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Diagnostic accuracy of ultrasound features for tubal ectopic pregnancy
Evidence review A
NICE Guideline, No. 126
National Guideline Alliance (UK).
1. Diagnostic accuracy of ultrasound features for tubal ectopic pregnancy
Review question
What ultrasound features are most diagnostic of a tubal ectopic pregnancy?
Introduction
Ectopic pregnancy remains the leading cause of maternal mortality in early pregnancy in the UK and early diagnosis is important to reduce this risk. Early diagnosis may also allow non-surgical treatment options, including expectant or medical management. The diagnosis of ectopic pregnancy is made using a combination of the clinical presentation, serum human chorionic gonadotrophin (hCG) levels and pelvic ultrasound scan findings.
Ultrasound features of ectopic pregnancy can vary widely between different individuals, and depend on a variety of factors, including the gestation of the pregnancy, experience of the sonographer, route of scanning (transabdominal or transvaginal) as well as features of the scan equipment. The aim of this review was to identify ultrasound scan features which have high diagnostic accuracy for the identification of ectopic pregnancy.
Summary of the protocol
Please see Table 1 for a summary of the Population, Index test, Reference test, and Outcome (PIRO) characteristics of this review.
Table 1
Summary of the protocol (PIRO table).
For full details see the review protocol in appendix A.
Methods and process
This evidence review was developed using the methods and process described in Developing NICE guidelines: the manual 2014. Please see the methods section of the 2012 guideline for further details.
Methods specific to this review question are described in the review protocol in appendix A.
The use of GRADE for reviews of diagnostic test accuracy has recently been adopted by NICE, and this methodology was applied to the review. Cross-sectional diagnostic test accuracy studies were initially rated as high quality, and the rating was amended according to the risk of bias (as assessed using the QUADAS-2 checklist) inconsistency, imprecision, indirectness and other factors, in a manner analogous to intervention reviews. Imprecision was assessed according to pre-specified thresholds for sensitivity and specificity, which were identified by the guideline committee as representing clinically meaningful results. In determining these thresholds, the committee recognised that the identification of ectopic pregnancy often requires an assessment of a combination of features (including the woman’s symptoms and hCG levels as well as ultrasound findings). Therefore they agreed a threshold of ≥75% for sensitivity and ≥80% for specificity would represent a very useful test. The lower threshold (representing a not useful test) was set at <50%.
Declarations of interest were recorded according to NICE’s 2018 conflicts of interest policy (see Register of Interests).
Clinical evidence
Included studies
Ten cohort studies were included in this review (4 prospective cohorts: Dart 2002, Malek-Mellouli 2013, Moore 2007, Sadek 1995; 6 retrospective cohorts: Ahmed 2004, Barnhart 2011, Dart 1998, Hammoud 2005, Mehta 1999, Nadim 2018).
All studies examined features seen using transvaginal ultrasonography (TVUS), and two studies additionally used transabdominal ultrasonography (TAS) (Hammoud 2005, Moore 2007).
Studies were conducted in three distinct populations of women and so the results have been analysed for these separate sub-populations:
- three studies included any women with bleeding and/or pain during the first trimester, who were referred for ultrasound (sub-population 1, all symptomatic women: Barnhart 2011, Moore 2007, Sadek 1995).
- two studies included only women with a suspected ectopic pregnancy or pregnancy of unknown location (PUL), where women with confirmed intrauterine pregnancies (IUP) were excluded from the analysis (sub-population 2, IUPs excluded: Hammoud 2005, Mehta 1999).
- five studies included women with PULs, where women with definite ectopic pregnancies and IUPs were excluded (sub-population 3, IUP and EP excluded, Ahmed 2004, Dart 1998, Dart 2002, Malek-Mellouli 2013, Nadim 2018).
Terminology used to define findings seen on the ultrasound varied across studies, and did not align precisely with terms used in the protocol. Consequently, the description given within each study was used to group like with like, and the wording in this review has been modified to reflect this:
- An adnexal mass with a gestational sac and yolk sac or fetal pole with/without fetal heartbeat is termed “adnexal ectopic”
- Sonographic findings reported as inhomogeneous mass, heterogeneous mass, or adnexal mass (no yolk sac or fetal pole visible) are termed “complex adnexal mass”
Meta-analysis of diagnostic accuracy measures for the different features identified on the ultrasound was not possible due to the small number of comparable studies (different populations, and/or different features visualised).
Studies are summarised in Table 2.
See also the literature search strategy in appendix B and study selection flowchart in appendix C.
Excluded studies
Studies not included in this systematic review with reasons for their exclusions are provided in appendix K.
Summary of clinical studies included in the evidence review
Table 2 provides a brief summary of the included studies.
Table 2
Summary of included studies.
See appendix D for full evidence tables.
Quality assessment of clinical outcomes included in the evidence review
See appendix F for full GRADE tables.
Economic evidence
A systematic review of economic literature was conducted, but no studies were identified which were applicable to this review question.
Economic model
No economic modelling was undertaken for this review.
Evidence statements
Sub-population 1. All symptomatic women (women with pain/bleeding or referred for a scan due to high risk of ectopic pregnancy)
TVUS: adnexal ectopic (adnexal mass with gestational sac and yolk sac or fetal pole +/− fetal heartbeat)
- Low quality evidence from 1 cohort study (N=1880) showed low sensitivity and high specificity to detect tubal ectopic pregnancy using the visualisation of an adnexal ectopic pregnancy with transvaginal ultrasound. The positive likelihood ratio showed this was a very useful feature: when an adnexal ectopic is visualised there is more likely to be a tubal ectopic pregnancy. The negative likelihood ratio showed it was not a useful feature: failure to identify an adnexal ectopic does not markedly reduce the chance of having an ectopic pregnancy.
TVUS: complex adnexal mass: inhomogeneous, heterogeneous, or adnexal mass (no yolk sac or fetal pole)
- Low quality evidence from 1 cohort study (N=1880) showed low sensitivity and high specificity to detect tubal ectopic pregnancy using the visualisation of a complex adnexal mass with transvaginal ultrasound. The positive likelihood ratio showed this to be a very useful feature: when visualised, it has increased likelihood of being an ectopic pregnancy. The negative likelihood ratio showed it was not a useful feature.
TVUS: Free fluid in the pelvis
- Moderate quality evidence from 1 cohort study (N=226) showed moderate sensitivity and specificity to detect tubal ectopic pregnancy using visualisation of free fluid in the pelvis with transvaginal ultrasound. The positive and negative likelihood ratios showed this was not a useful feature.
- High quality evidence from 1 cohort study (N=525) showed high sensitivity and specificity to detect tubal ectopic pregnancy using visualisation of free fluid in the pelvis with transvaginal ultrasound. The positive and negative likelihood ratios showed this to be a very useful feature.
TAS: Free fluid in the pelvis
- Moderate quality evidence from 1 cohort study (N=241) showed low sensitivity and high specificity to detect tubal ectopic pregnancy using visualisation of free fluid in the pelvis with transabdominal ultrasound. The positive likelihood ratio showed this to be a moderately useful feature, but the negative likelihood ratio showed it was not a useful feature.
Sub-population 2. High risk of ectopic pregnancy: includes pregnancy of unknown location and ectopic pregnancy (all intrauterine pregnancies excluded)
TVUS: Pseudo-sac
- Moderate quality evidence from 1 cohort study (N=403) showed low sensitivity and high specificity to detect tubal ectopic pregnancy using visualisation of a pseudo-sac with transvaginal ultrasound. The positive and negative likelihood ratios showed this was not a useful feature.
TVUS: Intrauterine fluid
- Low quality evidence from 1 cohort study (N=128) showed low sensitivity and moderate specificity to detect tubal ectopic pregnancy using visualisation of intrauterine fluid with transvaginal ultrasound. The positive and negative likelihood ratios showed this was not a useful feature.
TVUS: Complex adnexal mass: inhomogeneous mass, heterogeneous mass, or adnexal mass (no yolk sac or fetal pole)
- Low quality evidence from 1 cohort study (N=128) showed moderate sensitivity and high specificity to detect tubal ectopic pregnancy using visualisation of a complex adnexal mass with transvaginal ultrasound. The positive likelihood ratio showed this was a very useful feature. The negative likelihood ratio showed it was not a useful feature.
TVUS: Free fluid in the peritoneal cavity
- Low quality evidence from 1 cohort study (N=128) showed moderate sensitivity and high specificity to detect tubal ectopic pregnancy using visualisation of free fluid in the peritoneal cavity with transvaginal ultrasound. The positive likelihood ratio was not calculable (due to a specificity of 100%). The negative likelihood ratio showed that it was not a useful feature.
Sub-population 3. High risk of ectopic pregnancy: pregnancy of unknown location only (all intrauterine pregnancies and definite ectopic pregnancies excluded)
TVUS: Empty uterus
- Low quality evidence from 2 cohort studies (N=228 and N=635) showed high sensitivity and moderate specificity to detect tubal ectopic pregnancy using visualisation of an empty uterus with transvaginal ultrasound. The positive and negative likelihood ratios showed this was a not useful feature.
TVUS: Pseudo-sac
- Low quality evidence from 1 cohort study (N=77) showed low sensitivity and specificity to detect tubal ectopic pregnancy using visualisation of a pseudo-sac with transvaginal ultrasound. The positive and negative likelihood ratios showed this was a not useful feature.
TVUS: Intrauterine fluid
- Low and moderate quality evidence from 2 cohort studies (N=228 and N=635) showed low sensitivity and high specificity to detect tubal ectopic pregnancy using visualisation of intrauterine fluid with transvaginal ultrasound. The positive and negative likelihood ratios showed this was not a useful feature.
TVUS: Tubal ring sign (bagel sign)
- Low quality evidence from 1 cohort study (N=612) showed high sensitivity and specificity to detect tubal ectopic pregnancy using visualisation of the tubal ring sign with transvaginal ultrasound. The positive likelihood ratio showed this was a very useful feature. The negative likelihood ratio showed this was a moderately useful feature.
TVUS: Complex adnexal mass: inhomogeneous mass, heterogeneous mass, or adnexal mass (no yolk sac or fetal pole)
- Very low quality evidence from 1 cohort study (N=77) showed moderate sensitivity and high specificity to detect tubal ectopic pregnancy using visualisation of a complex adnexal mass with transvaginal ultrasound. The positive likelihood ratio showed this was a useful feature. The negative likelihood ratio showed this was not a useful feature.
- Moderate quality evidence from 1 cohort study (N=663) showed high sensitivity and specificity to detect tubal ectopic pregnancy using visualisation of a complex adnexal mass with transvaginal ultrasound. The positive and negative likelihood ratios showed this to be a very useful feature.
TVUS: Free fluid in the peritoneal cavity
- High quality evidence from 1 cohort study (N=94) showed low sensitivity and high specificity to detect tubal ectopic pregnancy using visualisation of free fluid in the peritoneal cavity with transvaginal ultrasound. The positive and negative likelihood ratios showed this to be not a useful feature.
The committee’s discussion of the evidence
Interpreting the evidence
The outcomes that matter most
The committee agreed that the correct and timely diagnosis of an ectopic pregnancy was vital to be able to offer the most appropriate management options to women. The committee identified the positive likelihood ratio as being of use in making a diagnosis of ectopic pregnancy. Features with a high positive likelihood ratio would increase the chance of identifying an ectopic pregnancy, making the correct diagnosis more likely.
This review aimed to determine the usefulness of individual features seen on an ultrasound scan, rather than whether or not ultrasound itself is a useful tool. Therefore it was noted that the sensitivity of individual features may not be particularly high – women with an ectopic pregnancy may have a variety of different features identified on scan, and a single feature could not be expected to be present in all women. The committee also noted that, overall, it was important not to miss a diagnosis of ectopic pregnancy (high sensitivity preferable), but that this would be accomplished through the current pathway of clinical follow up where scan findings were uncertain.
In addition, the specificity of certain features appeared to be very high in some studies – as the majority of women in the study had a viable, intrauterine pregnancy that was easily identified. Therefore the number of correctly identified “true negative” test results was high.
The committee therefore focused on the likelihood ratios when considering the evidence. Features showing a high positive likelihood ratio would mean that the chance of an ectopic pregnancy being present would be considerably increased. Similarly, a low positive likelihood ratio would reduce the clinical suspicion of an ectopic pregnancy.
The quality of the evidence
The quality of the evidence ranged from very low to high, with downgrading predominantly due to imprecision (based on the confidence intervals of both sensitivity and specificity) and concern over the risk of bias from participant flow (loss-to-follow up resulting in missing data from the final analysis).
On review of the evidence, it was noted that studies included different sub-populations of women. Some studies included all women with pain or bleeding in early pregnancy, others focused on women in whom a viable intrauterine pregnancy had been excluded. It was noted that the pre-test probability of an ectopic pregnancy differed markedly in these populations. Although an ectopic pregnancy is a relatively rare occurrence, if a viable intrauterine pregnancy cannot be seen, then the likelihood of an ectopic pregnancy is increased. Several studies reported on any woman presenting with pain or bleeding or any asymptomatic woman presenting for an ultrasound scan before 13+0 weeks gestation. Other studies excluded obvious IUPs (on first scan), and others excluded obvious IUPs and obvious ectopic pregnancies, so only presenting data for women with pregnancy of unknown location, or complex scan results.
Each of these populations were felt to be relevant to clinical practise, as women may undergo multiple ultrasound scans during the course of early pregnancy. For the first scan, data on all women is relevant. However, if a viable intrauterine pregnancy cannot be confirmed on this scan, then data on the “higher risk” populations becomes relevant. Therefore, the studies were separated into three distinct populations for consideration, but the quality of evidence was not downgraded for indirectness unless other concerns were noted.
The committee considered making separate recommendations for these groups of women (all women, and those at higher risk of ectopic pregnancy – in whom an intrauterine pregnancy had been excluded). However, it was felt that this may lead to a lack of clarity about how to apply the recommendations. Therefore the evidence from the different populations was considered together in order to make recommendations.
The committee discussed the age of the studies, and how the technical capabilities of ultrasound machines have improved over the last 20 years. They highlighted that the reported diagnostic accuracy for the visualisation of features in the studies pre-2000 may not reflect current practice, especially with the use of the transabdominal ultrasound in these earlier studies.
Benefits and harms
The committee noted that the evidence showed that visualisation of an adnexal mass with features of an early pregnancy (a gestational sac containing a yolk sac or fetal pole, with or without a fetal heartbeat) had a very high positive likelihood ratio for the diagnosis of ectopic pregnancy. This was entirely consistent with their clinical experience – that the identification of a mass showing such features would give a firm diagnosis. The committee did not consider that any other features could make such a definite diagnosis of an ectopic pregnancy.
However, other features were also shown to have a high positive likelihood ratio for the identification of ectopic pregnancy. Therefore, the committee agreed that these features should raise a strong suspicion of the diagnosis. These included the presence of a complex, inhomogeneous or non-cystic adnexal mass, or the presence of an adnexal mass with an empty gestation sac (containing no yolk sac, fetal pole or fetal heartbeat) (which may sometimes be described as a “tubal ring sign” or “bagel sign”).
The identification of a collection of fluid in the uterine cavity (which may sometimes be described as a pseudo-sac) or an empty uterus were not shown to have a high positive likelihood ratio for the diagnosis of ectopic pregnancy. However, based on their clinical expertise, the committee members agreed that these features, when present, should raise suspicion of ectopic pregnancy, but women presenting with these features would require further investigation.
The presence of free fluid in the peritoneal cavity on ultrasound scan was noted to cause challenges in interpretation. The committee were aware that a scan finding of “free fluid” could vary between a trace of fluid identified on transvaginal scan, to a large amount of free fluid visible transabdominally. The likelihood of an ectopic pregnancy would be very different in each of these circumstances. This was reflected in the evidence, where some studies showed a high positive likelihood ratio for the diagnosis of ectopic based on the presence of free fluid, and others showed a low positive likelihood ratio. From the evidence, there was no information as to the volume of free fluid in the peritoneal cavity that was visualised, how to measure it, or how the volume could be interpreted. The committee agreed that it may be a marker of an ectopic pregnancy based on the evidence presented, but free fluid alone could not be relied upon for a diagnosis, and women presenting with only this feature would require further investigation.
When scan findings were not conclusive (a diagnosis of ectopic pregnancy could not be made nor excluded) the committee stressed the importance of using other features to help determine the likelihood of an ectopic pregnancy being present. This would include assessing the clinical presentation and serum hCG levels, rather than relying on scan features alone.
The committee were aware that, although the incidence of heterotopic pregnancy (co-existing intrauterine pregnancy and ectopic pregnancy) is rare, it is known to be increasing. The committee members made a recommendation to highlight this issue, as clinicians should scan both the uterus and adnexa for any of the physical features of a pregnancy in all possible locations.
Diagnosis of tubal ectopic pregnancy using visualisation and correct interpretation of certain ultrasound features, will result in reduced delay in treatment and management of the ectopic pregnancy. This may permit a wider range of management options, such as medical or expectant management, in addition to surgery, giving greater choice for women. Early diagnosis should also reduce maternal mortality and morbidity.
Possible harms included the uncertainty of diagnosis in cases where an ultrasound is not definitive. This may lead to unnecessary concern or follow up for women who ultimately are identified as having an intrauterine pregnancy. However, the committee considered that the risks of a missed diagnosis of ectopic pregnancy were so great that this justified the additional follow up and monitoring that may be required.
The committee noted that the majority of the evidence reflected the accuracy of transvaginal, rather than transabdominal, scanning. Transabdominal scanning was considered less accurate, with poorer resolution, particularly at a lower gestational age. However, the committee were aware that some women may decline transvaginal scanning for a variety of reasons, and that this may put them at increased risk of an uncertain diagnosis.
The committee could not identify any obvious disadvantages to the use of certain features visualised on an ultrasound scan to make a diagnosis of ectopic pregnancy, however they acknowledged that ultrasound scan findings can be subjective, may depend on the operator experience, cannot be 100% accurate, and there will still be some false positives and false negatives.
Cost effectiveness and resource use
Ultrasound scanning is already used in women presenting to an early pregnancy unit and therefore there are no additional ultrasound costs due to these recommendations and no significant resource impact is anticipated. The committee agreed that early diagnosis of ectopic pregnancy using the visualisation of certain features on an ultrasound scan may lead to savings as it would lead to:
- Fewer visits to the hospital, clinic, or early pregnancy assessment unit to make a diagnosis
- Reduced number of blood tests (serum hCG) to make a diagnosis
- Reduced costs due to emergency admissions with ruptured ectopic pregnancies.
Overall, the committee agreed that there would be no significant resource impact from these recommendations.
Other factors the committee took into account
The committee were aware that interpretation of ultrasound findings is dependent upon the training of individuals performing the ultrasound scan and considered that each unit has to take the responsibility of having adequately trained and accredited professionals performing ultrasound scans.
The committee discussed that there may be additional factors regarding language barriers in women who did not speak English or women with learning disabilities, and therefore difficulty communicating the different degrees of certainty or uncertainty around the diagnosis of an ectopic pregnancy, and that clear information should be provided, tailored to an individual women’s needs.
The committee also noted that some women, or women from conservative groups within society may avoid transvaginal ultrasound (TVUS) due to possible stigma surrounding the insertion of an object into the vagina, and thus delay a diagnosis. These factors are often highlighted in maternal mortality reports, and the committee acknowledged the importance of working towards educating and supporting women to understand their health/clinical problems and help them to understand that TVUS can be helpful in making a more accurate diagnosis, but that transabdominal ultrasound could be used in these women if necessary (although was not as effective a tool for diagnosis).
References
Ahmed 2004
Ahmed, Ahmed A., Tom, Brian D. M., Calabrese, Peter, Ectopic pregnancy diagnosis and the pseudo-sac, Fertility and Sterility, 81, 1225–8, 2004 [PubMed: 15136081]Barnhart 2011
Barnhart, Kurt T., Fay, Courtney A., Suescum, Maria, Sammel, Mary D., Appleby, Dina, Shaunik, Alka, Dean, Anthony J., Clinical factors affecting the accuracy of ultrasonography in symptomatic first-trimester pregnancy, Obstetrics and Gynecology, 117, 299–306, 2011 [PubMed: 21252743]Dart 1998
Dart,R., Howard,K., Subclassification of indeterminate pelvic ultrasonograms: stratifying the risk of ectopic pregnancy, Academic Emergency Medicine, 5, 313–319, 1998 [PubMed: 9562194]Dart 2002
Dart, Robert Gerard, Burke, Garett, Dart, Linda, Subclassification of indeterminate pelvic ultrasonography: prospective evaluation of the risk of ectopic pregnancy, Annals of Emergency Medicine, 39, 382–8, 2002 [PubMed: 11919524]Hammoud 2005
Hammoud, Ahmad O., Hammoud, Ihab, Bujold, Emmanuel, Gonik, Bernard, Diamond, Michael P., Johnson, Samuel C., The role of sonographic endometrial patterns and endometrial thickness in the differential diagnosis of ectopic pregnancy, American Journal of Obstetrics and Gynecology, 192, 1370–5, 2005 [PubMed: 15902112]Malek-Mellouli 2013
Malek-Mellouli, Monia, Oumara, Maina, Ben Amara, Fethi, Zouch, Ons, Neji, Khaled, Reziga, Hedi, Prediction of ectopic pregnancy in early pregnancy of unknown location, La Tunisie medicale, 91, 27–32, 2013 [PubMed: 23404594]Mehta 1999
Mehta,T.S., Levine,D., McArdle,C.R., Lack of sensitivity of endometrial thickness in predicting the presence of an ectopic pregnancy, Journal of Ultrasound in Medicine, 18, 117–122, 1999 [PubMed: 10206804]Moore 2007
Moore, Chris, Todd, William M., O’Brien, Elizabeth, Lin, Henry, Free fluid in Morison’s pouch on bedside ultrasound predicts need for operative intervention in suspected ectopic pregnancy, Academic emergency medicine : official journal of the Society for Academic Emergency Medicine, 14, 755–8, 2007 [PubMed: 17554008]Nadim 2018
Nadim, B., Infante, F., Lu, C., Sathasivam, N., Condous, G., Morphological ultrasound types known as ‘blob’ and ‘bagel’ signs should be reclassified from suggesting probable to indicating definite tubal ectopic pregnancy, Ultrasound in obstetrics & gynecology : the official journal of the International Society of Ultrasound in Obstetrics and Gynecology, 51, 543–549, 2018 [PubMed: 28195383]Sadek 1995
Sadek,A.L., Schiotz,H.A., Transvaginal sonography in the management of ectopic pregnancy, Acta Obstetricia et Gynecologica Scandinavica, 74, 293–296, 1995 [PubMed: 7732802]
Appendices
Appendix A. Review protocols
Table 3. Review protocol for diagnostic accuracy for ultrasound features for tubal ectopic pregnancy
Appendix B. Literature search strategies
Review question search strategies
Appendix C. Clinical evidence study selection
Appendix D. Clinical evidence tables
Appendix E. Forest plots
There are no forest plots for this evidence review as no meta-analysis was performed.
Appendix F. GRADE tables
Table 6. High risk of ectopic pregnancy: includes PUL and ectopic pregnancy (all IUPs excluded)
Appendix G. Economic evidence study selection
Appendix H. Economic evidence tables
No economic evidence was identified for this review question.
Appendix I. Health economic evidence profiles
No economic evidence was identified for this review question.
Appendix J. Health economic analysis
No health economic analysis was conducted for this review question.
Appendix K. Excluded studies
Economic studies
No economic evidence was identified for this review question.
Appendix L. Research recommendations
No research recommendations were made for this review question.
FINAL
Evidence reviews
developed by the National Guideline Alliance, hosted by the Royal College of Obstetricians and Gynaecologists
Disclaimer: The recommendations in this guideline represent the view of NICE, arrived at after careful consideration of the evidence available. When exercising their judgement, professionals are expected to take this guideline fully into account, alongside the individual needs, preferences and values of their patients or service users. The recommendations in this guideline are not mandatory and the guideline does not override the responsibility of healthcare professionals to make decisions appropriate to the circumstances of the individual patient, in consultation with the patient and/or their carer or guardian.
Local commissioners and/or providers have a responsibility to enable the guideline to be applied when individual health professionals and their patients or service users wish to use it. They should do so in the context of local and national priorities for funding and developing services, and in light of their duties to have due regard to the need to eliminate unlawful discrimination, to advance equality of opportunity and to reduce health inequalities. Nothing in this guideline should be interpreted in a way that would be inconsistent with compliance with those duties.
NICE guidelines cover health and care in England. Decisions on how they apply in other UK countries are made by ministers in the Welsh Government, Scottish Government, and Northern Ireland Executive. All NICE guidance is subject to regular review and may be updated or withdrawn.
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