
in in vitro fertilization and embryo transfer process. J
In Vitro fert Embryo Transf 1987;4:232-5.
65. Seibel MM, Taymore ML. Emotional aspects of infertility.
Fertil Steril 1982;37:137-45.
66. Domar AS, Seibel MM, Benson H. The mind/body program
for infertility: a new behavioral treatment approach for
women with infertility. Fertil Steril 1990;53:246-9.
67. Chen A. An introduction to sequential electric acupuncture
(SEA) in the treatment of stress related physical and mental
disorders. Acupunct Electrother Res 1992;17:273-83.
68. Dong JT. Research on the reduction of anxiety and depression
with acupuncture. Am J Acupunct 1993;21:327-30.
69. Luo H, Meng F, Jia Y, Zhao X. Clinical research on the
therapeutic effect of the electroacupuncture treatment in
patients with depression. Psychiatry Clin Neurosci 1998;52:S338-40.
FERTILITY AND STERILITY® VOL. 78, NO. 6,
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