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Endometriosis and infertility
The Practice Committee of the American Society for Reproductive Medicine Women with endometriosis typically present with pelvic pain, infertility or an adnexal mass. Surgery forpersistent adnexal masses may be indicated to remove an endometrioma or other pelvic pathology. Surgical ormedical therapy is efficacious for pelvic pain due to endometriosis, but treatment of endometriosis in the femalepartner of an infertile couple raises a number of complex clinical questions that do not have simple answers.
(Fertil Steril௡ 2006;86(Suppl 4):S156 – 60. 2006 by American Society for Reproductive Medicine.) Women with endometriosis typically present with pelvic the 1980s in which fecundity of women with minimal endo- pain, infertility or an adnexal mass. Surgery for persistent metriosis was similar to that of other women undergoing adnexal masses may be indicated to remove an endometri- donor insemination On the premise that endometriosis oma or other pelvic pathology. Surgical or medical therapy is does cause infertility, then eradication of the disease should efficacious for pelvic pain due to endometriosis, but treat- improve fecundity. Two randomized controlled trials (RCTs) ment of endometriosis in the female partner of an infertile have compared outcomes following laparoscopic ablation or couple raises a number of complex clinical questions that do expectant management of endometriosis. In the Canadian not have simple answers. There are few infertility problems Collaborative Group on Endometriosis RCT involving 341 requiring greater clinical acumen than those needed to plan women with stage I/II disease followed for 36 weeks after therapy for an infertile woman with endometriosis.
laparoscopy, monthly fecundity was 0.047 and 0.024 in theablated and untreated groups, respectively In theGruppo Italiano per lo Studio dell’ Endometriosi RCT in- FECUNDITY IN WOMEN WITH ENDOMETRIOSIS
volving 101 women with stage I/II disease followed for 52 Fecundity is defined as the probability of a woman achieving weeks after laparoscopy, fecundity was 0.016 and 0.019 in a live birth for any given month In normal couples, the ablated and untreated groups, respectively Although fecundity is in the range of 0.15 to 0.20 per month and fecundity was significantly improved only in the Canadian decreases with age In untreated women with endome- surgical trial, fecundity remained significantly lower than that triosis and infertility, monthly fecundity is 0.02 to 0.10 observed in normal fertile women. Thus the visible lesions of Early studies suggested that 25% to 50% of infertile women endometriosis contribute only a small fraction of the reduced have endometriosis and that 30% to 50% of women with fecundity seen in women with endometriosis.
endometriosis are infertile There is a higher prevalenceof endometriosis in infertile women (48%) compared withfertile women undergoing tubal sterilization (5%) Other BIOLOGIC MECHANISMS THAT MAY LINK
reports have confirmed that infertile women are 6 to 8 times ENDOMETRIOSIS AND INFERTILITY
more likely to have endometriosis than fertile women Several mechanisms have been proposed to clarify the asso-ciation between endometriosis and infertility It shouldbe emphasized that none of these mechanisms has been ENDOMETRIOSIS AND INFERTILITY: CAUSE AND EFFECT
proven to decrease fecundity in women. These mechanisms The hypothesis that endometriosis causes infertility or a decrease in fecundity remains controversial. Whereas thereis a reasonable body of evidence to demonstrate an associ-ation between endometriosis and infertility, a cause and Distorted Pelvic Anatomy
effect relationship has not been established. In a prospective Major pelvic adhesions, including those that result from study of women undergoing therapeutic donor insemination, endometriosis, can impair oocyte release from the ovary or fecundity was 0.12 in women without endometriosis and 0.036 in those with minimal endometriosis The results ofthis study were at odds with two retrospective studies from Altered Peritoneal Function
Many studies demonstrate that women with endometriosis Education Bulletin
have an increased volume of peritoneal fluid, increased con- Reviewed June 2006.
centration of activated macrophages and increased peritoneal Received January 12, 2004; revised and accepted January 12, 2004.
fluid concentrations of prostaglandins, interleukin-1, tumor necrosis factor and proteases. Peritoneal fluid from women Correspondence to: Practice Committee, American Society for Reproduc- tive Medicine, 1209 Montgomery Highway, Birmingham, Alabama 35216.
with endometriosis reportedly contains an ovum capture S156 Fertility and Sterilityா Vol. 86, Suppl 4, November 2006
Copyright 2006 American Society for Reproductive Medicine, Published by Elsevier Inc.
inhibitor that prevents normal cumulus-fimbria interaction endometriosis (ASRM 1996) is the most widely accepted These alterations may have adverse effects on the oocyte, staging system Unfortunately, the staging system does sperm, embryo or fallopian tube function not correlate well with a woman’s chance of conceptionfollowing therapy. This poor predictive ability is related tothe arbitrary assignment of a point score for the observed Altered Hormonal and Cell-Mediated Function
pathology and the arbitrary cut-off points chosen to establish IgG and IgA antibodies and lymphocytes may be increased the stage of disease. The ASRM 1996 classification system in the endometrium of women with endometriosis. These might be enhanced by including a description of the mor- abnormalities may alter endometrial receptivity and embryo phologic subtype of disease or other biological markers implantation. Autoantibodies to endometrial antigens are re- It is unlikely that any accurate staging system will be intro- ported to be increased in some women with endometriosis duced until we have a better understanding of the pathophys-iology of endometriosis-associated infertility.
Endocrine and Ovulatory Abnormalities
It has been proposed that women with endometriosis may MEDICAL THERAPY FOR ENDOMETRIOSIS
have endocrine and ovulatory disorders, including the lutein- Whereas medical therapy is effective for relieving pain associ- ized unruptured follicle syndrome, luteal phase dysfunction, ated with endometriosis, there is no evidence that medical abnormal follicular growth and premature as well as multiple treatment of endometriosis improves fecundity. Several options luteinizing hormone (LH) surges Whereas these hypoth- have been suggested for treatment: danazol, gonadotropin- eses have been proposed, there is no evidence to validate them.
releasing hormone agonists (GnRH-a) and antagonists, pro-gestins and combined estrogen-progestin therapy. Several Impaired Implantation
RCTs demonstrate that danazol, other progestins or GnRH-a Mounting evidence suggests that disorders of endometrial are not effective treatments for infertility associated with function may contribute to the deceased fecundity observed minimal to mild endometriosis In two RCTs in- in women with endometriosis. Reduced endometrial expres- volving 105 infertile women with minimal to mild endome- sion of the ␣v␤ integrin (a cell adhesion molecule) during triosis, pregnancy rates were no better with danazol than the time of implantation has been described in some women expectant management In an RCT involving 71 with endometriosis More recently, very low levels of an infertile women with minimal to mild endometriosis, the one enzyme involved in the synthesis of the endometrial ligand for and two-year cumulative pregnancy rates were similar in the L-section (a protein that coats the trophoblast on the surface of groups receiving GnRH-a treatment (6 months) or expectant the blastocyst) have been observed in infertile women with management In a small RCT involving 37 infertile endometriosis These data lend credence to the hypothesis women with minimal to mild endometriosis treated with that functional disorders of the endometrium may both predis- progestins or expectant management, pregnancy rates were pose to the development of endometriosis and impair implan- similar at one year in both groups Also, in a small RCT tation mechanisms in affected women.
involving 31 women, pregnancy rates with progestins andexpectant management were 41% and 43%, respectivelyIn a meta-analysis that included seven studies compar- DIAGNOSIS AND STAGING
ing medical treatment to no treatment or placebo, the com- The current clinical opinion is that a surgical procedure such mon odds ratio for pregnancy was 0.85 (95% CI 0.95, 1.22) as laparoscopy is required for definitive diagnosis of endo- Thus hormonal treatment does not improve the fecundity metriosis. Given this state of clinical practice, an important of infertile women with Stage I/II endometriosis.
question is when to perform laparoscopy to determine ifendometriosis is present. A history and physical examinationcan yield a number of significant findings, including affected SURGERY FOR ENDOMETRIOSIS
first degree relatives, chronic pelvic pain and dysmenorrhea, In stage I/II endometriosis, laparoscopic ablation of endometrial retroverted uterus, adnexal masses, cul de sac nodularity and implants has been associated with a small but significant im- uterosacral ligament thickening and tenderness, but none is provement in live birth rates. Two RCTs have reported on the diagnostic. Ultrasound can help the clinician establish a effectiveness of laparoscopic surgery for Stage I or II endome- presumptive diagnosis of ovarian involvement with endome- triosis associated with infertility Both studies permit- triosis, but laparoscopy is necessary to confirm the diagnosis.
ted surgical discretion in the intervention regarding excision Endometriosis is a heterogeneous disease with typical and or ablation. The primary outcomes were slightly different: atypical morphology and spanning a spectrum from a single the Italian study analyzed pregnancies which occurred 1-mm peritoneal implant to 10-cm endometriomas with cul- within one year after laparoscopy and proceeded to live de-sac obliteration Consequently, a clinical staging system births; the Canadian study analyzed pregnancies which oc- is necessary to allow clinicians to communicate effectively curred within 36 weeks after laparoscopy and proceeded to regarding prognosis and treatment. The American Society 20 weeks gestation, an end- point which is nearly identical to for Reproductive Medicine revised classification system for the live birth rate. In the Italian study, 10/51 (20%) and 10/45 FERTILITY & STERILITY
(22%) of the ablation/ resection and no treatment patients, monthly fecundity in the gonadotropin/IUI group (0.09) respectively, were successful. In the Canadian study, 50/172 was significantly higher than the monthly fecundity in the (29%) and 29/169 (17%) of the ablation/resection and no IUI group (0.05), the gonadotropin/IC group (0.04) and treatment patients, respectively, were successful. The base- line untreated rates were 22% in 52 weeks and 17% in 36weeks, respectively, in the Italian and Canadian patients, Several studies also report success with SO/IUI in the indicating that the patient populations were similar. The treatment of endometriosis-associated infertility. In an RCT main difference was the lower power of the Italian study, comparing clomiphene citrate and IUI with preovulatory which was planned to detect a 2.7 fold higher live birth rate intercourse in patients with unexplained infertility or surgi- with ablation/resection When the results are combined, cally corrected endometriosis, a statistically significant in- there is no significant statistical heterogeneity and the overall crease in cycle fecundity was seen with four cycles of absolute difference is 8.6% in favor of therapy (95% CI 2.1, clomiphene citrate/IUI compared with controls (0.095 versus 15) The number needed to treat is 12 (95% CI 7, 49).
0.033, respectively) Another study randomized patients Thus, for every 12 patients having Stage I/II endometriosis to receive either gonadotropins with intercourse or gonado- diagnosed at laparoscopy, there will be one additional suc- tropins with IUI All patients had endometriosis previ- cessful pregnancy if ablation/ resection of visible endome- ously treated with laser laparoscopy. The fecundity was triosis is performed, compared to no treatment. There is no greater in the gonadotropin/IUI group (0.129; n ϭ 109) than evidence that the outcome is affected by the method of in the intercourse group (0.066; n ϭ 76). A randomized trial ablation, by electro-surgery or laser delivery systems of 40 women with stage I/II endometriosis and infertilitystudied the effect of either three cycles of gonadotropin/IUI A nonrandomized study demonstrated that the cumula- or no treatment (expectant management) The fecundity tive probability of pregnancy in 216 infertile patients with was 0.15 in the gonadotropin/IUI group and 0.045 in the severe endometriosis, followed for up to 2 years after lapa- untreated group (PϽ.05). Another study reported on the roscopy or laparotomy, was significantly increased, 45% and effects of expectant management, clomiphene citrate, gonad- 63%, respectively These and other observational stud- otropins or in vitro fertilization-embryo transfer (IVF-ET) on ies, that are not free from bias, suggest that in women with fecundity in women with infertility and minimal or mild Stage III/IV endometriosis, without other identifiable infer- endometriosis The observed cycle fecundity with go- tility factors, conservative surgical treatment with laparos- nadotropin treatment alone (0.073) was significantly higher copy and possible laparotomy may increase fertility COMBINATION MEDICAL AND SURGICAL THERAPY
Combination medical and surgical therapy for endometriosis The most recent report on in vitro fertilization-embryo transfer consists of either preoperative or postoperative medical ther- (IVF-ET) outcomes in the United States indicates that the overall apy. Although theoretically advantageous, there is no evi- delivery rate per retrieval in infertile women is 29.4% dence in the literature that combination medical-surgicaltreatment significantly enhances fertility and it may unnec- There are no large RCTs which definitely demonstrate that essarily delay further fertility therapy. Preoperative therapy IVF-ET is more effective than expectant management in the is reported to reduce pelvic vascularity and the size of treatment of stage-specific infertility associated with endome- endometriotic implants, thus reducing intraoperative blood triosis. In one small RCT, 21 women with endometriosis and loss and decreasing the amount of surgical resection needed.
infertility were randomized to receive either IVF (n ϭ 15) or Postoperative medical therapy has been advocated as a expectant management (n ϭ 6) None of the women in the means to eradicate residual endometriotic implants in pa- expectant management group became pregnant compared to five tients with extensive disease in whom resection of all im- of the 15 women who received IVF-ET (33%, PϭNS) plants is impossible or inadvisable. Postoperative hormonaltherapy may also treat “microscopic disease”; however, none Several studies suggest that in women with advanced of these treatments has been proven to enhance fertility.
endometriosis, long-term treatment with GnRH-a before ini-tiation of a cycle may improve fecundity. Among patientswith severe endometriosis, 6 months of hormonal suppres- SUPEROVULATION AND INTRAUTERINE
sion with GnRH-a resulted in higher numbers of oocytes INSEMINATION (COH/IUI)
retrieved, embryos transferred, and pregnancies The Superovulation (SO) with gonadotropins and intrauterine investigators concluded that long-term GnRH-a therapy insemination (IUI) are frequently used to treat women might reduce preclinical abortions in patients with severe with infertility An NIH Reproductive Medicine Net- endometriosis who are undergoing IVF-ET A recent study work study of 932 infertile couples with Stage I/II endo- demonstrated the benefits of prolonged down-regulation with metriosis or otherwise unexplained infertility randomized GnRH-a before initiation of IVF-ET in patients with endome- patients to intracervical insemination (IC), IUI, gonado- triosis In this RCT, the overall experience with 51 patients tropin/IC or gonadotropin/IUI. In this large RTC the undergoing IVF-ET demonstrated significantly higher ongoing Endometriosis and infertility
Cycle fecundity in women with stage I or II endometriosis, according to treatment.
Endometriosis-associated infertility
No treatment or intracervical insemination a PϽ.05 for treatment vs. no treatment.
ASRM Practice Committee. Endometriosis and infertility. Fertil Steril 2006. pregnancy rates with prolonged dura- tion of GnRH-a use tive surgery with laparoscopy and possible laparotomy are before IVF-ET Although these studies suggest that longer recommended. Several studies suggest that surgical therapy periods of pretreatment with GnRH-a will improve implanta- increases fertility in women with advanced endometriosis tion rates in patients, with endometriosis who undertake IVF- These studies indicate that expectant management is not a good ET, support for this treatment strategy is not unanimous option for women with infertility and severe endometriosis.
However, it should be pointed out that there are no RCTs to CLINICAL APPROACH TO INFERTILE WOMEN
define results of surgical treatment for stage III/IV disease.
For infertile women who have stage III/IV endometriosis Clinical decisions in the management of infertility associated and have previously had one or more infertility operations, with endometriosis are difficult because few RCTs have IVF-ET is often a better therapeutic option than another been conducted to evaluate and compare the effectiveness of infertility operation. There is no sufficiently powered pro- the various forms of treatment. Moreover, the available data spective randomized trial evaluating the effect on pregnancy are conflicting and prevent confident conclusions.
outcome of surgical treatment followed by IVF-ET versus For infertile women with suspected stage I/II endometri- IVF-ET alone. In one retrospective study, 23 women with osis, a decision must be made whether to perform laparos- stage III/IV endometriosis underwent IVF-ET and 18 copy before offering treatment with clomiphene, gonadotro- women underwent repeat surgery The pregnancy rate pins or IVF-ET. Clearly, the factors such as the patient’s age, after two cycles of IVF-ET was 70%, whereas the cumula- duration of infertility, family history and pelvic pain must be tive pregnancy rate was 24% within 9 months of a repeat taken into consideration. When laparoscopy is performed, operation. If initial surgery fails to restore fertility in patients the safe ablation or excision of visible endometriosis should with moderate to severe endometriosis, IVF-ET is an effec- be considered based on observations from RTC. This should tive alternative. In summary, there are limited data available be discussed openly with the patient when planning her to estimate the effect of surgical treatment in addition to treatment. Of course, if pain were also a concern, laparos- IVF-ET on the outcome of pregnancy in endometriosis- copy and surgical treatment would be appropriate. Expectant management after laparoscopy is an option for youngerwomen. Alternatively, superovulation with IUI may be of- SUMMARY AND RECOMMENDATIONS
fered. Female age is an important factor in designing ther- ● There are few RCTs on the treatment of endometriosis- apy. After age 35, there is a significant decrease in fecundity and an increase in the spontaneous abortion rate. The de- ● Female age, duration of infertility, family history, pelvic crease in fecundity due to the two variables of endometriosis pain and stage of endometriosis should be taken into and age may be additive. Consequently, in the older infertile account when formulating a management plan.
woman with endometriosis, a more aggressive therapeutic ● When laparoscopy is performed, the surgeon should consider plan with SO/IUI or IVF-ET may be reasonable rather than safely ablating or excising visible lesions of endometriosis.
● In women with stage I/II endometriosis-associated infer- For infertile women with ASRM 1996 stage III/IV endome- tility, expectant management or superovulation/IUI after triosis and no other identifiable infertility factor the conserva- laparoscopy can be considered for younger patients.
Women 35 years of age or older should be treated with 16. Lessey BA, Castelbaum AJ, Sawin SW, Buck CA, Schinnar R, Bilker W, et al. Aberrant integrin expression in the endometrium of women with endometriosis. J Clin Endocrinol Metab 1994;79:643–9.
In women with stage III/IV endometriosis-associated in- 17. Genbacev OD, Prakobphol A, Foulk RA, Krtolica AR, Ilic D, Singer fertility, conservative surgical therapy with laparoscopy MS, et al. Trophoblast L-selectin-mediated adhesion at the maternal- and possible laparotomy are indicated.
fetal interface. Science 2003;299:405– 8.
● For women with stage III/IV endometriosis who fail to 18. Kao LC, Germeyer A, Tulac S, Lobo S, Yang JP, Taylor RN, et al.
Expression profiling of endometrium from women with endometriosis conceive following conservative surgery or because of ad- reveals candidate genes for disease-based implantation failure and vancing reproductive age, IVF-ET is an effective alternative.
infertility. Endocrinology 2003;144:2870 – 81.
19. American Society for Reproductive Medicine. Revised American Society Acknowledgments: This report was developed under the direction of the for Reproductive Medicine classification of endometriosis: 1996. Fertil Practice Committee of the American Society for Reproductive Medicine as a service to their members and other practicing clinicians. While this 20. Schenken RS. Modern concepts of endometriosis. Classification and its document reflects appropriate management of a problem encountered in the consequences for therapy. J Reprod Med 1998;43:269 –75.
practice of reproductive medicine, it is not intended to be the only approved 21. Bayer SR, Seibel MM, Saffan DS, Berger MJ, Taymor ML. Efficacy of standard of practice or to dictate an exclusive course of treatment. Other danazol treatment for minimal endometriosis in infertile women. A plans of management may be appropriate, taking into account the needs of prospective randomized study. J Reprod Med 1988;33:179 – 83.
the individual patient, available resources, and institutional or clinical 22. Fedele L, Parazzini F, Radici E, Bocciolone L, Bianchi S, Bianchi C, et practice limitations. This report was approved by the Board of Directors of al. Buserelin acetate versus expectant management in the treatment of the American Society for Reproductive Medicine in September 2003.
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more trials: concepts to be kept in mind [letters]. Hum Reprod 2000; 3. Hughes EG, Fedorkow DM, Collins JA. A quantitative overview of con- trolled trials in endometriosis-associated infertility. Fertil Steril 1993;59: 27. Guzick DS, Carson SA, Coutifaris C, Overstreet JW, Factor-Litvak P, Steinkampf MP, et al. Efficacy of superovulation and intrauterine in- 4. Counsellor VS. Endometriosis. A clinical and surgical review. Am J semination in the treatment of infertility. N Engl J Med 1999;340:177– 83.
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tive evidence from an artificial insemination by donor program. Fertil 30. Fedele L, Bianchi S, Marchini M, Villa L, Brioschi D, Parazzini F.
Superovulation with human menopausal gonadotropins in the treatment 8. Portuondo JA, Echanojauregui AD, Herran C, Alijarte I. Early conception of infertility associated with minimal or mild endometriosis: a con- in patients with untreated mild endometriosis. Fertil Steril 1983;39:22–5.
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Endometriosis and infertility



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