A postal survey of embryo transfer practice in the UK

Osama H. Salha, Victoria K. Lamb and Adam H. Balen,1

Department of Reproductive Medicine, Clarendon Wing, Leeds General Infirmary, Leeds, UK


    Abstract
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix I. Questionnaire used...
 References
 
In this postal survey a questionnaire was sent to all unit directors in the UK to determine their attitudes to the factors influencing embryo transfer practice. They were requested to rate each step on a scale of 1-10, where 1 was irrelevant and 10 very important. A total of 80 practitioners from 40 units replied. Over 50% of the corresponding practitioners were consultants, 33% were middle-grade clinicians, and 12% were infertility nurse specialists. The factor that got the highest rating was the need for a standardized protocol for all unit staff regarding embryo transfer technique. The second critical factor voted by the respondents was the presence of blood on the embryo transfer catheter. Not touching the uterine fundus was deemed to be the third most important factor while the type of embryo transfer catheter used was a very close fourth. Prolonged bed rest following embryo transfer was voted the least important factor to influence the outcome. The wide variations in practice and choice of catheters encountered in this survey are indications of the divided opinion and lack of concrete evidence on which to base any firm decisions. The need for large clinical studies to assess clearly whether higher pregnancy rates will result from modifications in embryo transfer practice is highlighted.

Key words: catheter/embryo transfer technique/implantation rates


    Introduction
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix I. Questionnaire used...
 References
 
Embryo transfer is the last and probably least successful step in the IVF treatment cascade. The technique of embryo transfer remains largely unchanged since it was first described. Yet it is well documented that, even with excellent quality embryos, optimal pregnancy rates still may not be achieved if the embryo transfer technique is defective. Currently there are no markers by which to evaluate implantation. After embryo transfer, physicians and embryologists lose control of the cleaving embryos and wait helplessly for the forthcoming `pregnancy test'. One wonders whether all the embryos reach the endometrial cavity and whether each of them has the same chance of implantation. Various groups have presented their techniques (Craft et al., 1981Go; Kerin et al., 1981Go; Leeton et al., 1982Go; Edwards et al., 1984Go), but few IVF programmes have specifically examined variants in embryo transfer technique that may improve implantation. Most programmes have relied on `feel' by the clinician placing the transfer catheter and embryos within the uterine cavity at a point `near' the fundus.

Kovacs (1999) recently polled 50 Australian and New Zealand IVF clinicians regarding the important factors for successful embryo transfer after IVF. This survey was repeated, with his permission and a few modifications, to gauge the opinion of IVF practitioners in the UK.


    Materials and methods
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix I. Questionnaire used...
 References
 
A questionnaire was devised based on a number of possible factors which make up the `embryo transfer matrix' (Appendix I). The director of each IVF unit in the UK was sent a questionnaire to circulate to practitioners within their clinic to determine their attitudes with respect to the factors that influence embryo transfer practice. They were requested to rate each parameter on a scale of 1 to 10, where 1 was least important and 10 was very important. Each parameter therefore had a possible maximum score of 10 multiplied by the number of respondents. The total score for each parameter was calculated as a percentage of the maximum score. The mean score ± SD was also calculated for each variable.


    Results
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix I. Questionnaire used...
 References
 
The questionnaire was sent to all registered assisted conception units in England, Wales, Scotland, and Northern Ireland. A total of 80 practitioners from 40 centres replied, giving a possible maximum score of 800 for each parameter. The mean number of IVF/intracytoplasmic sperm injection (ICSI) cycles performed in the above units was 467.5 ± 112 (range 70–1500 cycles/year). The cumulative experience of the 80 practitioners who completed the questionnaire was >480 years of `hands on' IVF-embryo transfer (mean 6.1 years, range 1–17 years). Over 50% of the corresponding practitioners were consultants, 33% were middle-grade clinicians, and 12% were infertility nurse specialists.

The results of the survey are summarized in Table IGo. The factor that got the highest rating was the need for a standardized protocol for all unit staff regarding embryo transfer policy (mean score 8.5 ± 1.8, total score 85%). The second critical factor voted by the respondents was the presence of blood on the embryo transfer catheter at the end of the embryo transfer process (mean score 7.5 ± 2.6, total score 75%). Not touching the uterine fundus was deemed to be the third most important factor (mean 7.2 ± 2.7, total score 72%) while the type of catheter used in the embryo transfer was a close fourth (mean 7.2 ± 2.5, total score 71%).


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Table I. The relative importance of each factor as rated by the total, means score and SD. The maximum possible score for each variable is 800
 
The different types of embryo transfer catheters used by the 40 surveyed units are summarized in Table IIGo. The most popular catheter used by respondents was that manufactured by Wallace (72% of units used a Wallace with or without a stylet). The second and third most used catheters were the Frydman and Rocket used by 40 and 30% of the units respectively. In an easy transfer 45% of the units used a Wallace catheter without a stylet, but when the embryo transfer was judged to be difficult there was no clear favourite (25% used Wallace, 20% used a Frydman, 17.5% had no preference and 15% used a Cook). A stylet with a soft embryo transfer catheter was mainly used when the transfer was anticipated to be difficult. Of significance is that 18% of units had no preferred catheter to use in difficult transfers.


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Table II. The different types of embryo transfer catheters used by the 40 surveyed units
 

    Discussion
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix I. Questionnaire used...
 References
 
Embryo transfer, while critical to the IVF process, has been relatively underrated by most programmes in terms of evaluating changes that might improve clinical pregnancy rates. Most programmes still rely on clinical touch in positioning the transfer catheter in the upper part of the uterine cavity. Various facets of embryo transfer may be pivotal in improving implantation and clinical pregnancy rates: catheter position in the uterine cavity, choice of catheter, volume of transfer medium, retention of the fluid droplet and endometrial receptivity.

Having a unified protocol for all unit staff to follow was voted the most important factor that might influence the chance of success following embryo transfer in the survey. Variations in embryo transfer practice within the same unit were highlighted by Naaktgeboren et al. (1997) in a retrospective study of their IVF clinic results. Over 11 years they found that their pregnancy rate per embryo transfer varied by a factor of two, while results per clinician varied between 12 and 30%. After extensive evaluation of the different practices used by the various clinicians and unification of their policy, they reached their best ever pregnancy rate per embryo transfer of 37%.

The presence of blood and its position on the embryo transfer catheter may have an effect on embryo implantation. Blood found on the outside of the transfer catheter was associated with a six to seven-fold decrease in the rates of embryo implantation and clinical pregnancy per transfer, with the greatest amount of blood accompanied by the lowest chance of pregnancy (Goudas et al., 1998Go). These observations are consistent with previous in-vitro studies indicating that only blood reduces the rate of oocyte fertilization and embryo cleavage (Daya et al., 1990Go). They are also in agreement with reports suggesting that bleeding and cervical trauma at the time of embryo transfer diminish the embryo implantation rate (Englert et al., 1986Go; Wisanto et al., 1989Go).

As illustrated in Table IIGo, the most popular embryo transfer catheter used by the 40 units surveyed was that manufactured by Wallace (Simcare Manufacturing Ltd, Colchester, Sussex, UK), with or without the stylet (72%). The second most used catheter was the Frydman (Euro Surgical Ltd, Guilford, Surrey, UK) used by 40% of units while the Rocket (Embryon Rocket Medical PLC, Watford, UK) was third used by 30%. In an easy transfer 45% of the units used a Wallace catheter without a stylet. When the embryo transfer was deemed to be difficult, 25% of corresponding units still used a Wallace catheter (with or without a stylet) while a further 20% used a Frydman (with or without a stylet). An additional 15% used the harder Cook and 10% of units used Rocket catheters. It is surprising that only 18% of units had no nominated catheter to use in difficult embryo transfers.

The type of transfer catheter has been addressed in a number of studies. Significantly better pregnancy rates were obtained with a Frydman catheter compared with transfers performed with the Tom Cat catheter (Sherwood Medical, St Louis, MO, USA) (29 versus 16%) (Gonen et al., 1991Go). Wisanto et al. (1989) had previously compared the performance of Frydman catheters with the hard Tom Cat catheters and encountered more difficult transfers with the Frydman, but reported enhanced pregnancy rates when the Frydman catheter was used. A soft Wallace catheter also yielded significantly higher pregnancy rates over the Tom Cat catheter when compared with another study (Rosenlund et al., 1996Go). In addition, in this study soft Wallace catheters with complete aspiration of cervical mucus significantly reduced expulsion of methylene blue dye compared with transfers performed with stiffer Craft catheters. The authors therefore advocated complete aspiration of cervical mucus in order to reduce embryo expulsion rate.

The use of a Tom Cat catheter, without an introducing cannula, was found to be simple, painless and atraumatic to the cervical canal and the uterine cavity (Kerin et al., 1981Go). However, the use of an introducing cannula was felt to be advantageous for negotiating anatomical difficulties and preventing the entry of cervical mucus into the endometrial cavity (Craft et al., 1981Go). Edwards et al. (1984) first used Wallace catheters and described them as `flexible and enclosed in a moveable outer sleeve to give support if needed' for embryo transfer. Other researchers (E.G.Wood et al., 2000) achieved a significantly better clinical pregnancy rate per transfer using a soft (Wallace or Frydman) rather than a hard (Tom Cat or Tef Cat) catheter (36 versus 17% respectively). In addition, no significant difference was found (E.G.Wood et al., 2000) in clinical pregnancy rates between the two soft catheters, Frydman or Wallace, which was similar to previous findings (Al-Shawaf et al., 1993Go). The soft catheter may possibly be less irritating to the endometrium and induce fewer myometrial contractions, thus decreasing the expulsion rate of the transferred embryos. This might have been a key factor with regard to the increased pregnancy rate noted with soft catheters by E.G.Wood et al. (2000).

Another approach to embryo transfer is to perform a dummy embryo transfer prior to the IVF cycle in order to select the best catheter for the procedure. Randomized 335 IVF patients were allocated to either group A (n = 167) where a dummy embryo transfer was performed before the start of the IVF treatment cycle or group B (n = 168) where no dummy embryo transfer was performed (Mansour et al., 1994Go). Group B was further randomized to use either a soft Wallace catheter or a stiffer Craft catheter. The pregnancy rate was significantly higher in the dummy embryo transfer group (22.8 versus 13.1%). Furthermore, the number of difficult transfers was greatly reduced in the dummy transfer group (0 versus 29.8%). In the current survey the respondents ranked the need for a dummy embryo transfer before actual embryo transfer 12th and a dummy embryo transfer before the start of treatment 13th. The performance of a mock embryo transfer early in the treatment cycle was a low priority ranked 18th out of the 20 variables.

The impact of difficult embryo transfer on clinical pregnancy rates is a subject of debate in the literature. Some studies have shown that there is a correlation between difficult embryo transfer and reduced pregnancy rates (Leeton et al., 1982Go; Visser et al., 1993Go), whereas other studies have suggested that difficult or repeated embryo transfer does not adversely affect outcome (Tur-Kaspa et al., 1998Go). These contradictory findings may be explained in several ways. Most series of patients studied have been relatively small. Comparisons between studies are difficult to make because different definitions of difficult embryo transfer, which is a subjective diagnosis, have been used and patient selection has not been uniform. It seems reasonable, however, to believe that difficult embryo transfer may be associated with several factors that may play a role in inhibiting implantation. Bleeding, which almost always results from difficult embryo transfer, permits blood cells to coat the embryos and prevent their contact with endometrium (Goudas et al., 1998Go). The release of prostaglandins may cause uterine contractions, and this may result in expulsion of the embryos into the cervical canal or Fallopian tubes. Finally, repeated attempts at embryo transfer increase the risk of introduction of micro-organisms into the sterile environment of the uterine cavity.

The factor that got the highest votes (Kovacs, 1999Go) in a survey of Australian and New Zealand clinicians was the need to remove hydrosalpinges before embarking on IVF treatment. Although the presence of hydrosalpinges was found to have a negative influence on embryo implantation (Nackley and Muasher, 1998Go; Zeynelogu et al., 1998Go; Camus et al., 1999Go) due to possible harmful effects on endometrial receptivity, the UK clinicians ranked this only seventh in this survey. This highlights the wide divergence of opinion which seems to dominate the management of tubal pathology in terms of embryo implantation (Puttemans et al., 2000Go; Strandell and Lindhard, 2000Go) despite the recent publication of the largest prospective, randomized study which demonstrated the benefit of salpingectomy for ultrasonically diagnosed hydrosalpinges (Strandell et al., 1999Go).

Not touching the uterine fundus was ranked third in this survey and fourth in the Australian questionnaire. Avoiding the use of a tenaculum at the time of embryo transfer and removal of cervical mucus were rated the fifth and sixth most important factors on the clinicians' priority in this survey and that of Kovacs (Kovacs, 1999Go). Reviewing the literature, no data were found that examine the potential influence of touching the endometrium with the embryo transfer catheter. The use of a tenaculum, on the other hand, is usually associated with a degree of difficulty in performing the embryo transfer. The removal of healthy cervical mucus prior to the embryo transfer is another issue that is still open to debate. There is little concrete evidence on which to base any firm decisions regarding whether the cervical mucus should be removed, and if so, how to remove it. Preliminary data suggest that flushing of the cervical canal with embryo culture medium using a tuberculin syringe is associated with an improvement in clinical pregnancy rates (Sallam et al., 2000Go).

The rationale for ultrasound-guided embryo transfer includes real-time tracking of the catheter tip, a less traumatic transfer, and more predictable embryo placement. The possible use of ultrasound guidance to facilitate embryo transfer was first reported (Strickler et al., 1985Go). A total of 16 transfers guided by ultrasound and 12 performed by clinical `feel' were compared. They reported that ultrasound-guided transfers were easier with less catheter distortion. Moreover, the retention of the fluid bubble containing the embryos was found to be reassuring to the patients, lessening anxiety that the embryos might be displaced. Similar conclusions were reached (Leong et al., 1986Go). A subsequent study (Hurley et al., 1991Go) investigated the use of transvaginal guidance in embryo transfer, but did not identify a significant difference between this and the usual clinical touch method. However, it must be taken into account that the ultrasound guidance was only used after insertion of the catheter. Similarly, in a prospective study using abdominal ultrasound, (Al-Shawaf et al., 1993Go) it was found that there was no significant effect on treatment outcome. More recently (Woolcott and Stanger, 1998Go) it was confirmed that the `embryo bubble', as visualized by transvaginal ultrasound, remained on standing in all patients after embryo transfer, again providing reassurance to clinicians and patients. The adjuvant use of ultrasound guidance was evaluated in 61 transfers compared with 71 blind transfers and reported significantly higher pregnancy rates in the echo-guided cases (36.6 versus 22.6%) (Prapas et al., 1995Go). Few groups describe routine use of ultrasound, transvaginal or transabdominal, as a part of their embryo transfer protocol (Leong et al., 1986Go; Rosenlund et al., 1996Go; Sieck et al., 1997Go). Others have used ultrasound only in difficult cases or during transvaginal-transmyometrial transfers (Kato et al., 1993Go; Sharif et al., 1996Go), or transvesical embryo transfers (Parsons et al., 1987Go).

The only two large prospective studies comparing standard and ultrasound-guided embryo transfer presented conflicting outcomes. Ultrasound-guided and clinical touch embryo transfers were compared in 187 patients that were randomly allocated to either group (Kan et al., 1999Go). There was a non-significant trend towards higher pregnancy rates with ultrasound guidance in the whole group (37.8 versus 28.9%) and in subsets of older women (38.1 versus 20.4%). On the other hand, a large prospective randomized study compared 182 patients who had an ultrasound-guided embryo transfer with 180 patients who had a clinical touch embryo transfer (Coroleu et al., 2000Go). There were no significant differences between the two groups in terms of age, cause of infertility or in the characteristics of the IVF cycle. The pregnancy rate, however, was significantly higher among the ultrasound-guided group (50%) compared with the clinical touch group (33.7%). Furthermore, there was also a significant improvement in the implantation rate: 25.3% in the ultrasound group compared with 18.1% in the clinical touch group.

A new coaxial catheter system with an echodense tip for ultrasonographically guided embryo transfer was recently described (Letterie et al., 1999Go). In this preliminary, non-comparative study the echodense tip was immediately imaged by transabdominal techniques, thus reducing the need to move either the catheter or ultrasound transducer to facilitate identification. The use of this coaxial catheter system may provide less traumatic and more precise embryo placement. Conventional catheter systems frequently require some to-and-fro motion of the inner catheter sheath for adequate identification during sonographic monitoring, potentially disrupting the endometrium. The immediate identification of the catheter tip eliminates this aspect and may provide a method for precise, gentle embryo transfer. Larger studies are required, however, to assess whether higher pregnancy rates will result.

Historically bed rest following embryo transfer has been advised, ranging from 15 min to 24 h. A long period of bed rest is a precautionary measure to try to improve the implantation rate. However, this has never been shown to be related to a higher success rate and its importance in IVF is still controversial. A study of 103 IVF procedures with no bed rest following embryo transfer was reported (Sharif et al., 1995Go). The authors concluded that their positive results strongly supported the hypothesis that bed rest is unnecessary to improve the chance of conception and suggested that women, a few minutes after embryo transfer, can stand, empty their bladder, and return home with no apparent risk to the process of implantation. Similarly no restriction of the patients' routine activity need be advised after the transfer (Botta and Grudzinskas, 1997Go).

In a prospective randomized trial of 575 patients who had an embryo transfer with or without a full bladder, it was found that the number of patients requiring either transfer with stylet or cervical traction with a vulsellum was significantly greater with an empty bladder (S.Wood et al., 2000). The presence of a full bladder was found to facilitate easier transfer of embryos with significantly higher pregnancy rates.

In conclusion, it is still an enigma why embryo transfer remains the most inefficient step. Various facets of the embryo transfer practice may be pivotal in improving implantation and pregnancy rates. The need for a standardized protocol followed by all units' staff was voted the most important factor in this survey. We believe that such a protocol should cover the following factors: personnel qualified to perform embryo transfer and duration of training required; position of patient; full or empty bladder; the use of transabdominal/vaginal ultrasound scanning before, during or after transfer; the performance of `mock/dummy' transfer with empty catheter immediately before `real' transfer; preparation of cervix and the need to remove cervical mucus; loading of embryos, the amount of culture medium and air bolus within the catheter; type of embryo transfer catheter used for mock transfer and difficult cases; technique of embryo transfer, and the possible use of tenaculum; placement of embryos within the cavity, to use the `clinical touch' or ultrasound guidance; the duration embryo transfer catheter is left in cavity; the need for bed rest versus mobilization following embryo transfer; recommendations for subsequent embryo transfer in cases of previous difficult embryo transfer.

The absence of bleeding at the time of the transfer and not touching the uterine fundus were rated the second and third most important factors. Nonetheless, the wide variations in practice and choice of catheters encountered are indications of the divided opinion and lack of concrete evidence on which to base any firm decisions.


    Appendix I. Questionnaire used to gauge the opinion of IVF clinicians in the UK
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix I. Questionnaire used...
 References
 
Clinic:

Position:Consultant/Staff Grade/Clinical Assistant/Sub-Specialist Senior Registrar/Specialist

Registrar/Research Fellow: Nurse: Grade:

Number of years performing embryo transfers:

Size of Number of fresh cycles/year:

clinic: Number of practitioners performing embryo transfers:

How many embryo transfers do you perform in an average week?

Please rate the following factors with a score 1–10, with 1 indicating little importance and 10 indicating great importance:


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    Notes
 
1 To whom correspondence should be addressed at: Department of Reproductive Medicine, Clarendon Wing, Leeds General Infirmary, Leeds LS2 9NS, UK. E-mail: abalen{at}ulth.northy.nhs.uk Back


    References
 Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 Appendix I. Questionnaire used...
 References
 
Al-Shawaf, T., Dave, R., Harper, J. et al. (1993) Transfer of embryos into the uterus: how much do technical factors affect pregnancy rates? J. In Vitro Fertil. Embryo Transfer, 10, 31–36.

Botta, G. and Grudzinskas, G. (1997) Is prolonged bed rest following embryo transfer useful? Hum. Reprod., 12, 2489–1492.[Abstract]

Camus, E., Poncelet, C., Goffinet, F. et al. (1999) Pregnancy rates after IVF in cases of tubal infertility with and without hydrosalpinx: meta-analysis of published comparative studies. Hum. Reprod., 14, 1243–1249.[Abstract/Free Full Text]

Coroleu, B., Carreras, O., Veiga, A. et al. (2000) Embryo transfer under ultrasound guidance improves pregnancy rates after in-vitro fertilization. Hum. Reprod., 15, 616–620.[Abstract/Free Full Text]

Craft, I., McLeod, F. and Edmonds, K. (1981) Human embryo transfer technique. Lancet, ii, 1104–1105.

Daya, S., Kohut, J., Gunby, J. and Younglai, E. (1990) Influence of blood clots in the cumulus complex on oocyte fertilization and cleavage. Hum. Reprod., 5, 744–746.[Abstract]

Edwards, R.G., Fishel, S.B., Cohen, J. et al. (1984) Factors influencing the success of in vitro fertilisation for alleviating human infertility. J. In Vitro Fertil. Embryo Transfer, 1, 3–23.[Medline]

Englert, Y., Puissant, F., Camus, M. et al. (1986) Clinical study on embryo transfer after human in vitro fertilisation. J. In Vitro Fertil. Embryo Transfer, 3, 243–246.[Medline]

Gonen, Y., Dirnfeld, M., Goldman, S. et al. (1991) Does the choice of catheter for embryo transfer influence the success rate of in-vitro fertilisation? Hum. Reprod., 6, 1092–1094.[Abstract]

Goudas, V., Hammitt, D., Damario, M. et al. (1998) Blood on the embryo transfer catheter is associated with decreased rates of embryo implantation and clinical pregnancy with the use of in vitro fertilisation-embryo transfer. Fertil. Steril., 70, 878–882.[ISI][Medline]

Hurley, V.A., Osborn, J.C., Leoni, M.A. et al. (1991) Ultrasound-guided embryo transfer: a controlled trial. Fertil. Steril., 55, 559–562.[ISI][Medline]

Kan, A.K.S., Abdalla, H.I., Gafar, A.H. et al. (1999) Embryo transfer: ultrasound-guided versus clinical touch. Hum. Reprod., 14, 1259–1261.[Abstract/Free Full Text]

Kato, O., Takatsuka, R. and Asch, R. (1993) Transvaginal-transmyometrial embryo transfer: the Towako method; experience of 104 cases. Fertil. Steril., 59, 51–53.[ISI][Medline]

Kerin, J.F.P., Jeffrey, R., Warnes, G.M. et al. (1981) A simple technique for human embryo transfer into the uterus. Lancet, 10, 726–727.

Kovacs, G.T. (1999) What factors are important for successful embryo transfer after in-vitro fertilisation? Hum. Reprod., 14, 590–592.[Free Full Text]

Leeton, J., Trounson, A., Jessup, D. et al. (1982) The technique for human embryo transfer. Fertil. Steril., 38, 156–161.[ISI][Medline]

Leong, M., Leung, C., Tucker, M. et al. (1986) Ultrasound-assisted embryo transfer. J. In Vitro Fertil. Embryo Transfer, 3, 183–185.

Letterie, G.S., Marshall, L. and Angle, M. (1999) A new coaxial catheter system with an echodense tip for ultrasonographically guided embryo transfer. Fertil. Steril., 72, 266–268.[ISI][Medline]

Mansour, R.T., Aboulghar, M.A., Serour, G.I. et al. (1994) Dummy embryo transfer using methylene blue dye. Hum. Reprod., 9, 1257–1259.[Abstract]

Naaktgeboren, N., Broers, F.C., Heijnsbroek, I. et al. (1997) Hard to believe, hardly discussed, nevertheless very important for the IVF/ICSI results: embryo transfer technique can double or halve the pregnancy rate. Hum. Reprod., 12 (Suppl.), 149.

Nackley, A.C. and Muasher, S.J. (1998) The significance of hydrosalpinx in in vitro fertilisation. Fertil. Steril., 69, 373–384.[ISI][Medline]

Parsons, J.H., Bolton, V.N., Wilson, L. et al. (1987) Pregnancies following in vitro fertilisation and ultrasound-directed surgical embryo transfer by perurethral and transvaginal techniques. Fertil. Steril., 48, 691–693.[ISI][Medline]

Prapas Y., Prapas, N., Hatziparasidou, A. et al. (1995) The echoguide embryo transfer maximises the IVF results. Acta Eur. Fertil., 26, 113–115.[Medline]

Puttemans, P., Campo, R., Gordts, S. and Brosens, I. (2000) Hydrosalpinx and ART: hydrosalpinx|functional surgery or salpingectomy. Hum. Reprod., 15, 1427–1430.[Abstract/Free Full Text]

Rosenlund, B., Sjöblom, P. and Hillensjo, T. (1996) Pregnancy outcome related to the site of embryo deposition in the uterus. J. Assist. Reprod. Genet., 13, 511–513.[ISI][Medline]

Royal College of Obstetricians and Gynaecologists (2000) The Management of Infertility in Tertiary Care, Evidence-based Clinical Guideline No. 6. RCOG Press, London.

Sallam, H.N., Farrag, F., Ezzeldin, A. et al. (2000) Vigorous flushing of the cervical canal prior to embryo transfer | a prospective randomised study. Fertil. Steril., 74 (Suppl.), S203.

Sharif, K., Afnan, M. and Lenton, W. (1995) Mock embryo transfer with a full bladder immediately before the real transfer for in vitro fertilisation treatment: the Birmingham experience with 113 cases. Hum. Reprod., 10, 1715–1718.[Abstract]

Sharif, K., Bilalis, D., Afnan, M. et al. (1996) Transmyometrial embryo transfer after difficult immediate mock transcervical transfer. Fertil. Steril., 65, 1071–1074.[ISI][Medline]

Sieck, U.V., Hollanders, J.M.G., Jaroudi, K.A. et al. (1997) Cervical pregnancy following ultrasound-guided embryo transfer. Methotrexate treatment in spite of high ß HCG levels. Hum. Reprod., 12, 1114–1117.[Free Full Text]

Strandell, A., Lindhard, A., Waldenström, U. et al. (1999) Hydrosalpinx and IVF outcome: a prospective, randomised multicentre trial in Scandinavia on salpingectomy prior to IVF. Hum. Reprod., 14, 2762–2769.[Abstract/Free Full Text]

Strandell, A. and Lindhard, A. (2000) Salpingectomy prior to IVF can be recommended to a well-defined subgroup of patients. Hum. Reprod., 15, 2072–2074.[Abstract/Free Full Text]

Strickler, R.C., Christianson, C., Crane, J.P. et al. (1985) Ultrasound guidance for human embryo transfer. Fertil. Steril., 43, 54–61.[ISI][Medline]

Tur-Kaspa, I., Yuval, Y., Bider, D. et al. (1998) Difficult or repeated embryo transfers do not adversely affect in vitro fertilisation pregnancy rates or outcome. Hum. Reprod., 13, 2452–2455.[Abstract]

Visser, D.S., Fourie, F., Le, R. and Kruger, H.F. (1993) Multiple attempts at embryo transfer: effect on pregnancy outcome in an in vitro fertilisation and embryo transfer program. J. Assist. Reprod. Genet., 10, 37–43.[ISI][Medline]

Wisanto, A., Camus, M., Janssens, R. et al. (1989) Performance of different embryo transfer catheters in a human in vitro fertilisation program. Fertil. Steril., 52, 79–84.[ISI][Medline]

Wood, E.G., Batzer, F.R., Go, K.J. et al. (2000) Ultrasound-guided soft catheter embryo transfers will improve pregnancy rates in in-vitro fertilisation. Hum. Reprod., 15, 107–112.[Abstract/Free Full Text]

Wood S., Thomas K., Stephton V. et al. (2000) The effect of bladder distension on embryo transfer in assisted conception cycles. J. Reprod. Fertil., 1 (Suppl.), P50.

Woolcott, R. and Stanger, J. (1998) Ultrasound tracking of the movement of embryo-associated are bubbles on standing after transfer. Hum. Reprod., 13, 2107–2109.[Abstract]

Zeynelogu, H.B., Arici, A. and Olive, D.I. (1998) Adverse effects of hydrosalpinx on pregnancy rates after in vitro fertilisation-embryo transfer. Fertil. Steril., 70, 492–499.[ISI][Medline]

Submitted on September 15, 2000; accepted on January 15, 2001.