Hum. Reprod. Advance Access originally published online on January 28, 2009
Human Reproduction 2009 24(5):1092-1098; doi:10.1093/humrep/den491
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Anxiety and depression have no influence on the cancellation and pregnancy rates of a first IVF or ICSI treatment
1 Department of Obstetrics and Gynaecology, Radboud University Nijmegen Medical Centre, 6500 HB Nijmegen, The Netherlands 2 Department of Medical Psychology, Radboud University Nijmegen Medical Centre, PO Box 9101, 6500 HB Nijmegen, The Netherlands 3 Department of Public Health, Erasmus MC, University Medical Center, Dr Molewaterplein 50, PO Box 2040, 3000 CA Rotterdam, The Netherlands 4 Department of Gynaecology and Obstetrics, St Elisabeth Hospital, Hilvarenbeekse Weg 60 5022 GC Tilburg, The Netherlands
5 Correspondence address. Tel: +31-24-3619573; Fax: +31-24-3668597; E-mail: a.lintsen{at}obgyn.umcn.nl
| Abstract |
|---|
|
|
|---|
BACKGROUND: After many years of research, the impact of psychological distress on the IVF treatment outcome is still unclear. This study aimed to determine the influences of anxiety and depression before and during IVF or ICSI treatment on the cancellation and pregnancy rates of inductees.
METHODS: In a multicentre prospective cohort study, we assessed anxiety and depression at baseline and the procedural anxiety level one day before oocyte retrieval, with the short versions of the State Anxiety Inventory (STAI) and the Beck Depression Inventory-Primary Care (BDI-PC). The effect of baseline anxiety and depression on the cancellation and pregnancy rates of 783 women in their first IVF or ICSI treatment was evaluated. We also determined if a change in anxiety from the start of treatment until just before oocyte retrieval affects the pregnancy rate. The predictive value of distress was assessed while controlling for several factors in subfertility treatment.
RESULTS: Neither baseline nor procedural anxiety, nor depression affected the ongoing pregnancy rates, with odds ratios (ORs) of 1.04 (95% CI 0.82–1.33), 0.96 (95% CI 0.77–1.20) and 0.85 (95% CI 0.65–1.10), respectively. Neither did the anxiety gain score affect the pregnancy rate, OR 1.08 (95% CI 0.83–1.41). A cancellation of treatment could not be predicted by either anxiety or depression, OR 1.16 (95% CI 0.83–1.63) and 0.85 (95% CI 0.59–1.22), respectively.
CONCLUSIONS: Inductees in IVF treatment can be reassured that anxiety and depression levels before and during treatment have no significant influence on the cancellation and pregnancy rates.
Key words: anxiety/depression/distress/IVF/pregnancy rate
| Introduction |
|---|
|
|
|---|
Subfertility and stress are inextricably linked. Women experience the period of a long unfulfilled child wish, and the treatments that may arise from this need, as very stressful. The perception that stress has an adverse effect on the chance of pregnancy has become widely accepted, but in spite of many years of research on psychological factors and IVF outcome, the results are still contradictory. Reviews have suggested a negative association between distress and IVF outcome (Eugster and Vingerhoets, 1999
Stress before and during the IVF treatment is multidimensional. There is the chronic source of stress caused by the threat of the permanency of the infertility and loss of hope. Another source of stress is the prospect of the treatment itself. These sources of distress can be measured before treatment, by baseline anxiety and depression. In addition, the third source of stress is the actual participation in the treatment, which can be measured by the level of anxiety as a result of the threat of the treatment itself, the so-called procedural or situational distress at a certain point in time. It can be the fear of the daily hormone injections or a painfully oocyte retrieval, or the strain of the emotional moment at the embryo transfer.
Several prospective studies (with a range of women studied: between 40 and 291 inductees), have differentiated with standardized psychological tests, the influence of baseline anxiety or depression and/or procedural distress on the chance of IVF pregnancy: a high baseline distress level has negatively influenced the pregnancy rate in the studies of Demyttenaere et al. (1992), Thiering et al. (1993
), Klonoff-Cohen et al. (2001
), Smeenk et al. (2001
), Verhaak et al. (2001
), Eugster et al. (2004
) and in a large study of Boivin and Schmidt (2005
) (818 couples, 75% were inductees). Conversely, baseline distress did not affect the pregnancy chance in the studies of Merari et al. (1992
), Boivin and Takefman (1995
), Emery et al. (2003
), Anderheim et al. (2005
) and De Klerk et al. (2008)
. Indications of adverse effects of procedural stress, as measured by psychological or biological tests (e.g. hormone level), on the chance of IVF pregnancy were established by Boivin and Takefman (1995
), Facchinetti et al. (1997
), Gallinelli et al. (2001)
and Smeenk et al. (2005
). On the other hand, this influence was not found by Klonoff-Cohen et al. (2001
), Lovely et al. (2003
) and De Klerk et al. (2008)
. Contrary to all expectations, Merari et al. (1992
) observed a significant higher state of anxiety level before oocyte retrieval for women who became pregnant. According to the study of Boivin and Takefman (1995
), the period of the highest stress level during an IVF treatment is measured between hCG administration and oocyte retrieval. Also the association of a lower adrenalin level at oocyte retrieval with an increased pregnancy chance observed by Smeenk et al. (2005
) implicates that high anxiety levels shortly before oocyte retrieval might influence the implantation phase. To gain more insight into the interaction of stress and IVF treatment, we also studied if a change in anxiety, measured before treatment and just before oocyte retrieval, has a independent effect on the pregnancy rate. Furthermore, pretreatment depression and anxiety scores have been related to the passive dropout rate, concerning patients who voluntarily discontinue after first or subsequent treatment (Smeenk et al., 2004
). In this study, we assessed if basal psychological distress also has an association with unfinished, so-called cancelled treatments. By discriminating the influence of distress on the cancelled versus the non-cancelled cycles, we tried to distinguish the influence of distress on the stimulation phase versus the implantation phase.
In summary, so far studies on distress and IVF pregnancy are still inconclusive. The objective of this large prospective multicentre study with women having their first IVF or ICSI treatment is to determine the influence of distress at different points during treatment and with different end-points, while controlling for potential confounding factors in fertility treatment.
| Materials and Methods |
|---|
|
|
|---|
Design and subjects
We performed a prospective study in seven IVF clinics in the Netherlands: one university hospital and two general hospitals with licensed IVF laboratories, one satellite and three transport IVF clinics. In the latter two types of clinics, the stimulation phase is started and the patients are referred to the licensed IVF centre for oocyte retrieval and/or embryo transfer. All new couples with an indication for IVF or ICSI treatment according to the IVF guideline formulated by the Dutch Society for Obstetrics and Gynaecology (NVOG, IVF guideline no 9, 1998
This study was part of the national cohort study, on prediction of pregnancy rates with IVF and ICSI treatment, that was performed between 2002 and 2004 and published recently (IVF dataset: Lintsen et al., 2007
). The IVF outcome data and the fertility specific background variables, such as pregnancy history, duration and cause of subfertility of all inductees participating to this study, as well as all other inductees, were registered in the national cohort study. The psychological dataset was matched with the IVF dataset of the seven participating hospitals.
The ethical committees of the participating clinics gave approval for the study.
IVF treatment
The treatment protocols were hospital specific, but all women were treated with conventional ovarian stimulation with gonadotrophins combined with a preceding pituitary down-regulation through a GnRH agonist co-treatment. The oocyte retrieval was timed 34–36 h after administration of 5000 or 10 000 IU hCG. Fertilization was performed by standard IVF or ICSI technique. A maximum of two embryos were transferred. Luteal support was given by progesterone vaginally. Additional good quality embryos were cryopreserved and transferred in a later cycle if the treatment had been unsuccessful.
Distress measures
The baseline emotional status was defined in terms of state anxiety and depression. Anxiety was measured by means of the abridged Dutch version of the State Anxiety Inventory (STAI: Dutch translation: Spielberger, 1983
; van der Ploeg et al., 2000
), by 10 items, out of 20, each ranging in score from 1 to 4. Each item has a four-point evaluation with a maximum sum score of 40, which indicates highest anxiety. Depression was measured using the Beck Depression Index for primary care (BDI-PC) (Beck et al., 1997
). The BDI-PC consists of 7, out of a total of 21 items, ranging from 0 to 3 to indicate the severity of the symptoms. The maximum score could be 21. The questionnaires used have shown reliability and validity (Huiskes et al., 1990a
, b
; Verhaak et al., 2001
, 2005
, 2006
). The questionnaire on T1, one or two months before the start of treatment, measured the baseline anxiety and depression status by asking how the participant has felt over the last week. The questionnaire on T2, one day before oocyte retrieval, measured the procedural state anxiety by means of the same abridged Dutch version of the STAI. The stress response to treatment was assessed by comparing baseline anxiety at T1 with procedural anxiety at T2 and calculating the residual gain score indicating a change in anxiety by controlling for baseline anxiety. The different scales showed excellent reliability: anxiety alpha = 0.88; depression alpha = 0.82.
Definitions
Primary subfertility indicates that the woman had no pregnancy before referral to IVF. Duration of subfertility is defined as the time between the date of active child wish, or the date of last miscarriage, and the date of first IVF. The cause of subfertility contributing to the primary indication for IVF was divided into tubal, hormonal, unexplained, endometriosis, mild male-related subfertility, treated with IVF, and severe male subfertility, treated with ICSI. The first outcome measure was ongoing pregnancy after first IVF or ICSI treatment, confirmed by ultrasound of at least one fetus with positive heartbeat at 8 weeks gestation. A second outcome measure was cancellation of treatment, defined as having started stimulation without reaching oocyte retrieval.
Data analyses
Univariate frequencies and means of biological patient characteristics were calculated and compared between participants versus non-participants. Univariate frequencies of psychological scores at baseline were calculated for women with a cancelled cycle versus women who completed the first cycle, and psychological scores were compared between pregnant versus non-pregnant women. Multivariate logistic regression analyses were used to estimate the predictive effect of psychological scores on the probability of cancellation and of an ongoing pregnancy in non-cancelled cycles. The psychological scores were the baseline state anxiety and depression level at T1, the procedural state anxiety level at T2 and the residual gain score from T1 to T2. We adjusted for the following established variables: women's age, pregnancy history, cause and duration of subfertility (Stolwijk et al., 1996
; Templeton et al., 1996
; Lintsen et al., 2007
). All analyses were performed using SPSS 14.0. Statistical testing on all outcome measures was done at a 0.05 two-sided level of significance.
| Results |
|---|
|
|
|---|
Of 1124 eligible women 783 women filled in the first questionnaire before the start of treatment (70% participation). Figure 1 provides a flowchart of the inclusion. For 78 women, the treatment was cancelled before oocyte retrieval. 284 women did not complete, or forgot to bring along, the second questionnaire that had to be filled in one day before oocyte retrieval. We had complete follow-up of the first IVF or ICSI treatment for 421 women who filled in a questionnaire at both T1 and at T2. Table I presents baseline characteristics and main treatment outcomes of women at T1, of women who also contributed at T2, and of all other inductees in the period of study treated in one of the hospitals involved (non-participants to this study). Frequencies and means are equivalent for the three groups. The mean duration of subfertility was longer in the non-participating group.
|
|
Table II shows that there were no differences in the mean anxiety and depression levels at baseline and no differences in the frequencies and means for biological variables for women who completed a first cycle and for women who did not reach the oocyte retrieval because of cancellation. Women with a cancelled cycle did have a longer mean duration of subfertility compared with women who completed the first cycle (3.9 versus 3.3 years, P = 0.02).
|
In Table III, the levels of anxiety and depression before and during IVF treatment and the anxiety gain score from pretreatment to oocyte retrieval are shown to be not different for pregnant compared with non-pregnant women. Pregnant women were younger than non-pregnant women, but the level did not reach significance.
|
We constructed a multivariable logistic regression model for the prediction of cancellation and the ongoing pregnancy rate with the basal anxiety and depression scores at T1 (Table IV). We also build a model for the prediction of the chance of ongoing pregnancy with procedural anxiety at T2 and with the anxiety gain score from T1 to T2 (the latter two models not shown). In all models we adjusted for potential biological confounders: female age, pregnancy history, duration and cause of subfertility. Overall, as could be expected from the univariate results, neither baseline anxiety nor depression showed an influence on the cancellation rate, with ORs 1.16 (95% CI 0.83–1.63) and 0.85 (95% CI 0.59–1.22), respectively. The chance of cancellation could be predicted by a longer duration of subfertility, OR 1.14 (95% CI 1.01–1.27). There was no influence of baseline, or procedural anxiety, nor of the anxiety gain score on the ongoing pregnancy rate, ORs 1.04 (95% CI 0.82–1.33), 0.96 (95% CI 0.77–1.20) and 1.08 (95% CI 0.83–1.41), respectively. Depression could not predict the pregnancy rate either, OR 0.85 (95% CI 0.65–1.10). Pregnancy history, duration and cause of subfertility also had no influence on the pregnancy rate. With higher female age, there was a trend towards a decreased chance of pregnancy, OR 0.95 (95% CI 0.90–1.00) (P = 0.07). The results did not change if we used the composite score for anxiety and depression.
|
| Discussion |
|---|
|
|
|---|
In this large prospective multicentre study, we examined the relation of anxiety and depression on the rates of cancellation and pregnancy for women having their first IVF treatment. Both in univariate and in multivariate analyses, psychological distress before and during treatment did not affect the chance of pregnancy.
In accordance with other studies on anxiety before and during first IVF treatment, we did not find an impact of baseline psychological factors or procedural anxiety on the pregnancy rate (Thiering et al., 1993
; Boivin and Takefman, 1995
; Klonoff-cohen et al., 2001
; Emery et al., 2003
; Anderheim et al., 2005
; Smeenk et al., 2005
; De Klerk et al., 2008
). Influence of procedural stress in inductees before oocyte retrieval has been found only in small sample studies (Boivin and Takefman, 1995
; Facchinetti et al., 1997
; Gallinelli et al., 2001
).
Former results from our own research group have shown that high baseline state anxiety and depression levels have a negative impact on the chance of pregnancy for inductees (Smeenk et al., 2001
; Verhaak et al., 2001
), but this could not be confirmed later on (Smeenk et al., 2005
). In the latter study, the relation between anxiety and the pregnancy outcome was suggested with a lower baseline adrenalin and lower (nor)-adrenalin level at embryo transfer observed in women who succeeded with a pregnancy. In the current study, this relation could not be confirmed with the procedural anxiety level measured before oocyte retrieval.
Surprisingly, higher women's age showed only a trend towards a lower pregnancy chance. All other biological factors studied (pregnancy history, cause and duration of subfertility), did not have an impact on the pregnancy rate. These factors have been shown to be of importance in large prospective studies (Templeton et al., 1996
; Lintsen et al., 2007
). Despite participation of a fairly large number of women in this study, the number was probably not high enough to reach significance in the prediction of pregnancy.
We showed that psychological factors were not associated with the cancellation rate. In daily practice, the most important reason for cancellation will be medical: imminent ovarian hyperstimulation, or in contrast, poor ovarian response. However, this was not reflected in a difference of biological characteristics between cancelled and non-cancelled women. The only factor predicting cancellation was a longer duration of subfertility.
We compared the baseline state anxiety and depression levels of women that completed a questionnaire pretreatment with the anxiety and depression scores of the Dutch Community norms and found the levels of our participants to be within the normal range. This is in accordance with the systematic review of Verhaak et al. (2007
) in which the investigation of the emotional adjustment before the start of IVF treatment over the last 25 years is reviewed: the depression level of IVF patients in that study was similar compared with the norm groups, but the pretreatment state anxiety scores differed considerably for patient groups as well as for norm groups. This difference in the norm group is partly explicable by cultural differences, but the difference in patient approach might be of even greater influence for the patient's emotional response.
We had access to the complete database of all eligible new patients and 70% participated, but selection bias of participants cannot be fully ruled out. Perhaps nervous women were not asked, or maybe women with high distress levels refused to participate. As far as biological patient characteristics are concerned, there were no differences between participants and non-participants, except for a longer duration of subfertility for inductees in the non-participating group, which we cannot explain.
We regret that lifestyle factors such as smoking, weight, and caffeine and alcohol intake were not studied. Although of unarguable influence in IVF treatment and in fertility in general (Sharpe and Franks, 2002
; Klonoff-Cohen, 2005
; Lintsen et al., 2005
), the complexity of research, where lifestyle factors are understood as mediators in the relationship between distress and fertility, requires a different intention of study (Verhaak and Hammer Burns, 2006
).
The emotional impact of an IVF treatment should not be underestimated, but we agree with Boivin et al. (1995) and Verhaak et al. (2007
), that high expectations of the first treatment after adaptation to the subfertility problem after several years, will positively influence the patient's emotional disposition. On the other hand, after unsuccessful IVF treatment, 20% of women showed subclinical forms of anxiety and/or depression (Verhaak et al., 2005
). We therefore do recommend research in the field of prediction (Verhaak et al., 2006
), and of counselling and therapy of women who are susceptible to, or have developed, emotional problems after unsuccessful IVF treatment.
In summary, in our large prospective study on psychological distress and IVF, we did not find an influence of anxiety or depression on the IVF cancellation rates or pregnancy rates. The small confidence intervals in the multivariate analyses implicate accurate findings. The coherence between psychological factors and IVF outcome is probably more complex and cannot be solved without the research of mediating factors such as lifestyle and sexual behaviour. Large prospective studies on psychological and contributory factors are necessary to reveal more information about the interrelationship between emotions and fertility.
| Role of the authors |
|---|
|
|
|---|
D.D.M.B. and C.M.V. had the idea and developed the hypothesis for this manuscript. M.J.C.E. and C.M.V. performed the data management and the statistical analyses; both had substantial contributions to the conception and design, and special contributions came from J.M.J.S. A.M.E.L. did the acquisition of the data and was the main author. All authors critically revised the article.
| Funding |
|---|
|
|
|---|
This study was supported by grant 945-12-013 from ZonMW, The Netherlands Organization for Health Research and Development, The Hague, The Netherlands.
| Acknowledgements |
|---|
|
|
|---|
We would like to thank the participating clinics and their fertility nurses and doctors who contributed to the inclusion of all women in this study: Gelre Ziekenhuis, Apeldoorn, Ziekenhuis Gelderse Vallei, Ede, Medisch Spectrum Twente, Enschede, Universitair Medisch Centrum, Nijmegen, St Elisabeth Ziekenhuis, Tilburg, Máxima Medisch Centrum, Veldhoven and Isala Klinieken, Zwolle.
| References |
|---|
|
|
|---|
Anderheim L, Holter H, Bergh C, Möller A. Does psychological stress affect the outcome of in vitro fertilization? Hum Reprod (2005) 20:2969–2975.
Beck AT, Guth D, Steer RA, Ball R. Screening for major depression disorders in medical inpatients with the Beck Depression Inventory for primary care. Behav Res Ther (1997) 35:785–791.[CrossRef][Web of Science][Medline]
Boivin J, Takefman JE, Tulandi T, Brender W. Reactions to infertility based on extent of treatment failure. Fertil Steril (1995) 63:801–807.[Web of Science][Medline]
Boivin J, Takefman JE. Stress level across stages of in vitro fertilization in subsequently pregnant and nonpregnant women. Fertil Steril (1995) 64:802–810.[Web of Science][Medline]
Boivin J, Schmidt L. Infertility-related stress in men and women predicts treatment outcome 1 year later. Fertil Steril (2005) 83:1745–1752.[CrossRef][Web of Science][Medline]
Campagne DM. Should fertilization treatment start with reducing stress? Hum Reprod (2006) 21:1651–1658.
Demyttenaere K, Nijs P, Evers-Kiebooms G, Koninckx PR. Personality characteristics, psychoendocrinological stress and outcome of IVF depend upon the etiology of infertility. Gynecol Endocrinol (1994) 8:233–240.[Web of Science][Medline]
Demyttenaere K, Bonte L, Gheldof M, Vervaeke M, Meuleman C, Vanderschuerem D, D'Hooghe T. Coping style and depression level influence outcome in in vitro fertilization. Fertil Steril (1998) 69:1026–1033.[CrossRef][Web of Science][Medline]
De Klerk C, Hunfeld JA, Heijnen EM, Eijkemans MJ, Fauser BC, Passchier J, Macklon NS. Low negative affect prior to treatment is associated with a decreased chance of live birth from a first IVF cycle. Hum Reprod (2008) 23:112–116.
Dutch Society for Obstetrics and Gynaecology. NVOG-Guideline no 09. Indication for IVF (1998) www.nvog.nl.
Emery M, Béran MD, Darwiche J, Oppizzi L, Joris V, Capel R, Guex P, Germond M. Results from a prospective, randomized, controlled study evaluating the acceptability and effects of routine pre-IVF counselling. Hum Reprod (2003) 18:2647–2653.
Eugster A, Vingerhoets AJ. Psychological aspects of in vitro fertilization: a review. Soc Sci Med (1999) 48:575–589.[CrossRef][Web of Science][Medline]
Eugster A, Vingerhoets AJ, van Heck GL, Merkus JM. The effect of episodic anxiety on an in vitro fertilization and intracytoplasmic sperm injection treatment outcome: a pilot study. J Psychosom Obstet Gynaecol (2004) 25:57–65.[CrossRef][Medline]
Facchinetti F, Matteo ML, Artini GP, Volpe A, Genazzani AR. An increased vulnerability to stress is associated with a poor outcome of in vitro fertilization-embryo transfer treatment. Fertil Steril (1997) 67:309–314.[CrossRef][Web of Science][Medline]
Gallinelli A, Roncaglia R, Matteo ML, Ciacco I, Volpe A, Facchinetti F. Immunological changes and stress are associated with different implantation rates in patients undergoing in vitro fertilization-embryo transfer. Fertil Steril (2001) 76:85–91.[CrossRef][Web of Science][Medline]
Huiskes CJ, Kraaimaat FW, Bijlsma JW. Development of a self-report questionnaire to assess the impact of rheumatic diseases on health and lifestyle. J Rehabil Sci (1990) a. 65–70.
Huiskes CJ, Kraaimaat FW, Bijlsma JW. Handleiding bij de zelfbeoordelingslijst Invloed van Reuma op Gezondheid en Leefwijze: De IRGL [Manual to the self-report questionnaire Impact of Rheumatic diseases on General health and Lifestyle: The IRGL] (1990) b. Lisse: Swets & Zeitlinger BV.
Klonoff-Cohen H. Female and male lifestyle habits and IVF: what is known and unknown. Hum Reprod Update (2005) 11:180–204.
Klonoff-Cohen H, Chu E, Natarajan L, Sieber W. A prospective study of stress among women undergoing in vitro fertilization or gamete intrafallopian transfer. Fertil Steril (2001) 76:675–687.[CrossRef][Web of Science][Medline]
Lintsen AM, Pasker-de Jong PC, de Boer EJ, Burger CW, Jansen CA, Braat DD, van Leeuwen FE. Effects of subfertility cause, smoking and body weight on the success rate of IVF. Hum Reprod (2005) 20:1867–1875.
Lintsen AM, Eijkemans MJ, Hunault CC, Bouwmans CA, Hakkaart L, Habbema JD, Braat DD. Predicting ongoing pregnancy chances after IVF and ICSI: a national prospective study. Hum Reprod (2007) 22:2455–2462.
Lovely LP, Meyer WR, Ekstrom RD, Golden RN. Effect of stress on pregnancy outcome among women undergoing assisted reproduction procedures. South Med J (2003) 96:548–551.[Web of Science][Medline]
Merari D, Feldberg D, Elizur A, Goldman J, Modan B. Psychological and hormonal changes in the course of in vitro fertilization. J Assist Reprod Genet (1992) 161–169.
Sharpe RM, Franks S. Environment, lifestyle and infertility—an inter-generational issue. Nat Cell Biol (2002) 4:s33–s40.[Web of Science][Medline]
Smeenk JM, Verhaak CM, Eugster A, van Minnen A, Zielhuis GA, Braat DD. The effect of anxiety and depression on the outcome of in-vitro fertilization. Hum Reprod (2001) 16:1420–1423.
Smeenk JM, Verhaak CM, Stolwijk AM, Kremer JA, Braat DD. Reasons for dropout in an in vitro fertilization/intracytoplasmic sperm injection program. Fertil Steril (2004) 81:262–268.[CrossRef][Web of Science][Medline]
Smeenk JM, Verhaak CM, Vingerhoets AJ, Sweep CG, Merkus JM, Willemsen SJ, van Minnen A, Straatman H, Braat DD. Stress and outcome success in IVF: the role of self-reports and endocrine variables. Hum Reprod (2005) 20:991–996.
Spielberger CD. Manual for the State-trait Anxiety Scale (1983) Palo Alto, CA: Consulting Psychologists Press.
Stolwijk AM, Zielhuis GA, Hamilton CJ, Straatman H, Hollanders JM, Goverde HJ, van Dop PA, Verbeek AL. Prognostic models for the probability of achieving an ongoing pregnancy after in-vitro fertilization and the importance of testing their predictive value. Hum Reprod (1996) 11:2298–2303.
Templeton A, Morris JK, Parslow W. Factors that affect the outcome of in-vitro fertilisation treatment. Lancet (1996) 348:1402–1406.[CrossRef][Web of Science][Medline]
Thiering P, Beaurepaire J, Jones M, Saunders D, Tennant C. Mood state as a predictor of treatment outcome after in vitro fertilization/embryo transfer technology (IVF/ET). J. Psychosom Res (1993) 37:481–491.[CrossRef][Web of Science][Medline]
Van der Ploeg HM, Defares PB, Spielberger CD. Handleiding bij de Zelfbeoordelingsvragenlijst: een Nederlandse bewerking van de Spielberger State Trait Anxiety Inventory (2000) Lisse: Swets & Zeitlinger.
Verhaak C, Hammer Burns L. Behavioral medicine approaches to infertility counseling. In: Infertility Counseling, A Comprehensive Handbook for Clinicians—Convington SN, Hammer Burns L, eds. (2006) Cambridge University Press. 169–195.
Verhaak CM, Smeenk JM, Eugster A, van Minnen A, Kremer JA, Kraaimaat FW. Stress and marital satisfaction among women before and after their first cycle of in vitro fertilization and intracytoplasmic sperm injection. Fertil Steril (2001) 525–531.
Verhaak CM, Smeenk JM, van Minnen A, Kremer JA, Kraaimaat FW. A longitudinal, prospective study on emotional adjustment before, during and after consecutive fertility treatment cycles. Hum Reprod (2005) 20:2253–2260.
Verhaak CM, Lintsen BM, Kraaimaat FW, Kremer JA, Braat DD. Who is at risk of developing emotional problems after in vitro fertilization (IVF): pre treatment identification of risk groups. (2006) ASRM 62nd Annual Meeting. Abstract O-6.
Verhaak CM, Smeenk JM, Evers AW, Kremer JA, Kraaimaat FW, Braat DD. Women's emotional adjustment to IVF: a systematic review of 25 years of research. Hum Reprod Update (2007) 13:27–36.
Submitted on October 31, 2008; resubmitted on December 8, 2008; accepted on December 10, 2008.
![]()
CiteULike
Connotea
Del.icio.us What's this?
Related articles in Hum. Reprod.:
- Editor's Choice
- André Van Steirteghem
Hum. Reprod. 2009 24: 1007.[Extract] [FREE Full Text]
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
