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DOI: 10.1055/a-1967-2134
Judging Urgency in 343 Ectopic Pregnancies Prior to Surgery – The Importance of Transvaginal Sonographic Diagnosis of Intraabdominal Free Blood
Beurteilung der operativen Dringlichkeit in 343 Eileiterschwangerschaften – die Bedeutung von freiem intraabdominalem Blut in der TransvaginalsonografieAbstract
Objectives Assessing urgency in ectopic pregnancies (ECP) remains controversial since the disorder covers a large clinical spectrum. Severe conditions such as acute abdomen or hemodynamic instability are mostly related to intra-abdominal blood loss diagnosed as free fluid (FF) on transvaginal sonography (TVS). The aims of the current study were to investigate the value of FF and to assess other potentially predictive parameters for judging urgency.
Methods Retrospective cohort analysis on prospectively collected cases of proven ECP (n = 343). Demographics, clinical and laboratory parameters, and findings on TVS and laparoscopy (LSC) were extracted from the digital patient file. FF on TVS and free blood (FB) in LSC were evaluated. Low urgency was defined as FB (LSC) < 100 ml and high urgency as FB (LSC) ≥ 300 ml. The best subset of variables for the prediction of FB was selected and predictors of urgency were evaluated using receiver operator characteristic (ROC) curves.
Results Clinical symptoms, age, β-HCG, hemoglobin (HB) preoperative, and FF were examined in multivariate analysis for the cutoff values of 100 ml and 300 ml. FF was the only independent predictor for low and high urgency; HB preoperative was only significant for high urgency offering marginal improvement. ROC analysis revealed FF as an excellent discriminatory parameter for defining low (AUC 0.837, 95% CI 0.794–0.879) and high urgency (AUC 0.902, 95 % CI 0.860–0.945).
Conclusion Single assessment of FF on TVS is most valuable for judging urgency. However, the exact cutoff values for a low- and high-risk situation must still be defined.
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Zusammenfassung
Ziele Die Beurteilung der Dringlichkeit bei ektopen Schwangerschaften ist aufgrund des breiten klinischen Spektrums schwierig. Schwere Verläufe (akutes Abdomen oder hämodynamische Instabilität) sind meist mit intraabdominalem Blutverlust verbunden, welcher als freie Flüssigkeit (FF) mittels transvaginaler Sonografie (TVS) diagnostiziert werden kann. Ziel der vorliegenden Studie war es, den diagnostischen Wert der FF sowie andere potenziell prädiktive Parameter für die Beurteilung der Dringlichkeit zu untersuchen.
Methode Retrospektive Kohortenanalyse von prospektiv erhobenen Fällen (n=343) mit nachgewiesener ektopen Schwangerschaft. Demografische Daten, Klinik, Laborparameter, sonografische und Befunde der Laparoskopie (LSC) wurden einbezogen. Die Bewertung von FF in der TVS und freiem Blut (FB) in der LSC erfolgte anhand des Bildmaterials. FB < 100ml wurde als wenig- und ≥ 300ml als hochdringlich definiert. Die besten Variablen für die Vorhersage von FB wurden bestimmt und ihre Prädiktion der Dringlichkeit mittels ROC-Kurven bewertet.
Ergebnisse Klinik, Alter, β-HCG, präoperatives Hämoglobin (HB) und FF wurden in einer multivariaten Analyse für die Cut-off-Werte 100ml und 300ml untersucht. Zur Bestimmung geringer (AUC 0,837, 95% CI 0,794–0,879) und hoher Dringlichkeit (AUC 0,902, 95% CI 0,860–0,945) war FF ein hervorragend diskriminierender Parameter; das HB erbrachte nur eine marginale Verbesserung der Vorhersagekraft und nur für hohe Dringlichkeit.
Schlussfolgerungen FF ist für die Beurteilung der Dringlichkeit am wertvollsten, wobei die genauen Grenzwerte für eine Niedrigrisiko- oder Hochrisikosituation festzulegen bleiben.
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Introduction
In the last two decades, substantial progress has been made in the diagnosis of ectopic pregnancy (ECP) by transvaginal sonography (TVS), leading to direct ECP visualization in the vast majority of cases [1] [2] [3] [4] [5] [6]. In contrast, urgency remains debatable since the clinical course of ECP covers a large spectrum with different prognoses. It varies from spontaneous resolution as described in 42% of cases [7], including cases without [8] or only limited free fluid (FF) on TVS [9], justifying expectant [7] [10] or conservative [11] management, to a potentially life-threatening condition, indicating emergency intervention without delay [12].
Usually, the danger arising from ECP is defined by severe conditions such as abdominal pain, acute abdomen, low or decreasing venous hemoglobin levels (HB), and hemodynamic instability [13] [14] [15] [16] [17]. All these conditions are mostly related to occult intra-abdominal blood loss diagnosed as FF on TVS and confirmed as free blood (FB) in laparoscopy (LSC), appearing as hemoperitoneum with liquid and clotted parts [6].
Any assessment of FB is more or less imprecise [18] even if based on intraoperative blood aspiration [12]. However, in cases with a suspicion of ECP, the amount of FF on TVS was found to correlate with FB in LSC, paving the way to comprehensively define preoperative urgency. An estimate of FB 300–400 mL has been proposed as a preoperative cutoff value to diagnose severe hemorrhage, declaring high urgency as well as the need for rapid operative intervention [5] [12] [19] [20].
In this study, we investigated the value of FF assessment on TVS and other potentially predictive factors to define not only high but also low urgency.
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Methods
This study is a retrospective cohort analysis on prospectively collected cases between January 2012 and March 2020 of laparoscopically investigated ECP. Only cases with adequate documentation of FF on TVS and FB in LSC were included ([Fig. 1]).
![](https://www.thieme-connect.de/media/ultraschall/202306/thumbnails/10-1055-a-1967-2134_19673502.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)
We extracted demographics, risk factors, clinical and laboratory findings, TVS examinations, and findings in laparoscopy from the patient’s digital chart file ([Table 1]). All laboratory measures including the exact time of each blood examination were assessed (compare [Table 1]): The last HB before operation, the first HB after operation, the difference between them, and the last β-HCG before operation.
The sonographic examination was typically performed in a supine position on a gynecologic chair with a slightly elevated upper body. This examination was usually done by a resident on duty and supervised by a staff physician. FF includes different types of blood consistency with liquid and clotted parts. In case of ECP, we counted any representation of FF found in the pelvic or abdominal cavity as part of FB, independently from its echogenicity [6] [19] [20] [21] [22]. Following the concept of the sentinel clot, which appears first in the vicinity of the bleeding source [23] [24], we primarily relied on TVS ([Fig. 2]), and, if needed, extended the examination by transabdominal sonography (TAS) to assess the entire abdomen, especially Morison’s pouch (hepatorenal, right upper abdomen) and Koller’s pouch (lienorenal, left upper abdomen).
![](https://www.thieme-connect.de/media/ultraschall/202306/thumbnails/10-1055-a-1967-2134_19673503.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)
FF (TVS) was not described in detail in the clinical routine, so that three experienced sonographers reviewed the complete dataset. The experts rated each case regarding the total amount of FF in milliliters, as well as separately for liquids and clots, and assigned them to one of the four semiquantitative categories ([Table 2]): no FF, minimal FF (only in pouch of Douglas (POD), less than 3 × 3 cm), moderate FF (only in the POD more than 3 × 3 cm), severe FF (in the POD more than 3 × 3 cm and/or adnex and/or excavatio vesicouterina and/or Morison's pouch), trapped fluid outside the ovary (e.g., hematosalpinx) or inside the ovary (e.g., corpus luteum graviditatis) was not counted as FF [6]. In cases of divergent estimates, the reviewers tried to achieve consent through discussion. Otherwise, the opinion of the majority (2 to 1) was recorded.
The beginning of LSC was assessed by its protocolled start time. We defined the complete intraperitoneal FB as being equal to hemoperitoneum, and equal to the total amount of FB, clotted, and liquid together ([Fig. 2]). FB was estimated by the operator regularly at the beginning of the operation, not necessarily being measured by aspiration. Only in cases of low or very low quantities, where numeric estimations were not given, we transformed the verbal descriptions as follows: “no” to 0 mL, “minimal” to 10 mL, “few” to 30 mL, “some” to 50 mL, thereby consciously assigning these descriptions to the group of FB < 100 mL. Similar to FF, we divided FB into four categories ([Table 2]) and assessed it separately for liquid and clots. We set the stop of bleeding equal to the beginning of the operation. Furthermore, the presence or absence of ECP rupture was recorded.
We investigated the value of FF assessment on TVS as well as other potentially predictive factors for defining not only high (FB ≥ 300 mL) but also low urgency (FB < 100 mL) ([Fig. 2], image 2a).
Data were collected in Microsoft Excel (Excel 2019, Microsoft Corporation, Redmond, Washington, USA). Statistical analyses were performed using R version 4.0.0 (R Foundation for Statistical Computing, Vienna, Austria). Continuous variables are presented as median with interquartile range (IQR) or mean ± standard deviation (SD) with range. Continuous and ordinal variables were correlated using Spearman’s rank correlation rho. Changes in continuous and ordinal variables from TVS to LSC were analyzed using Wilcoxon's signed rank test with continuity correction. Differences between groups were assessed using the Wilcoxon rank sum test with continuity correction and the Kruskal-Wallis test. Categorical and ordinal variables are presented as frequencies and percentages. Differences in categorical variables between groups were assessed using Pearson’s chi-square test and Fisher’s exact test as appropriate. Proportions like sensitivity, specificity, positive and negative predictive value are presented with 95% Wilson confidence intervals (CI). Two-sided p-values less or equal to 0.05 were considered statistically significant. Univariate and multivariable linear regressions were performed to predict FB. Variables with skew distributions were logarithmically transformed for these analyses. For transformations, zero values of FF and FB were set to 10 mL. Variables were included based on p-values < 0.2 in univariate analyses and clinical knowledge. A best subset of variables for prediction of FB was selected based on the Bayesian information criterion (BIC) using the procedure bestglm. The best model was used in logistic regressions to predict low and high urgency. The results are presented as odds ratios (OR) with 95% CI. Predictors of urgency were evaluated using receiver operator characteristic (ROC) curves and presented as areas under the curve (AUC) with 95% CI.
Prior to this retrospective study, ethics approval by the local ethics committee was obtained. Only patients who provided written general consent for the incorporation of their data into research were included. This study considered the STROBE criteria.
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Results
In total, 343 patients with confirmed tubal and nontubal ECP and adequately documented FF on TVS and FB in LSC were included ([Fig. 1]). Demographics are given by [Table 1]. Based on the literature and our own experience, we analyzed a selection of potentially predictive factors to define urgency in ECP (Supplementary Table 1).
Time of diagnosis and clinical presentation. In our cohort, the great majority (85%, 293/343) declared symptoms such as pain and/or vaginal bleeding. No asymptomatic patient (with LMP) presented severe FB ≥ 300 mL before 7+0 (weeks + days) ([Table 1]). Only one asymptomatic woman (2%, 1/41) had sonographically diagnosed FF and operatively confirmed FB of 300 mL, but at 7+5 with β-HCG 1,103 IU/L. She had no prior history of ECP and received infertility treatment. Furthermore, all nine patients with hemodynamic instability (3%, 9/343) presented severe FB ([Fig. 3]). Here, pregnancy was diagnosed in consequence of the emergency examination, and not before, taking place in two patients at 4+0 or earlier, and in three patients at 7+0 or later.
![](https://www.thieme-connect.de/media/ultraschall/202306/thumbnails/10-1055-a-1967-2134_19673504.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)
Hemoglobin: Pre- and postoperative HB as well as its difference correlated significantly with FB (LSC) (all p < 0.001) ([Fig. 4], Supplementary Table 1).
![](https://www.thieme-connect.de/media/ultraschall/202306/thumbnails/10-1055-a-1967-2134_19673505.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)
Hemoglobin: Pre- and postoperative HB as well as its difference correlated significantly with FB (LSC) (all p < 0.001) (Supplementary Table 1).
Hemodynamic instability. Seven of the patients with hemodynamic instability (78%, 7/9) were diagnosed with FF 1,657 ± 883 (400–3,000) and confirmed as hemoperitoneum of FB 2,478 ± 924 (500–3,500) (mL, mean ± SD (range)). Conversion to laparotomy was necessary in two cases. The preoperative HB (96 ± 26 (39–122)), postoperative HB (60 ± 12 (41–78)), and HB difference (43 ± 10 (28–59) (g/L) correlated significantly with FB. The operators defined hemoperitoneum as a consequence of slow but long-lasting bleeding (89%, 8/9) rather than as a result of a sudden rise in bleeding due to arrosion of one or more bigger vessels (11%, 1/9) ([Fig. 2]).
Correlation of FF (TVS) with FB (LSC). We found a strong correlation between the total amounts of FF and FB (Spearman’s rank correlation p < 0.001, rho = 0.7) (Supplementary Table 1, [Fig. 3]).
Liquid and clotted parts. We found moderate to high correlations between FF on TVS and FB in LSC, for both liquid (rho 0.47, p < 0.001) and clotted parts (rho 0.60, p < 0.001) ([Fig. 3]). No difference was found between the categories of liquid and clotted parts, comparing FF and FB ([Table 2]). Otherwise, the difference between these parts depended significantly on the amount of FB (p < 0.001, Kruskal-Wallis rank sum test): In higher total amounts of FF, deviations were greater, both in terms of under- and overestimation ([Fig. 5]). However, there was no evidence of a systematic error to under- or overestimate liquids or clots (p 0.15 and 0.30, Wilcoxon signed rank test with continuity correction).
![](https://www.thieme-connect.de/media/ultraschall/202306/thumbnails/10-1055-a-1967-2134_19673506.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)
Major bleeding site. Tubal ECP, representing 91% (311/343) of all confirmed ECP, showed FB of 100 mL (median, range 0–3,000 mL). The other seven ECP locations together covered 9%, showing very differing amounts of FB ([Fig. 6]). Due to the low numbers in all locations other than tubal ECP, major bleeding site was not used for risk stratification.
![](https://www.thieme-connect.de/media/ultraschall/202306/thumbnails/10-1055-a-1967-2134_19673507.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)
Risk stratification of intraperitoneal hemorrhage. The following factors correlated significantly with the total amount of FB in LSC (Supplementary Table 1): the absence of clinical symptoms, only vaginal bleeding, only pain, hemodynamic instability, age, HB pre- and postoperative, HB difference, FF, also in its morphologically different aspects (FF liquid and clotted), and ruptured ECP. In univariate analysis (Supplementary Table 1), most of these factors correlated significantly with the total amount of FB (LSC), examined also for two different cutoff values (100 mL and 300 mL). We did not process the clearly not significant parameters (obstetric history), underpowered (hemodynamically unstable), postoperative (HB postoperative, HB difference, ruptured ECP) as well as factual dependent parameters (FF clotted and FF liquid). In multivariable linear regression ([Table 3]), we analyzed clinical symptoms as a categorical variable with five categories of symptoms. In this analysis, clinical symptoms, HB preoperative, and FF were significant predictors of FB. Best subset selection among 32 tested models found FF together with preoperative HB as the BIC optimal predictor. The second-best model consisted of FF alone. In the logistic regressions for prediction of low and high urgency, FF was the only independent predictor for both low and high urgency. Preoperative HB was only significant for high urgency ([Table 3]).
ROC analysis revealed FF (TVS) as an excellent discriminatory parameter for defining low urgency as well as high urgency. Adding preoperative HB to FF revealed only a marginal, probably clinically not relevant improvement in the prediction of FB in LSC for defining high urgency ([Fig. 7]). The Youden Index based on the calculated ROC curves was used to determine the best differentiating threshold for low and high urgency. The optimum cutoff value for predicting low urgency (FB < 100 mL) was 150 mL FF; the optimum cutoff value for predicting high urgency (FB ≥ 300 mL) was 250 mL FF ([Table 4]).
![](https://www.thieme-connect.de/media/ultraschall/202306/thumbnails/10-1055-a-1967-2134_19673508.jpg)
![Zoom Image](/products/assets/desktop/css/img/icon-figure-zoom.png)
Outcome and survival: All 343 patients recovered from ECP and left the hospital within 8 days.
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Discussion
Our study revealed FF on TVS as the main factor for reasonably defining low and high urgency in ECP.
Time of diagnosis and clinical presentation. None of the asymptomatic patients with LMP (12%, 41/343) presented severe FB (LSC) before 7+0 (weeks + days). Furthermore, none of the patients with hemodynamic instability (3%, 9/343) were aware of their pregnancy, since no one had attended regular first pregnancy examination before 7+1 or had done a urine pregnancy test as usual when menstruation is lacking.
The correlation of FF (TVS) with FB (LSC) was highly significant, not only for the total amounts ([Fig. 3]) but also for liquid and clotted parts separately ([Fig. 5], [Table 2]). The time-related differences between the assessments in TVS and LSC are considered to be irrelevant. TVS is well known as a reliable method for assessing FF in the pelvis [5] [6] [12] [21] [25] [26] [27] whereas different semiquantitative approaches have been applied [6] [9] [12] [19] [21]. We found the equivalent of a hemoperitoneum of 300 mL in a POD filled with FF of any echogenicity, and just exceeding the edge of the fundus on TVS ([Fig. 2], image 2a). It is an easily reproducible landmark and in perfect agreement with other assessments [5] [9] [12].
Liquid and clotted parts. A blurred uterus contour or a generally remarkably reduced view may serve as strong indicators for clots in contact with the uterus ([Table 2]). For liquid and clotted parts, a higher amount of FB correlated with higher deviations of TVS-estimated FF ([Fig. 5]). Although the occurrence of clots may be considered an indicator for urgency [12], we found that liquid and clotted parts on TVS and LSC typically appeared in an approximately 1:1 relation between 100 mL and 1000 mL, so that differentiation of liquidity would probably not help to define urgency ([Fig. 5]).
Predictors of intraperitoneal hemorrhage. None of the investigated preoperative parameters was able to predict low or high urgency, except for the assessment of FF on TVS ([Fig. 3], Supplementary Table 1), and notably HB ([Table 3]), but only as a low degree additive for the assessment in high urgency ([Fig. 7]). Hemodynamic instability constitutes a common presentation in medically less developed countries. However, in our cohort, these rare events did not have a relevant influence on risk stratification. Moreover, stable hemoperitoneum with ECP undergoing spontaneous resolution may be treated expectantly. Pain was a significant indicator for “not low urgency” only in univariate analysis. The optimum cutoff value was FF = 150 mL for predicting low urgency, and FF = 250 mL for high urgency ([Fig. 7]). The search for reasonable cutoff values may also be based on > 90% sensitivity for defining high urgency and > 90% specificity for defining low urgency ([Table 4]). This approach would lead to FF < 10 mL determining low urgency and FF ≥ 100 mL determining high urgency, which is substantially more restrictive than the cutoffs we had empirically chosen. Prospective clinical studies should determine the meaningful application of cutoff values for FF assessment in diagnosing FB.
Possible limitations of the study are its retrospective design, the impracticality of precise free fluid assessment even during laparoscopy, and the lack of reproducibility. Gestational age is based only on the reported LMP so that we cannot exclude a stronger influence of this parameter on urgency. In our cohort, 44 women became pregnant following fertility treatment, whereby the potential confounder of an increased amount of FF after ovarian stimulation cannot be excluded. Strengths included the high denominator, the histological ECP diagnosis, and the gold standard outcomes. Future considerations should include the implementation of this approach in a multicenter study.
We conclude that assessing FF on TVS is of outmost relevance in assigning low and high urgency, supporting an optimum ECP management. The more FF in TVS, the higher the urgency. However, the exact cutoff values remain debatable. We found the equivalent of a hemoperitoneum of 300 mL, defining high urgency, in a POD filled with FF of any echogenicity, and just exceeding the edge of the fundus on TVS.
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Conflict of Interest
The authors declare that they have no conflict of interest.
Acknowledgement
Our deep thanks go to the patients and all members of our Department of OB/GYN and Reproductive Endocrinology at the University Hospital of Zurich for their dedication and great support in this project, especially to Mrs. Carla Trachsel, and Dr. Deivis Strutas. This project was supported by a generous research grant of the EMDO Foundation, Zurich, Switzerland.
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References
- 1 Condous G, Okaro E, Khalid A. et al. The accuracy of transvaginal ultrasonography for the diagnosis of ectopic pregnancy prior to surgery. Hum Reprod 2005; 20: 1404-1409
- 2 Jurkovic D, Mavrelos D. Catch me if you scan: ultrasound diagnosis of ectopic pregnancy. Ultrasound Obstet Gynecol 2007; 30: 1-7
- 3 Casikar I, Reid S, Condous G. Ectopic pregnancy: Ultrasound diagnosis in modern management. Clin Obstet Gynecol 2012; 55: 402-409
- 4 Kirk E, Bottomley C, Bourne T. Diagnosing ectopic pregnancy and current concepts in the management of pregnancy of unknown location. Hum Reprod Update 2014; 20: 250-261
- 5 Dooley WM, Chaggar P, De Braud LV. et al. Effect of morphological type of extrauterine ectopic pregnancy on accuracy of preoperative ultrasound diagnosis. Ultrasound Obstet Gynecol 2019; 54: 538-544
- 6 Pape J, Bajka A, Strutas D. et al. The predictive value of decisive and soft ultrasound criteria for ectopic pregnancy identification in 321 preoperative cases. Ultraschall in Med 2021; DOI: 10.1055/a-1487-5030.
- 7 Elson J, Tailor A, Banerjee S. et al. Expectant management of tubal ectopic pregnancy: prediction of successful outcome using decision tree analysis. Ultrasound Obstet Gynecol 2004; 23: 552-556
- 8 Mol BW, Hajenius PJ, Engelsbel S. et al. Can noninvasive diagnostic tools predict tubal rupture or active bleeding in patients with tubal pregnancy?. Fertil Steril 1999; 71: 167-173
- 9 Bignardi T, Condous G. Does tubal ectopic pregnancy with hemoperitoneum always require surgery?. Ultrasound Obstet Gynecol 2009; 33: 711-715
- 10 Mavrelos D, Nicks H, Jamil A. et al. Efficacy and safety of a clinical protocol for expectant management of selected women diagnosed with a tubal ectopic pregnancy. Ultrasound Obstet Gynecol 2013; 42: 102-107
- 11 Lipscomb GH, McCord ML, Stovall TG. et al. Predictors of success of methotrexate treatment in women with tubal ectopic pregnancies. N Engl J Med 1999; 341: 1974-1978
- 12 Rajah K, Goodhart V, Zamora KP. et al. How to measure size of tubal ectopic pregnancy on ultrasound. Ultrasound Obstet Gynecol 2018; 52: 103-109
- 13 AAFP. 2020 Accessed February 15, 2021 at: https://www.aafp.org/afp/2020/0515/p599.html
- 14 ACOG. Practice Bulletin 191: Tubal ectopic pregnancy. 2018 Accessed February 15, 2021 at: https://journals.lww.com/greenjournal/Fulltext/2018/02000/ACOG_Practice_Bulletin_No__191__Tubal_Ectopic.38.aspx
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- 18 Yefet E, Yossef A, Suleiman A. et al. Hemoglobin drop following postpartum hemorrhage. Sci Rep 2020; 10 (01) 21546 DOI: 10.1038/s41598-020-77799-0.
- 19 Fauconnier A, Mabrouk A, Salomon LJ. et al. Ultrasound assessment of haemoperitoneum in ectopic pregnancy: derivation of a prediction model. World J Emerg Surg 2007; 2: 23 DOI: 10.1186/1749-7922-2-23.
- 20 Popowski T, Huchon C, Toret-Labeeuw F. et al. Hemoperitoneum assessment in ectopic pregnancy. Int J Obstet Gyn 2012; 116: 97-100
- 21 Frates MC, Brown DL, Doubilet PM. et al. Tubal rupture in patients with ectopic pregnancy: diagnosis with transvaginal US. Radiology 1994; 191: 769-772
- 22 Frates MC, Doubilet PM, Peters HE. et al. Adnexal sonographic findings in ectopic pregnancy and their correlation with tubal rupture and human chorionic gonadotropin levels. J Ultrasound Med 2014; 33: 697-703
- 23 Baqué P, Iannelli A, Dausse F. et al. A new method to approach exact hemoperitoneum volume in a splenic trauma model using ultrasonography. Surg Radiol Anat 2005; 27: 149-253
- 24 Lubner M, Menias C, Rucker C. et al. Blood in the belly: CT findings of hemoperitoneum. Radiographics 2007; 27 (01) 109-125
- 25 Sickler GK, Chen PC, Dubinsky TJ. et al. Free echogenic pelvic fluid: correlation with hemoperitoneum. J Ultrasound Med 1998; 17: 431-435
- 26 Abrams BJ, Sukumvanich P, Seibel R. et al. Ultrasound for the detection of Intraperitoneal Fluid : The role of Trendelenburg positioning. AM J Emerg Med 1999; 17: 117-120
- 27 Salomon LJ, Nassar M, Bernard JP. et al. A score-based method to improve the quality of emergency gynaecological ultrasound examination. Eur J Obstet Gynecol Reprod Biol 2009; 143: 116-120
Correspondence
Publication History
Received: 15 February 2022
Accepted after revision: 19 October 2022
Article published online:
19 January 2023
© 2023. Thieme. All rights reserved.
Georg Thieme Verlag KG
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References
- 1 Condous G, Okaro E, Khalid A. et al. The accuracy of transvaginal ultrasonography for the diagnosis of ectopic pregnancy prior to surgery. Hum Reprod 2005; 20: 1404-1409
- 2 Jurkovic D, Mavrelos D. Catch me if you scan: ultrasound diagnosis of ectopic pregnancy. Ultrasound Obstet Gynecol 2007; 30: 1-7
- 3 Casikar I, Reid S, Condous G. Ectopic pregnancy: Ultrasound diagnosis in modern management. Clin Obstet Gynecol 2012; 55: 402-409
- 4 Kirk E, Bottomley C, Bourne T. Diagnosing ectopic pregnancy and current concepts in the management of pregnancy of unknown location. Hum Reprod Update 2014; 20: 250-261
- 5 Dooley WM, Chaggar P, De Braud LV. et al. Effect of morphological type of extrauterine ectopic pregnancy on accuracy of preoperative ultrasound diagnosis. Ultrasound Obstet Gynecol 2019; 54: 538-544
- 6 Pape J, Bajka A, Strutas D. et al. The predictive value of decisive and soft ultrasound criteria for ectopic pregnancy identification in 321 preoperative cases. Ultraschall in Med 2021; DOI: 10.1055/a-1487-5030.
- 7 Elson J, Tailor A, Banerjee S. et al. Expectant management of tubal ectopic pregnancy: prediction of successful outcome using decision tree analysis. Ultrasound Obstet Gynecol 2004; 23: 552-556
- 8 Mol BW, Hajenius PJ, Engelsbel S. et al. Can noninvasive diagnostic tools predict tubal rupture or active bleeding in patients with tubal pregnancy?. Fertil Steril 1999; 71: 167-173
- 9 Bignardi T, Condous G. Does tubal ectopic pregnancy with hemoperitoneum always require surgery?. Ultrasound Obstet Gynecol 2009; 33: 711-715
- 10 Mavrelos D, Nicks H, Jamil A. et al. Efficacy and safety of a clinical protocol for expectant management of selected women diagnosed with a tubal ectopic pregnancy. Ultrasound Obstet Gynecol 2013; 42: 102-107
- 11 Lipscomb GH, McCord ML, Stovall TG. et al. Predictors of success of methotrexate treatment in women with tubal ectopic pregnancies. N Engl J Med 1999; 341: 1974-1978
- 12 Rajah K, Goodhart V, Zamora KP. et al. How to measure size of tubal ectopic pregnancy on ultrasound. Ultrasound Obstet Gynecol 2018; 52: 103-109
- 13 AAFP. 2020 Accessed February 15, 2021 at: https://www.aafp.org/afp/2020/0515/p599.html
- 14 ACOG. Practice Bulletin 191: Tubal ectopic pregnancy. 2018 Accessed February 15, 2021 at: https://journals.lww.com/greenjournal/Fulltext/2018/02000/ACOG_Practice_Bulletin_No__191__Tubal_Ectopic.38.aspx
- 15 NICE. Accessed February 15, 2021 at: https://www.nice.org.uk/guidance/ng126/chapter/recommendations
- 16 RCOG. Accessed February 15, 2021 at: https://www.rcog.org.uk/en/guidelines-research-services/guidelines/gtg21/
- 17 UpToDate. Accessed February 15, 2021 at: https://www.uptodate.com/contents/ectopic-pregnancy-clinical-manifestations-and-diagnosis
- 18 Yefet E, Yossef A, Suleiman A. et al. Hemoglobin drop following postpartum hemorrhage. Sci Rep 2020; 10 (01) 21546 DOI: 10.1038/s41598-020-77799-0.
- 19 Fauconnier A, Mabrouk A, Salomon LJ. et al. Ultrasound assessment of haemoperitoneum in ectopic pregnancy: derivation of a prediction model. World J Emerg Surg 2007; 2: 23 DOI: 10.1186/1749-7922-2-23.
- 20 Popowski T, Huchon C, Toret-Labeeuw F. et al. Hemoperitoneum assessment in ectopic pregnancy. Int J Obstet Gyn 2012; 116: 97-100
- 21 Frates MC, Brown DL, Doubilet PM. et al. Tubal rupture in patients with ectopic pregnancy: diagnosis with transvaginal US. Radiology 1994; 191: 769-772
- 22 Frates MC, Doubilet PM, Peters HE. et al. Adnexal sonographic findings in ectopic pregnancy and their correlation with tubal rupture and human chorionic gonadotropin levels. J Ultrasound Med 2014; 33: 697-703
- 23 Baqué P, Iannelli A, Dausse F. et al. A new method to approach exact hemoperitoneum volume in a splenic trauma model using ultrasonography. Surg Radiol Anat 2005; 27: 149-253
- 24 Lubner M, Menias C, Rucker C. et al. Blood in the belly: CT findings of hemoperitoneum. Radiographics 2007; 27 (01) 109-125
- 25 Sickler GK, Chen PC, Dubinsky TJ. et al. Free echogenic pelvic fluid: correlation with hemoperitoneum. J Ultrasound Med 1998; 17: 431-435
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