Hum. Reprod. Advance Access originally published online on January 26, 2006
Human Reproduction 2006 21(5):1212-1217; doi:10.1093/humrep/dei493
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Ovarian response to stimulation of HIV-positive patients during IVF treatment: a matched, controlled study
1 Department of Obstetrics and Gynaecology and 2 Department of Internal Medicine, Division of Infectious Diseases, CHU Saint-Pierre, Université Libre de Buxelles, Brussels, Belgium
3 To whom correspondence should be addressed at: Department of Obstetrics and Gynaecology, CHU Saint-Pierre, 322 rue Haute, 1000 Brussels, Belgium. E-mail: annick_delvigne{at}stpierre-bru.be
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Abstract |
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BACKGROUND: Our aim was to compare the ovarian response of HIV-positive and -negative patients during IVF. METHODS: Setting – HIV and IVF reference university hospital. Twenty-seven HIV-infected patients who had undergone IVF between March 2000 and March 2005 were matched with 77 HIV-negative patients for age, aetiology of infertility, whether it was primary or secondary infertility, duration of infertility, history of pelvic surgery and type of pituitary inhibition. Outcome – poor responders were defined using one of the following criteria: a cancelled cycle (for insufficient ovarian response), less than four mature follicles (
16 mm), peak serum levels of E2 lower than 1000 pg/ml. RESULTS: There were no differences between the two groups of patients for the matched criteria. The proportion of African women and of women with a history of pelvic inflammatory disease was significantly higher among HIV patients than among the control group. With the exception of a lower number of transferred embryos among HIV-positive patients versus HIV-negative ones (1.3 versus 1.9; P = 0.035), there was no significant difference between the two groups of patients regarding ovarian response parameters. CONCLUSION: HIV-infected patients who are in good general condition and who are matched to a control group present a similar ovarian response to stimulation, suggesting the existence of a similar ovarian reserve.
Key words: case-control study/HIV/IVF/poor response
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Introduction |
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At the beginning of the AIDS epidemic, because of the poor prognosis of those infected with the disease, couples with an infected HIV partner were discouraged from planning a pregnancy. AIDS remains worldwide a serious condition with a continuing mortality, and even in industrial countries where efficient and innovative treatments are available, HIV infection remains a chronic disease with high morbidity. Nevertheless, due to anti-retroviral therapies, life expectancy of many seropositive patients as well as their quality of life have dramatically improved during the last 10 years and many couples, with an HIV-positive partner, can consider pregnancy planning (Minkoff and Santoro, 2000
; Englert et al., 2001; Bujan et al., 2004). Assisted reproductive technology (ART) reduces the risk of contamination of the uninfected partner and helps couples conceive (Minkoff and Santoro, 2000; Garrido et al., 2004; Semprini and Fiore, 2004). Furthermore, in recent years, the vertical transmission risk (the risk of infecting the newborn baby) has drastically decreased (to become less than 2%) due to the ability to reach undetectable maternal viral loads during pregnancy, the liberal use of Caesarean section and restricted breastfeeding (Coll et al., 2002). Finally, certain authors have observed that pregnancy does not worsen the progression of HIV infection or its immunological parameters (Brettle et al., 1995; Saada et al., 2000). In this reassuring context, many IVF centres have decided to treat serodiscordant couples using ART (Delvigne et al., 2001; Ohl et al., 2003; Terriou et al., 2005). As this change in attitude is quite recent, few data are available about the IVF/ICSI results in HIV-infected patients, totalling only 178 IVF cycles in less than one hundred couples (Coll et al., 2002; Ohl et al., 2003; Ohl et al., 2005; Terriou et al., 2005). Most epidemiological data about fertility in HIV-infected patients have been obtained in developing countries, suggesting reduced pregnancy rates in HIV-infected women as compared with the general population (Gray et al., 1998; Yaro et al., 2001). However, in these studies, many confounding factors intervene, such as sexually transmitted diseases or fear of contamination resulting in reduced sexual contact. In industrial countries, other factors may explain the reduced fertility seen in HIV-positive patients. These patients are often older, as pregnancy was discouraged for many years. Drug addiction, one of the causes of contamination, is also an important confounding factor, as drugs, such as opiates, have been shown to induce a dysfunction of the hypothalamic-pituitary-gonadal axis (Cicero et al., 1974; Smith and Asch, 1987). Currently, there are very few data concerning a possible untoward effect of the HIV virus and its treatment on ovarian function (Lo and Schambelan, 2001). Five years ago, our department, (a tertiary ART centre and Infectious Disease Clinic), decided to start treating HIV couples for their fertility problems using a specific protocol (Delvigne et al., 2003). The request of each couple is evaluated by a multidisciplinary group including a fertility specialist, an obstetrician, a pediatrician, a specialist in infectious diseases and a psychiatrist who will deliver specific information and counselling. All decisions are taken during multidisciplinary meetings involving all of the above. There are no a priori exclusion criteria except the sole condition to be a couple. Nevertheless, the history of the patient concerning viral load and the T-cell-count evolution, the stage of disease, the possible development of drug resistance and the patient’s compliance are considered (Delvigne et al., 2003).
On the basis of clinical impression, some of our physicians hypothesized that seropositive women might have a reduced ovarian response to stimulation as compared with uninfected patients. Other authors have also assessed the quality of ovarian response in these patients (Coll et al., 2005; Terriou et al., 2005). This study compares the ovarian response of HIV-positive patients to that of negative ones, using a matched, control study allowing for the most important confounding factors.
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Materials and methods |
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In this retrospective, case-matched, control study, all HIV-infected women who had been treated by IVF in our department, between March 2000 and March 2005 (n = 33), were included. The diagnosis of infertility in HIV-positive patients relied on one of the following criteria: (i) intercourse without pregnancy after a period lasting for at least 1 year (sometimes within the couple where both partners are HIV positive, or during a period anterior to the diagnosis of the HIV infection), and at this time an evaluation of the infertility aetiology is carried on, which will indicate whether IIU or IVF will be used; (ii) identification of an infertility factor (often tubal or male) during the latter evaluation; (iii) more than 1 year of self-inseminations or 4–6 months of medically assisted inseminations (IIU); (iv) an identified infertility factor in the history of one of the partners. Only the first cycle of each patient was considered except in three cases for which the first cycle had been interrupted for non-medical reasons (non-observance of the stimulation cycle or failure to obtain sperm from the partner). In these three cases, we compiled a second IVF cycle. For each HIV case, we selected three matched controls. These were taken from a data bank containing all HIV-negative patients who had been treated for a first IVF cycle during the same period of time (n = 1324 patients). Matching criteria were as follows: age of the patient (±1 year), aetiology of the fertility problem, whether it concerned primary or secondary infertility, duration of the infertility (±2 years), history of pelvic surgery and type of pituitary inhibition (long or short treatments). In the event that several control patients were found for these criteria, three of them were randomly chosen. The selection and exclusion of controls was carried out blindly, without the knowledge of other relevant clinical data or outcome of the IVF trial. We excluded six HIV-positive patients, as we were unable to match them according to the predetermined matched criteria (older age, long period of infertility and a history of ovariectomy). The age restriction in our program is identical in HIV-postive or -negative women. Nevertheless, because the pool of aged patients is smaller, we were unable to find appropriate matched controls for these six patients. The IVF outcome of these six patients was as follows: two cycles were cancelled, there was one oocyte retrieval failure and there were three implantation failures. For two other cases, we were able to find only one matched, control instead of three (one patient had been stimulated using a short GnRH protocol and the other had a history of ovarian cyst resection).
In the end, we included and analysed 27 cases which were matched with 77 controls.
Collected information
The following relevant clinical data were collected prospectively during the IVF trial and encoded in the patients’ medical file which was stored in a databank, i.e. the patient’s age, her gynaecological history, known aetiology of the infertility, treatments that have been used and ethnic origin. Although we did not use a standard screening test for ovarian reserve, serum levels of FSH, LH and estradiol (E2) were measured on the third day of the cycle in some patients.
In HIV-positive patients, information about the viral load and CD4 levels at the time of the IVF trial is also systematically collected. For patients who had an undetectable viral load, the limit was set at 49 copies/ml as the minimal (detection was 50 copies/ml). Data about the IVF trial response were recorded: the number of retrieved oocytes, the total dose of administered gonadotrophins, the number of obtained mature follicles (more than 16 mm in diameter), peak serum level of E2, number of retrieved oocytes, number of days of stimulation and whether the cycle was cancelled, the fertilization rate (defined as the number of 2 and 3 pronucleï zygotes obtained, divided by the number of retrieved oocytes), the number and rate of mature oocytes (defined as the number of oocytes with extrusion of the first polar body divided by the number of retrieved oocytes) and the number (defined as embryos graded 1–6 according to Dokras et al., 1993 criteria) and rate of top quality embryos (number of top embryos divided by the total number of obtained embryos). We also evaluated the number of clinical pregnancies (defined as the presence of a gestational sac at ultrasound or chorionic villi at pathological examination of abortion material).
Poor responders were defined using one of the following criteria: a cycle cancelled for insufficient ovarian response, less than four mature follicles (measuring 16 mm or more) or peak serum levels of E2 that were lower than 1000 pg/ml.
The ratio between the maximum E2 levels and total amount of administered gonadotrophins as well as the ratio between the number of retrieved oocytes and total amount of administered gonadotrophins was calculated.
Ovarian stimulation was carried out with the same long treatment protocols in infected and uninfected patients (Delvigne et al., 2003). All these procedures were approved by the local ethical committee.
Statistical analysis was performed using the program Statistix (conditional logistical regression) or using SPSS (non-paired Mann–Whitney test). The level of significance was set at P < 0.05).
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Results |
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The clinical characteristics of the 27 seropositive patients and the 77 controls are presented in Table I. There were no differences between the two groups of patients for the matched criteria (age, duration of infertility, proportion of primary and secondary infertility and infertility aetiology). On the other hand, the proportion of African women and of women with a history of pelvic inflammatory disease was significantly higher among HIV patients than among the control group (P = 0.0094 and P = 0.0298, respectively). All the patients were asymptomatic. The mean duration of their disease was 7 years (range 2–17). The mean CD4 level was 574/ml (range 161–1478); two patients had levels of CD4 lower than 200/ml. The mean viral load was 1783 copies/ml (range not detectable to 9900). Sixteen patients had an undetectable viral load. At the time of the IVF trial, 18 HIV patients were treated and 10 among them were using proteases inhibitors. In total, 15 patients had been treated with proteases inhibitors at some time.
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With the exception of a lower number of transferred embryos among HIV-positive patients versus HIV-negative ones (1.3 versus 1.9; P = 0.035), there was no significant difference between the two groups of patients regarding ovarian response parameters (Table II). Elective Single embryo transfer occurred in 31.6 and 15.5% of the embryo transfers in HIV-positive and -negative women, respectively. Moreover, only one embryo was obtained (and transferred) in 15.7 and 5.1% of HIV-positive and -negative women, respectively. The comparison between these different parameters shows only a slight tendency towards a lower response among HIV-positive patients, but no significance could be established in this respect.
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Discussion |
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This study evaluates the ovarian response to IVF stimulation of HIV-positive patients as compared with control patients. Various definitions have been proposed to characterize ‘poor responders’, but no consensus has emerged (Surrey and Schoolcraft, 2000
; Tarlatzis et al., 2003; Kailasam et al., 2004). Poor response may be evaluated, for instance, in terms of an insufficient number of collected follicles, insufficient number of oocytes retrieved, inadequate cumulative doses of administered gonadotrophins or low peak serum E2 (Surrey and Schoolcraft, 2000). Poor ovarian response has been correlated to insufficient ovarian reserve and to early menopause (De Boer et al., 2002; Nikolaou and Templeton, 2004). Other markers have been used to predict poor ovarian response: serum basal levels of FSH, inhibin and anti-Müllerian hormone, dynamic tests such as the clomiphene response test or the Exogenous FSH ovarian response test (EFFORT) and imaging techniques such as the ultrasound evaluation of the number of follicles and ovarian volume (Bukman and Heineman, 2001; Bancsi et al., 2002; Klinkert et al., 2005). Nevertheless, these tests are not very sensitive: only extreme values are indicative of poor ovarian reserve (Bancsi et al., 2003). Therefore, a diminished ovarian reserve and an inadequate ovarian response can only be diagnosed retrospectively after a trial of ovarian stimulation (Bancsi et al., 2003).
Some authors reported prolonged cycles and increased frequency of amenorrhea in asymptomatic HIV-positive patients, suggesting that HIV affects ovarian response (Chirgwin et al., 1996; Harlow et al., 2000). Not all authors observed such findings, however, as in HIV-positive patients with regular cycles, hormonal serum levels comparable with those of the general population were found (Shah et al., 1994; Ellerbrock et al., 1996; Cu-Uvin et al., 2000). In patients at an advanced stage of AIDS, on the contrary, increased prevalence of amenorrhea has been reported and attributed to metabolic imbalances and to cachexia (Grinspoon et al., 1997). This was not the case in this study, as all the patients were in good general condition. Two studies with limitations in their methodologies have assessed the age of menopause in HIV patients: Clark et al. (2000) reported an earlier menopause in 26 HIV-positive patients as compared with the general population; but 92% of the studied patients were smokers. The same group (Clark et al. 2000) also observed elevated FSH levels and a higher prevalence of anovulation.
In our study, we used standard doses of 150 U (or 250 U if the patient was older than 35 years) of gonadotrohins which was prescribed on day 3 of the first IVF cycle and adapted in relation to the ovarian response after a week of stimulation. No significant difference was observed between HIV-positive patients and matched, negative controls in terms of ovarian response to stimulation. The only significant difference was the number of transferred embryos, which was lower among HIV-positive patients but which can be explained by a voluntary reduction of the number of embryos transferred to reduce the risk of multiple pregnancies and the risk of vertical viral transmission. A similar attitude has been adopted by Ohl et al. (2005) and Terriou et al. (2005). This may partially explain a rather low pregnancy rate (11% in seropositive women versus 20.8% in seronegative ones, no significant difference between the two groups). Pregnancy rates are expressed per cycle and not per transfer and therefore include the cancelled cycles which also tended to be high among HIV-infected women, as reported by Terriou et al. (2005) and Ohl et al. (2005). The pregnancy rate calculated per transfer was 14%, which is lower than that obtained by Ohl et al. (2005) (23.9%), but comparable with those obtained by Terriou et al. (2005) (16.1%). The latter authors performed ICSI and IVF in a series of 29 seropositive women (66 cycles) and compared their results with an age-matched group of uninfected women and to their overall uninfected population. Higher cancellation rates and lower pregnancy rates were observed when the overall population was considered, but these differences disappeared when using an age-matched group. Coll et al., (2005) also found a clinical pregnancy rate of 16.2% among infected patients (n = 50) which was half that of a group of age-matched uninfected patients (37.5%). When they restricted their analysis only to cycles with oocyte donation, these differences disappeared (36.0 versus 44% patients, respectively). These authors concluded, therefore, that poor IVF results in HIV-positive women, which may be due to reduced ovarian response. Finally, Guibert et al. (2004) observed increased FSH levels on the third day of the cycle in a population of 80 HIV-positive patients as compared with a control group of similar age (n = 70) and concluded that HIV infection accelerates the ovarian reserve depletion. On the other hand, when selecting women younger than 42 years of age, with normal basal FSH and inhibin levels, no difference in ovarian response was observed between HIV-positive (n = 14) and HIV-negative patients. The authors concluded that IVF is not influenced by HIV infection in patients with normal ovarian reserve. These discrepancies in the results between studies may be explained by heterogeneities in the studied populations: for instance, the low pregnancy rate in HIV-positive women may also be explained in our population by a high prevalence of myoma found in this predominantly African population (six patients out of 27), which may be less often surgically treated because of their HIV status. Differences in the matching processes and lack of power of the various studies are other possible explanations. We have not excluded patients involved in an ART program, based on their age or the results of predictive tests of the ovarian reserve. This study is still hampered by a number of limitations: a higher incidence of history of PID was observed among HIV-positive patients than among HIV-negative ones, although we matched cases and controls for age, fertility aetiology and past pelvic surgery. PID has been shown to reduce ovarian stimulation due to direct damage to the ovaries and follicle loss or due to mechanical alterations of follicle development. This may result from adherances or deficient ovarian vascularisation (Csemiczky et al., 1996; Keay et al., 1998). For instance, a significantly higher prevalence of serum IgG antibodies to Chlamydia trachomatis was observed in poor responders, suggesting a possible detrimental effect of C. trachomatis on subsequent ovarian function (Keay et al., 1998).
This may explain a tendency towards reduced ovarian response among HIV-positive patients. Other confounding factors were not considered in the matching and may also have induced a bias: smoking, excess or insufficient body mass index race, family history of early menopause or a history of toxicomania (Augood et al., 1998; El-Nemr et al., 1998; Cooper et al., 2003; Fedorcsak et al., 2004). One should notice that in this series of patients only one woman presented a history of drug addition. There was, however, a race bias, as 70% of HIV-infected women were of African origin as compared with 37.7% of the controlled group.
In conclusion, this study reports that HIV-infected patients who are in good general condition and who are matched to a control group (for age, infertility aetiology, length and type of infertility and history of pelvic surgery) present a similar ovarian response to stimulation, suggesting the existence of a similar ovarian reserve. The clinical impression of physicians that HIV-infected patients respond less well to IVF stimulation is probably due to a bias and to confounding factors such as a more advanced age and a high prevalence of tubal pathologies among HIV-infected women.
Obviously, further studies should include larger numbers of patients. They could also involve histological evaluation of the ovaries of infected patients as well as epidemiological study of menopausal age in HIV-positive patients and evaluation of ovarian reserve in relation to the severity of HIV disease.
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Acknowledgements |
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We acknowledge Christian Melot (Prof of Statistics ULB) for his statistical advice and help.
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Submitted on September 23, 2005; resubmitted on December 7, 2005; accepted on December 14, 2005.
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