|Year : 2020 | Volume
| Issue : 2 | Page : 505-510
Acquired uterine enhanced myometrial vascularity after dilation and curettage diagnosed by color flow Doppler ultrasonography
Mohamed A Emara, Abdelhaseib S Saad, Sara M Fadl, Abdel Hameid E. Shahin
Department of Obstetrics and Gynecology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
|Date of Submission||01-Dec-2019|
|Date of Decision||31-Dec-2019|
|Date of Acceptance||11-Jan-2020|
|Date of Web Publication||27-Jun-2020|
Sara M Fadl
Anas Street, Shebin El-Kom, Menoufia
Source of Support: None, Conflict of Interest: None
To assess the role of color flow Doppler ultrasonography (US) in the diagnosis of acquired uterine enhanced myometrial vascularities (EMV).
EMV represents arteriovenous malformations that may be acquired after dilatation and curettage (D&C).
Patients and methods
This was a prospective study that included 107 patients presented with abnormal uterine bleeding, and after D&C, they were followed up to detect acquired EMV by using two-dimensional US and color flow Doppler.
This study included 107 patients with age ranged between 18 and 59 years. The patients presented with intermittent or progressive vaginal bleeding owing to abortion (n = 95) (88.8%), dysfunctional uterine bleeding (n = 6) not controlled by medications, and secondary postpartum hemorrhage after caesarian section (n = 6). Two-dimensional ultrasonic picture of myometrial texture after D&C was done, and it showed heterogeneous lesion in 34 (31.8%) and homogeneous texture in 73 (68.2%) patients. The use of color power Doppler on suspected lesion showed high-velocity blood flow within the vascular 'web' with peak systolic velocity ranging from 16 to 48 cm/s in 24 (22.4%) patients and the resistance index recorded ranging from 0.28 to 0.79, with a mean of 0.56. The incidence of highly suggested EMV among 107 patients who had undergone dilation and curettage in the Department of Obstetrics and Gynecology in Menoufia University Hospital was 22.4%.
Routine gray-scale and color Doppler US evaluation of patients with early pregnancy failure or cesarean scar pregnancy is indicated to detect EMV as early as possible.
Keywords: dilatation and curettage, Doppler, enhanced myometrial vascularity
|How to cite this article:|
Emara MA, Saad AS, Fadl SM, E. Shahin AH. Acquired uterine enhanced myometrial vascularity after dilation and curettage diagnosed by color flow Doppler ultrasonography. Menoufia Med J 2020;33:505-10
|How to cite this URL:|
Emara MA, Saad AS, Fadl SM, E. Shahin AH. Acquired uterine enhanced myometrial vascularity after dilation and curettage diagnosed by color flow Doppler ultrasonography. Menoufia Med J [serial online] 2020 [cited 2020 Jul 15];33:505-10. Available from: http://www.mmj.eg.net/text.asp?2020/33/2/505/287791
| Introduction|| |
Acquired uterine enhanced myometrial vascularities (EMVs) are abnormal communication between the branches of the uterine artery and the venous plexuses within the myometrium. They occur exclusively in women in their reproductive years. They were first described by Dubreil and Loubat in 1926 as 'aneurysme cirsoide de l'uterus'. They may cause life-threatening hemorrhage. They can occur when the thin wall of the abnormal vessels are disrupted either naturally after menstruation or artificially after instrumentation. EMVs result from previous uterine surgery including diagnostic or therapeutic dilatation and curettage (D&C), cesarean section (CS), or myomectomy. Endometrial carcinoma, cervical carcinoma, and gestational trophoblastic disease have also been implicated as causes of EMVs.
The clinical symptoms of EMVs can appear gradually or suddenly, most commonly in the form of heavy or irregular vaginal bleeding after a miscarriage, uterine surgery, or treated or untreated cesarean scar pregnancy.
If there is increased bleeding during D&C performed for abnormal uterine bleeding (AUB), EMVs should be suspected.
Historically, EMVs were diagnosed by pathological examination after hysterectomy. Recently, less-invasive imaging studies have been used for diagnostic purposes. Transvaginal ultrasound (US) is the initial imaging study of choice for AUB. As a definitive diagnosis based on gray-scale US imaging is difficult alone, Doppler imaging is imperative to the diagnosis. Although the presence of a tubular, hypoechogenic structure in the myometrium by gray-scale IS imaging is common, it is not specific for EMVs. The identification of uterine high-velocity blood flow with low resistance by Doppler US is highly suggestive for EMVs. The diagnosis can be confirmed when these imaging findings are coupled with maternal serum beta subunit human chorionic gonadotropin, which has a slower decline in retained products of conception; computed tomography; and additional information beyond that can be garnered by MRI.
Historically, treatment for symptomatic EMVs required hysterectomy, and transcatheter embolization (TCE) has provided an alternative and less-invasive treatment option for patients wishing to preserve fertility. Laparoscopic occlusion of the internal iliac arteries was successfully performed using nonabsorbent clips for acquired EMVs that had persistent bleeding 6 weeks following two uterine artery embolization procedures. Additionally, surgical ligation of the uterine arteries after TCE has been reported as well as when coupled with laparoscopic myometrial lesion resection. Unilateral or bilateral laparoscopic bipolar coagulation of the uterine arteries has also been performed successfully for acquired EMVs. These procedures were most commonly performed for persistent bleeding despite initial or repeat TCE.
The aim of this study was to detect the incidence of acquired EMVs among female patients who had undergone D&C at Menoufia University Hospital by using color flow Doppler US.
| Patients and Methods|| |
After approval of the Local Ethical Committee of Menoufia University Hospital, written consents from all patients were obtained to participate in our study. This is a prospective study that was conducted in Obstetrics and Gynecology Department at Menoufia University Hospital in the period from October 2018 to October 2019. The study was carried on all patients who presented to outpatient clinic or emergency room with AUB, and after D&C, they were followed up for 2–6 weeks to detect acquired EMVs. The number of patients who were included in this study was 107. Exclusion criteria included patients with viable pregnancies at the time of EMV diagnosis, patients on contraceptive methods or anticoagulant, and patients with history of congenital EMVs or symptoms suggest them. All participants were subjected to full history taking, complete clinical examination, and laboratory investigations (BHCG (Beta subunit Human Chorionic Gonadotropin), complete blood count, and prothrombin time). Moreover, transvaginal gray-scale US imaging was done to detect if suspected lesion presented or not in the myometrium, and then color flow Doppler US (Sonata plus, Egypt) with customary frequencies of 2–12 MHz), with pulse repetition for Doppler settings of 600 and 900 MHz, was done on suspected lesions, and Doppler velocities and resistive indices were measured.
Criteria for the sonographic diagnosis (suspected lesion) were anechoic, tubular, and tortuous structures seen by two-dimensional (2D) gray-scale US imaging on sagittal and/or transverse section of the uterus, which subjectively reveal an unusually rich vascularity with tortuous-appearing blood vessels that were concentrated in a small area of myometrium adjacent to the uterine cavity, with or without clearly visible products of conception followed by color power Doppler imaging. Objectively a demonstration of high-velocity blood flow within the vascular 'web' with a peak systolic velocity (PSV) and low resistance to determine the highest peak systolic velocity, we used a very narrow sampling window (2 mm) and measured at least 5–10 different sites within the vascular malformation. We used the highest PSV value to represent the EMVs as shown in [Figure 1]. Patients were followed up to 6 weeks postoperatively.
|Figure 1: (a) Anechoic, tubular, and tortuous structures were seen by two-dimensional gray-scale ultrasound imaging in myometrium. (b) Color Doppler reveals an unusually rich vascularity with tortuous-appearing blood vessels that are concentrated in a small area of myometrium. (c) Doppler flow indices' measurements (PSV-ED-S\D). PSV, peak systolic velocity.|
Click here to view
Statistical analysis was performed with Statistical Package for Social Science statistical software (SPSS) (version 22; SPSS Inc., Chicago, Illinois, USA). Data from questionnaires were entered as numerical or categorical, as appropriate. Two types of statistics were done: descriptive statistics or analytical, such as Spearman's correlation, which was used when data were not normally distributed. P value was considered statistically significant when it is less than 0.05 and highly significant if less than or equal to 0.01.
| Results|| |
This study included 107 patients with age ranged between 18 and 59 years, with mean age of 29.64 ± 8.124 years. The parity number was from 0 to 6, with a mean of 2.03 ± 1.262. The range of number of abortions was from 0 to 7, with a mean of 0.55 ± 1.268. The range of gestational age (GA) among pregnant patients who undergone D&C owing to abortion or secondary postpartum hemorrhage was 0–37 weeks, with mean GA of 13.19 ± 7.9 weeks. A total of 95 (88.8%) patients presented with intermittent or progressive vaginal bleeding owing to abortion [either incomplete abortion (45.8%) or missed abortion (37.4%) or therapeutic termination of pregnancy by misoprostol and then dilatation and suction evacuation or curettage owing to fetal lethal congenital anomalies in 5.6%]; other six patients were referred owing to Dysfunctional Uterine Bleeding (DUB) not controlled by medications (either perimenopausal bleeding in four patients, represented by 3.7%, or postmenopausal bleeding in two patients, represent 1.9%); and the remaining six patients presented with secondary postpartum hemorrhage after CS surgical history of the patients included 15 patients with history of previous D&C and 61 patients with history of previous CS, one patient had undergone left salpingectomy on top of ectopic pregnancy, and one patient had undergone hysteroscopic removal of intrauterine septum.
Two-dimensional US picture of myometrial texture, which was done after D&C, showed myometrial heterogeneous hypoechoic tubular structure in 34 (31.8%) patients and homogenous texture in 73 (68.2%) patients. The use of color power Doppler on the suspected lesion showed high-velocity blood flow within the vascular 'web,' with PSV ranged from 16 to 48 cm/s in 24 (22.4%) patients, and the resistance index (RI) recorded ranged from 0.28 to 0.79, with a mean of 0.56, as shown in [Table 1] and [Figure 2].
|Table 1: Spectral Doppler analysis of uterine enhanced myometrial vascularities|
Click here to view
|Figure 2: (a) Color power Doppler reveals an unusually rich vascularity with tortuous-appearing blood vessels that are concentrated in a small area of myometrium. (b) Measurement of blood flow indices.|
Click here to view
The positive group was divided into three subgroup: the first section PSV ranged from 16 to 18 cm/s in five (20.8%) patients, second section ranged from 18 to 20 cm/s in one (4.2%) patient, and third one was more than 20 cm/s in 18 (75%) patients. The incidence of highly suggested EMVs in the studied group by using color Doppler as a noninvasive primitive diagnostic tool among 107 patients who had undergone D&C in the Department of Obstetrics and Gynecology in Menoufia University Hospital was 22.4%, as shown in [Table 2].
Myometrial heterogeneous lesion was detected in the anterior wall in 12 (50%) patients, in posterior wall in nine (37.5%) patients, and in fundal area in three (12.5%) patients. Sensitivity and specificity of 2D US as a less-invasive initial imaging tool have been used for diagnostic purposes of AUB, which were compared with color Doppler US. The study assumed that sensitivity of 2D US as screening tool is 100%, specificity 88%, accuracy 91%, positive predictive value 71%, and negative predictive value is 100%.
Clinical course follow-up for 6 weeks of positive group beyond that was mild to moderate bleeding in 22 (91.7%) patients and severe vaginal bleeding in two (8.3%) patients, in the form of postpartum hemorrhage in one patient and postabortive bleeding in another one (both needed blood transfusion and antihemorrhagic measures, and hysterectomy was done on one of them).
By analysis of the statistical data, the results were as following: a significant positive correlation was between PSV and ED, whereas a significant negative correlation was between PSV and ED and RI, a significant positive co-relation was found between GA in pregnant patients group, whereas a significant negative co-relation was between number of previous abortions and PSV. A positive significant co-relation was found between number of previous D&C and probability of occurrence of EMVs and women who had undergone previous D&C 9.1 more susceptible for EMVs than whom without history of previous D&C. These results are shown in [Table 3].
|Table 3: Significant (negative or positive co-relation) and nonsignificant correlation were shown between multiple variables|
Click here to view
| Discussion|| |
This study included 107 patients who were highly suggestive to have EMVs, with an age range from 18 to 59 years, with a mean of 29.64 years, that is, almost patients in their reproductive years. These results coincide with Touhami et al., Yoon et al., and Agarwal et al., who stated that EMVs most exclusively occur in women in childbearing period, with mean age of 29 years, which ensures our results.
In this study, the most common complaint was either intermittent or progressive vaginal bleeding owing to either because of postabortive bleeding in 95 (88.8%) patients; six patients referred owing to DUB not controlled by medications, with either perimenopausal bleeding in four patients, represented by 3.7%, or postmenopausal bleeding in two patients, represent by 1.9%; and other six patients presented with secondary postpartum hemorrhage after CS. These results coincide with Yoon et al., Timor-Tritsch et al., Evans et al., and Zhu et al., who stated that the most common complaint of the studied group is vaginal bleeding, either intermittent or progressive vaginal bleeding.
In this study, 107 patients had undergone D&C owing to variable reasons, such as incomplete abortion and therapeutic-induced abortion in 95 (88.8%) patients, or AUB not controlled by medications with negative BHCG either perimenopausal or postmenopausal bleeding in six (5.6%) patients, or other six patient presented with secondary postpartum hemorrhage after CS with positive significant co-relation with previous intrauterine surgical history especially previous history of D&C in 10 (41.7%) patients and in 16 patients from 61 patients with previous history of CS, but no significant relation with number of other surgeries, as the study included one patient with history of excision of hysteroscopic excision intrauterine septum and one patient with left salpingectomy owing to ectopic pregnancy. These results showed that the most common intrauterine surgery related to acquired EMVs is D&C and then CS. The results of Kim et al. showed that 14 patients among 19 patients who had acquired EMVs had a D&C history. Lalitha et al. conducted a retrospective study covering the period from 2008 to 2013, which stated that five positive patients had a previous D&C history. The study by Yoon et al. was carried out on 54 patients with acquired EMVs, who stated that 93% of patients had a history of uterine surgeries, especially D&C. Timor-Tritsch and colleagues revealed that 55.5% of studied patients had a history of previous intrauterine surgeries, which coincides with this study. Mosedale et al. considered CS was the most common cause of EMVs, which was not the situation of this study. Ultrasonic scan in this study was done within 2-week interval from D&C, which coincides with Timor-Tritsch et al., Evans et al., and Agarwal et al., which assumed that main cause of acquired EMVs is D&C. All these studies coincide with this study. Zhu et al. revealed that all included patients were diagnosed with EMVs secondary to curettage, CS, or gestational trophoblastic disease. Among the 62 patients, 21 (33.9%) patients had a history of CS, 53 (85.5%) patients had a history of curettage, 18 (29.0%) patients had a history of both CS and D&C, and the other six (9.5%) patients had no history of either CS or D&C, including four had a history of medical abortion and the other two had a history of vaginal delivery.
In this study, 2D US picture showed either myometrial heterogeneous tubular lesion in 34 (31.8%) patients and anechoic myometrium in 73 (68.2%) patients. These ultrasonic pictures coincide with Evan et al., who considered gray-scale US is a primitive diagnostic tool for scanning of EMVs, and this coincides with this study, which assumed that sensitivity of 2D US as screening tool is 100%, specificity 88%, accuracy 91%, positive predictive value 71%, and negative predictive value is 100%. This study revealed that heterogeneous tubular structure's anatomical site is anterior wall in 12 (50%) patients, in posterior wall in nine (37.5%) patients and in fundal area in three (12.5%) patients. This coincides with the study by Maleux et al.. This study used color power Doppler on suspected lesion detected by 2D US showing high-velocity blood flow within the vascular 'web' with a PSV and low RI, which coincides with Evans et al. and Patki et al.. This study revealed that clinical status follow-up for 6 weeks of the positive group beyond that was mild to moderate bleeding in 22 (91.7%) patients and severe vaginal bleeding in two (8.3%) patients, in the form of postpartum hemorrhage in one patient and postabortive bleeding in another one. This coincides with the study by Van den Bosch et al., which regarded EMVs as a reflection of the intermediate stages in the involution of the placental bed. They disappear and usually do not cause abnormal postpartum postabortive bleeding. Timmerman et al. suggested that EMVs represent a subinvolution of the placental bed with failed obliteration of vessels in the absence of retained Products of Conception (POCs) after cessation of the pregnancy; this explains the severe bleeding after the case of a delayed postabortive hemorrhage or after curettage of cesarean scar pregnancy. The study by Whitehead et al. revealed that asymptomatic EMVs are common in the puerperium and disappear spontaneously in most cases, which coincides with this study.
This study revealed there was a significant co-relation between PSV and ED, whereas a significant negative co-relation between PSV and RI, which coincides with Evans et al..
| Conclusion|| |
Acquired EMVs are a pathological phenomenon that occur because of intrauterine treatment procedures and are usually presented by vaginal bleeding. Clinicians should be aware that the sonographic diagnosis can be based only by Doppler interrogation of the uterus. Spontaneous abortions, D&C, and, recently, CS seem to present known risks for an acquired EMV. Although in the past uterine artery angiography was the gold standard for diagnosis, presently transvaginal gray-scale and color Doppler US evaluation are emerging as the simplest, best, and most cost-effective diagnostic imaging modalities. Routine gray-scale and color Doppler US evaluation of patients with early pregnancy failure is indicated to detect EMVs as early as possible.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Darlow KL, Horne AW, Critchley HOD, Walker J, Duncan WC. Management of vascular uterine lesions associated with persistent low-level human chorionic gonadotropin. J Fam Plann Reprod Health Care 2008; 34
Lowe LH, Marchant TC, Rivard DC, Scherbel AJ. Vascular malformations: classification and terminology the radiologist needs to know. Semin Roentgenol 2012; 47
Lui MW, Shek NW, Li RH, Chu F, Pun TC. Management of heterotopic cesarean scar pregnancy by repeated transvaginal ultrasonography-guided aspiration with successful preservation of normal intrauterine pregnancy and complicated by arteriovenous malformation. Eur J Obstet Gynecol Reprod Biol 2014; 175
Evans A, Roland E, Richard M, Meghan M, Robert L, Jarrod C, et al
. Acquired uterine arteriovenous fistula following dilatation and curettage: an uncommon cause of vaginal bleeding. Radiol Case Rep 2017; 12
Przybojewski SJ, Sadler DJ. Novel image-guided management of a uterine arteriovenous malformation. Cardiovasc Intervent Radiol 2011; 34
Touhami O, Gregoire J, Noel P, Trinh XB, Plante M. Uterine arteriovenous malformations following gestational trophoblastic neoplasia: a systematic review. Eur J Obstet Gynecol Reprod Biol 2014; 181
Patki SS, Dabade T, Kumar V. Uterine arteriovenous malformation. Int J Reprod Contracept Obstet Gynecol 2017; 6
Timmerman D, Wauters J, Van Calenbergh S, Van Schoubroeck D, Maleux G, Van Den Bosch T, et al
. Color Doppler imaging is a valuable tool for the diagnosis and management of uterine vascular malformations. Ultrasound Obstet Gynecol 2003; 21
Rangarajan RD, Moloney JC, Anderson HJ. Diagnosis and nonsurgical management of uterine arteriovenous malformation. Cardiovasc Intervent Radiol 2007; 30
Timmerman D, Van den Bosch T, Peeraer K, Debrouwere E, Van Schoubroech D, Stockx L, et al
. Vascular malformations in the uterus: ultrasonographic diagnosis and conservative management. Eur J Obstet Gynecol Reprod Biol 2000; 92
Katz MD, Sugay SB, Walker DK, Palmer SL, Marx MV. Beyond hemostasis: spectrum of gynecologic and obstetric indications for transcatheter embolization. Radiographics 2012; 32
Wilms GE, Favril A, Baert AL, Poppe W, Van Assche FA. Transcatheter embolization of uterine arteriovenous malformations. Cardiovasc Intervent Radiol 1986; 9
Chen SQ, Jiang HY, Li JB, Fan L, Liu MJ, Yao SZ. Treatment of uterine arteriovenous malformation by myometrial lesion resection combined with artery occlusion under laparoscopy: a case report and literature review. Eur J Obstet Gynecol Reprod Biol 2013; 169
Wu YC, Liu WM, Yuan CC, Ng HT. Successful treatment of symptomatic arteriovenous malformation of the uterus using laparoscopic bipolar coagulation of uterine vessels. Fertil Steril 2001; 76
Yoon DJ, Jones M, Taani JA, Buhimschi C, Dowell JD. A systematic review of acquired uterine arteriovenous malformations: pathophysiology, diagnosis, and transcatheter treatment. Am J Perinatol Rep 2016; 6
Agarwal N, Chopra S, Aggarwal N, Gorsi U. Congenital uterine arteriovenous malformations presenting as postcoital bleeding: a rare presentation of a rare clinical condition. J Clin Imaging Sci 2017; 7
Timor-Tritsch IE, Monteagudo A, Santos R, Tsymbal T, Pineda G, Arslan AA. The diagnosis, treatment, and follow-up of cesarean scar pregnancy. Am J Obstet Gynecol 2012; 207
Zhu YP, Sun ZJ, Lang JH, Pan J. Clinical characteristic and management of acquired uterine arteriovenous malformation. Chin Med J (Engl) 2018; 131
Kim D, Moon NR, Lee SR, Won YD, Lee HJ, Park TC, et al
. Acquired uterine arteriovenous malformation in a cesarean scar pregnancy. Taiwan J Obstet Gynecol 2013; 52
Lalitha N, Seetha P, Shanmugasundaram R, Rajendiran G. Uterine arteriovenous malformation: case series and literature review. J Obstet Gynecol India 2016; 66
Mosedale TE, Martin G, Majumdar A. Uterine arteriovenous malformation: a rising cause of postpartum haemorrhage?. J Obstet Gynaecol 2016; 36
Maleux G, Timmerman D, Heye S, Wilms G. Acquired uterine vascular malformations: radiological and clinical outcome after transcatheter embolotherapy. Eur Radiol 2006; 16
Van den Bosch T, Van Schoubroeck D, Timmerman D. Maximum peak systolic velocity and management of highly vascularized retained products of conception. J Ultrasound Med 2015; 34
Whitehead KJ, Smith MC, Li DY. Arteriovenous malformations and other vascular malformation syndromes. Cold Spring Harb Perspect Med 2013; 3
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]