Free Echogenic Pelvic Fluid: Correlation with Hemoperitoneum

Free Echogenic Pelvic Fluid: Correlation with Hemoperitoneum G. Kimberly Sickler, MD, Phebe C. Chen, MD, Theodore J. Dubinsky, MD, Nabil Maklad, MD, PhD Echogenic fluid is an important extrauterine finding of ectopic pregnancy. The purpose of this study was to determine how accurately echogenic fluid correlates with hemoperitoneum at surgery. Transvaginal sonography was performed in 831 consecutive patients referred to rule out ectopic pregnancy over a 36 month period. Scans were retrospectively evaluated for the presence or absence and echogenicity of free pelvic fluid. Subsequently, 185 patients had a laparotomy or laparoscopy and had documentation of the presence or absence of hemoperitoneum. On transvaginal sonography 125 patients had echogenic fluid, 30 patients had anechoic fluid, and 30 patients had no fluid. Of the 125 patients with echogenic fluid, 122 (98%) patients had hemoperitoneum; none of the patients with anechoic fluid or no detected fluid had hemoperitoneum (0%). Echogenic fluid had a sensitivity of 100%, specificity of 95%, positive predictive value of 98%, and an accuracy of 98% for detecting hemoperitoneum. This study demonstrates that echogenic fluid detected by transvaginal ultrasonography accurately correlates with hemoperitoneum detected at surgery in patients with suspected ectopic pregnancy. KEY WORDS: Ectopic pregnancy; Pregnancy abnormalities; Pregnancy, ultrasonography. T ransvaginal ultrasonography has proven to be a valuable modality in evaluation of women with suspected ectopic pregnancy. 1 4 IUP, Intrauterine pregnancy ABBREVIATIONS Received January 13, 1998, from the Department of Radiology, The University of Texas Health Sciences Center at Houston, Houston, Texas (G.K.S., P.C.C., N.M.); and the Department of Radiology, Harborview Medical Center, University of Washington, Seattle, Washington (T.J.D.). Revised manuscript accepted for publication March 28, 1998. Presented at the 1997 meeting of the American Roentgen Ray Society, San Diego, California. Address correspondence and reprint requests to G. Kimberly Sickler, MD, Department of Radiology, The University of Texas HSC- Houston, 6431 Fannin 2.132 MSB, Houston, TX 77030. Its value lies not only in the near exclusion of ectopic pregnancy by identification of an IUP but also in the diagnosis of an ectopic pregnancy by recognition of key adnexal findings. Transvaginal ultrasonography enables the detection of extrauterine living embryos, tubal rings, complex masses, and free pelvic fluid. Pelvic fluid is an important extrauterine finding in the evaluation of a possible ectopic pregnancy. The identification of moderate to large amounts of fluid has been shown to correlate with a high risk for ectopic pregnancy. 5,6 More recently, characterizing the fluid as echogenic has been proposed as a significant extrauterine risk factor for ectopic pregnancy, regardless of the amount of fluid. 7 The purpose of this study was to evaluate how echogenic fluid detected by transvaginal ultrasonography correlates with surgically proven hemoperitoneum in suspected ectopic pregnancies. 1998 by the American Institute of Ultrasound in Medicine J Ultrasound Med 17:431 435, 1998 0278-4297/98/$3.50

432 FREE ECHOGENIC PELVIC FLUID J Ultrasound Med 17:431 435, 1998 MATERIALS AND METHODS A retrospective study was performed of 831 consecutive patients referred to two institutions for suspected ectopic pregnancy over a 36 month period from March 1993 to March 1996. Patient selection criteria included a positive urine pregnancy test, clinical suspicion for ectopic pregnancy, a transabdominal and transvaginal ultrasonogram within 48 h of a laparotomy or laparoscopy, indication for surgery as determined by an obstetrics and gynecology team, and surgical documentation of the presence or absence of hemoperitoneum. Of the 831 women originally referred, 185 women met the selection criteria and made up the study group. Mean maternal age of the study group was 29 years (range, 15 44 years). Mean menstrual age per last menstrual period was 8 weeks 3 days (range, 4 weeks 2 days 15 weeks 5 days). The human chorionic gonadotropin level ranged from 24,000 to 43,380 miu/ml. Eleven women had prior ectopic pregnancies. Four women had prior bilateral tubal ligations. Sixty-seven women came in initially with pain, 42 women came in with bleeding, and 76 women came in with both pain and bleeding. One of four ultrasonographic systems was used: Acuson 128 XPI (Acuson, Mountain View, CA), Toshiba SSA-270A (Toshiba, Dallas, TX), ATL HDI (Advanced Technology Laboratories, Bothell, WA), and ATL 3000 (Advanced Technology Laboratories). All patients were scanned transabdominally regardless of bladder status, then scanned transvaginally with an empty bladder. A 5 MHz or a 9 5 MHz broadband transvaginal transducer was used. The original ultrasonographic reports and images from both the transabdominal and transvaginal examinations were retrospectively reviewed. Retrospective review was performed by two authors. A standard imaging protocol, including images of the cul-de-sac, adnexa, and periuterine area, had been used in the original search for fluid. Ultrasonographic examinations were performed by board certified sonographers and reviewed, and the majority rescanned by board certified sonologists. The presence or absence of pelvic fluid was documented, regardless of amount. Fluid was categorized as echogenic or anechoic. Fluid was considered echogenic when echoes were identified within the fluid, regardless of degree of echogenicity (Fig. 1). The presence or absence of a clot was not specifically documented on all initial examinations. The authors were blinded to the surgical findings at the time of review. Authors observations were initially made independently, with joint agreement reached on all cases. The presence or absence of an adnexal mass was documented. Surgical and clinical findings were obtained by chart review. RESULTS Of the 185 women studied, 125 (67.6%) women had echogenic fluid, 30 (16.2%) women had anechoic fluid, and 30 (16.2%) women had no fluid detected by transvaginal ultrasonography. Among the 125 women with echogenic fluid, 122 (97.6%) women had hemoperitoneum documented at surgery, and three women had no hemoperitoneum detected at surgery. Of the 30 women with anechoic fluid and 30 women with no fluid detected, none (0%) had hemoperitoneum at surgery (Table 1). Echogenic fluid had a sensitivity of 100%, specificity of 95%, positive predictive value of 97.6%, negative predictive value of 100%, and accuracy of 98.4% for hemoperitoneum. Of the 185 women, 170 women had ectopic pregnancies. Of these, 120 women had hemoperitoneum, and all 120 women had echogenic fluid. Fifty women had no hemoperitoneum, of whom 24 women had no fluid detected at transvaginal ultrasonography, 23 women had anechoic fluid detected, and three women had echogenic fluid detected. Twelve (7%) women had echogenic fluid as the only abnormal finding at transvaginal ultrasonography. Four (2%) women had no adnexal mass or echogenic fluid detected on an ultrasonogram. Table 2 summarizes the extrauterine findings. Twelve of the 185 women had incomplete abortions. Two of the 12 women had echogenic free fluid, an adnexal mass, and hemoperitoneum. Three of the 185 women had a nonvisualized IUP in which diagnostic laparoscopy and not a dilatation and curettage was performed. DISCUSSION Transabdominal and transvaginal ultrasonography play key roles in the evaluation of patients with suspected ectopic pregnancy. 1 11 Intrauterine and extrauterine findings are important in both the exclusion and the diagnosis of ectopic pregnancy. Identification of an IUP, whether normal or abnormal, essentially excludes the diagnosis of ectopic pregnancy. However, as the rate of heterotopic pregnancy increases, 12,13 predominately in the assisted reproduction group, increased suspicion and a careful search for adnexal findings should be undertaken in this subset of patients.

J Ultrasound Med 17:431 435, 1998 SICKLER ET AL 433 A B Figure 1 Transvaginal ultrasonogram shows echogenic fluid. A, Diffuse echoes in cul-de-sac fluid. B, Diffuse echoes plus echogenic clot. Pelvic fluid is an important extrauterine finding of ectopic pregnancies. 5 8,14 Not only is the identification of fluid important but also its characterization as echogenic or anechoic. Free pelvic fluid has been shown to carry a risk for ectopic pregnancy, with echogenic fluid much more worrisome in patients referred with a clinical suspicion. 5 9,15 17 Accurate characterization of pelvic fluid requires adequate gain setting. Too high gain settings can create artifactual echoes in anechoic fluid, and too low settings can cause echogenic fluid to appear anechoic. We have found comparison to the urinary bladder to be helpful in questionable cases, adjusting the gain setting to a level that eliminates artificial echoes in the urine. Additionally, true echoes often demonstrate swirling motion on real-time imaging, either spontaneously or by pressure from the transducer or hand pressure over the lower abdomen. Echogenic amorphous or rounded avascular masses likely representing blood clots can be seen in echogenic fluid, aiding in characterization. 18 Unfortunately, not all the initial examinations commented on the presence or absence of a clot. As this was a retrospective study, specific analysis of clot detection could not be made, but it remains an important observation. Color Doppler examination was also not specifically studied, but it may be helpful in clot characterization. Accurate characterization of free fluid also requires adequate contact with the vaginal wall, as echogenic fluid may appear anechoic if adequate contact is not obtained. Improving contact is easily done by adjusting transducer position. Echogenic fluid was recognized by both the 5 MHz and the 9 5 MHz broadband transvaginal transducers. Echogenic fluid was more easily recognized with the 9 5 MHz broadband transducer, as much of the fluid was located in the pelvic cul-de-sac. Although transabdominal ultrasonography still plays an important role in the evaluation of ectopic pregnancies, 8 transvaginal ultrasonography is superior in the detection of small amounts of free fluid. 11,19 Transvaginal ultrasonography also allows better characterization of this fluid. 7 Caution should be taken when trying to characterize fluid on transabdominal examinations. Fluid appearing anechoic on a transabdominal examination may actually be echogenic on transvaginal ultrasonography. All the patients in the current study underwent transvaginal ultrasonography. We characterized free fluid only on the transvaginal ultrasonography. Occasionally, obviously echogenic fluid was seen on transabdominal examination and confirmed on transvaginal examination. The superior detection and characterization of pelvic fluid by transvaginal ultrasonography lies in the higher frequency transducers, shorter focal zones, closer proximity to the cul-de-sac and adnexa, avoidance of imaging through subcutaneous fat, and absence of need for a full bladder, which can displace small quantities of free fluid out of the pelvis. Transabdominal examination is useful in the detection of free fluid in the upper abdomen, especially the hepatorenal space and paracolic gutters. Free fluid was seen most commonly in the pelvic cul-de-sac, especially when present in small amounts. Fluid was also identified in the adnexa, both on the side of the ectopic pregnancy and contralaterally, and

434 FREE ECHOGENIC PELVIC FLUID J Ultrasound Med 17:431 435, 1998 adjacent to the uterine fundus, particularly in cases with a retroverted uterus. A careful search of these areas should be undertaken in each case of suspected ectopic pregnancy. The amount of echogenic fluid did not alter the correlation with hemoperitoneum. Even very small amounts of echogenic fluid detected in the cul-de-sac correlated with hemoperitoneum. Because of the retrospective nature of this study, it was difficult to correlate accurately the exact amount of fluid seen on transvaginal ultrasonography and the amount of hemoperitoneum. The degree of echogenicity also did not affect the accuracy of echogenic fluid. Both highly echogenic fluid with numerous diffuse echoes and mildly echogenic fluid with scattered echoes represented blood. The present study documents the correlation of transvaginally detected echogenic fluid with hemoperitoneum in the patients with possible ectopic pregnancy for whom surgery was judged to be clinically indicated. We previously have compared ultrasonographic detection of echogenic fluid and culdocentesis. 20 However, the accurate correlation of echogenic fluid and hemoperitoneum had not been studied specifically. Echogenic fluid has a high sensitivity, specificity, positive predictive value, and accuracy for hemoperitoneum in this setting, emphasizing the importance of fluid characterization. Surgery was used as the gold standard for hemoperitoneum in this study, which inherently implies a selection bias of only those patients who had a laparotomy or laparoscopy. Hemoperitoneum was found in 71% of the ectopic pregnancies, correlating with what has been shown previously that up to 81% of ectopic pregnancies can have associated hemoperitoneum of more than 25 ml. 21 Previous sonographic studies have reported echogenic or particulate fluid in 25 to 57% of ectopic pregnancies. 7,16,22 23 The higher rate in this study likely reflects the selected patient population. Although not specifically studied prior to this study, echogenic fluid has correlated with hemoperitoneum. 7,16 Extrauterine findings of a mass, echogenic Table 1: Sonographically Detected Pelvic Fluid and Presence or Absence of Hemoperitoneum at Surgery (n = 185) Hemoperitoneum No Hemoperitoneum Echogenic fluid 122 3 Anechoic fluid 0 30 No fluid 0 30 fluid, or both a mass and echogenic fluid were identified in 166 of the 170 ectopic pregnancies in the current study (94%). The combination of a mass and echogenic fluid was the most common finding of ectopic pregnancy in this study group. Both an isolated adnexal mass and the combination of an adnexal mass and pelvic fluid have been shown to carry a high risk for ectopic pregnancy. 7,16,24 Tongsong and Pongsatha have shown that the combination of echogenic free fluid and an adnexal mass carries a 95% positive predictive value for ectopic pregnancy. 16 Echogenic fluid was an isolated adnexal finding in 7% of our ectopic pregnancy patients as compared with isolated echogenic fluid and isolated fluid representing blood in 15% of ectopic pregnancy patients found in previous studies. 2,7 Although the echogenicity of the fluid was not specifically stated in the latter study, all patients had hemoperitoneum, which emphasizes that echogenic fluid may be the only finding in ectopic pregnancy. Three patients with ectopic pregnancies had echogenic fluid but no hemoperitoneum detected at surgery. The amount of echogenic fluid was small in all three patients. Perhaps this small amount of hemoperitoneum was not documented or recognized at surgery. This may reflect the retrospective nature of this study. Four of the confirmed ectopic pregnancy patients had no echogenic fluid or adnexal mass identified on an ultrasonogram. This coincides with other reports of ectopic pregnancies in which the only finding was an empty uterus in 4.2 and 2.8% of ectopic pregnancies. 2,9 Although these numbers can be reassuring in the setting of a negative ultrasonogram, this reemphasizes the point that despite advances in ultrasonographic imaging, some ectopic pregnancies, although a small number, will be unrecognized sonographically other than by the absence of an IUP. Although not specifically studied, no correlation was found between the presence of echogenic fluid and ectopic rupture. This agrees with previous studies in which fluid was identified in both ruptured and unruptured ectopic pregnancies. 25,26 Identification of echogenic fluid has not proven to be a reliable indicator of tubal rupture. Two patients in this study had ultrasonographic findings suggestive of ectopic pregnancy, with absence of an IUP and the identification of an adnexal mass and echogenic fluid. Both were proven to have incomplete abortions and hemoperitoneum at surgery. Unfortunately, both women were lost to follow-up. It can be postulated that the adnexal masses were ruptured corpus luteum cysts, causing

J Ultrasound Med 17:431 435, 1998 SICKLER ET AL 435 Table 2: Extrauterine Findings in 185 Patients with Suspected Ectopic Pregnancy and Surgical Correlation IUP Ectopic Abortion (Not Visualized) (n = 170) (n = 12) (n = 3) Pelvic fluid: None 24 5 1 Echogenic 123 2 0 Anechoic 23 5 2 Adnexal mass: None 16 8 2 Present 154 4 1 Echogenic fluid and adnexal mass: Neither 4 8 2 Both 111 2 0 Only adnexal mass 43 2 1 Only echogenic fluid 12 0 0 hemoperitoneum. Mahony and associates had a similar case in which the adnexal mass was shown to resolve. 6 In conclusion, echogenic free pelvic fluid detected by transvaginal ultrasonography accurately correlates with hemoperitoneum detected at surgery in patients suspected to have an ectopic pregnancy. A careful search for, and characterization of, pelvic fluid should be undertaken in cases of suspected ectopic pregnancy. REFERENCES 1. Nyberg DA, Mack LA, Jeffrey Jr. RB, et al: Endovaginal sonographic evaluation of ectopic pregnancy: A prospective study. AJR 149:1181, 1987 2. Frates MC, Laing FC: Sonographic evaluation of ectopic pregnancy: An update. AJR 165:251, 1995 3. Braffman BH, Coleman BG, Ramchandani P, et al: Emergency department screening for ectopic pregnancy: A prospective US study. Radiology 190:797, 1994 4. Filly RA: Ectopic pregnancy: The role of sonography. Radiology 162:661, 1987 5. Romero R, Kadar N, Castro D, et al: The value of adnexal sonographic findings in the diagnosis of ectopic pregnancy. Am J Obstet Gynecol 158:52, 1988 6. Mahony BS, Filly RA, Nyberg DA, et al: Sonographic evaluation of ectopic pregnancy. J Ultrasound Med 4:221, 1985 7. Nyberg DA, Hughes MP, Mack LA, et al: Extrauterine findings of ectopic pregnancy at transvaginal US: Importance of echogenic fluid. Radiology 178:823, 1991 8. Zinn HL, Cohen HL, Zinn DL: Ultrasonographic diagnosis of ectopic pregnancy: Importance of transabdominal imaging. J Ultrasound Med 16:603, 1997 9. Dashefsky SM, Lyons EA, Levi CS, et al: Suspected ectopic pregnancy: Endovaginal and transvesical US. Radiology 169:181, 1988 10. Kivikoshi AI, Martin CM, Smeltzer JS: Transabdominal and transvaginal ultrasonography in the diagnosis of ectopic pregnancy: A comparative study. Am J Obstet Gynecol 163:123, 1990 11. Valenzano M, Anserini P, Remorgida V, et al: Transabdominal and transvaginal ultrasonographic diagnosis of ectopic pregnancy: Clinical implications. Gynecol Obstet Invest 31:8, 1991 12. Rizk B, Tan SL, Morcos S, et al: Heterotopic pregnancies after in vitro fertilization and embryo transfer. Am J Obstet Gynecol 164:161, 1991 13. Goldman GA, Fisch B, Ovadia J, et al: Heterotopic pregnancy after assisted reproductive technologies. Obstet Gynecol Surv 47:217, 1992 14. Rottem S, Thaler I, Timor-Tritsch E: Classification of tubal gestations by transvaginal sonography. Ultrasound Obstet Gynecol 1:197, 1991 15. Cacciatore B, Stenman U-H, Ylostalo P: Comparison of abdominal and vaginal sonography in suspected ectopic pregnancy. Obstet Gynecol 73:770, 1989 16. Tongsong T, Pongsatha S: Transvaginal sonographic features in diagnosis of ectopic pregnancy. Int Gynecol Obstet 43:277, 1993 17. Rempen A: Vaginal sonography in ectopic pregnancy. A prospective evaluation. J Ultrasound Med 7:381, 1988 18. Jeffrey RB, Laing FC: Echogenic clot: A useful sign of pelvic hemoperitoneum. Radiology 145:139, 1982 19. Nyberg DA, Laing FC, Jeffrey RB: Sonographic detection of subtle pelvic fluid collections. AJR 143:261, 1984 20. Chen PC, Sickler GK, Dubinsky TJ, et al: Sonographic detection of echogenic fluid and correlation with culdocentesis in the evaluation of ectopic pregnancy. AJR 170:1299, 1998 21. DiMarchi JM, Kosasa TS, Hale RW: What is the significance of the human chorionic gonadotropin value in ectopic pregnancy? Obstet Gynecol 74:851, 1989 22. Cacciatore B: Can the status of tubal pregnancy be predicted with transvaginal sonography? A prospective comparison of sonographic, surgical, and serum hcg findings. Radiology 177:481, 1990 23. Fleischer AC, Pennell RG, McKee MS, et al: Ectopic pregnancy: Features at transvaginal sonography. Radiology 174:375, 1990 24. Brown DL, Doubilet PM: Transvaginal sonography for diagnosing ectopic regnancy: Positivity criteria and performance characteristics. J Ultrasound Med 13:259, 1994 25. Frates MC, Brown DL, Doubilet PM, et al: Tubal rupture in patients with ectopic pregnancy: Diagnosis with transvaginal US. Radiology 191:769, 1994 26. Atri M, Stempel J, Bret PM: Accuracy of transvaginal ultrasonography for detention of hematosalpinx in ectopic pregnancy. J Clin Ultrasound 20:255, 1992