Uterine arteriovenous malformations (AVMs) are rare vascular lesions causing abnormal and possible life-threatening bleeding [1] [2]. They are classified as congenital, resulting from abnormality in the embryonic uterine angiogenesis and acquired, usually traumatic and resulting from prior uterine curettage, pregnancy termination, cesarean section or uterine surgery [3]. The common anatomical landmark is represented by a tangle of vessels showing connections between feeding arteries and draining veins without interposed capillary network [4]. Functionally, AVMs show high blood-flow and low resistance, presenting as color mosaic with flow reversal on Color Doppler Ultrasound (US) and low-impedance and high-velocity on spectral analysis [5]. Angiography computed tomography (CT) and magnetic resonance imaging (MRI) scan can define feeder vessels and the anatomy of AVMs [6]. Angiography is considered the gold standard for AVMs diagnosis, recognizing feeder arteries and early venous filling [3] [7]. Hysteroscopy is the reference technique to assess intrauterine pathology but currently there are few reports assessing the endoscopic imaging of AVMs [8][9][10][11]. To our knowledge in current literature no patients with AVM underwent hysteroscopy treatment. We report the case of a patient with a uterine AVM unintentionally treated by hysteroscopy, following a preoperative diagnosis of submucous myoma.

A 52-years-old female without significant medical history was scheduled for hysteroscopy resection of an intrauterine mass. She had an obstetrical history of cesarean section at 23-years-old due to breech presentation and an uncomplicated vaginal birth at 36-years-old. In the last four years chronic heavy periodic menstrual bleeding and intermenstrual bleeding have been reported. Oral estroprogestins have been administered during the last 18 months with no improvement of symptoms. In October 2014, transvaginal gray scale US detected an endometrial lesion measuring 28 mm in largest diameter, suspected to be a fundal submucous myoma by saline infusion sonography (Figure 1). No further investigation was accomplished. No abnormality was found at physical examination. Hysteroscopy was carried out under conscious sedation by an experienced surgeon (GG). After cervical dilatation, uterine cavity was assessed by a 27 Fr resectoscope fitted with 4 mm bipolar loop (Versapoint Bipolar System, Gynecare, Ethicon Inc., Menlo Park CA) set at 160 W power and Versapulse vapor-cutting mode. Continuous saline flow was delivered at working pressure set at 40 mmHg by an electronic irrigation-suction device. Hysteroscopy identified a soft mass sizing 30 mm, arising from the uterine fundus by a large pedicle. The covering mucosal lining was evenly smooth, neither prominent vascularization nor pulsatile vessels were found. Based on these findings, rather than a myoma, inspective features oriented the surgeon to a polyp-like mass (Figure 2). Since the beginning of resection, a heavy bleeding was originated from crowded vessels showing both arterial (pulsating, roundly-shaped vessels showing a thickened muscular wall) and venous (non pulsating, oval shaped vessels showing a thin wall) features (Figure 3A-B). An extensive use of low-frequency current was applied to achieve hemostasis. The mass was almost entirely removed but near its pedicle an uncontrollable bleeding hampered the safe visualization of surgical field. The procedure was stopped and a Foley catheter was inserted into the endometrial cavity and 10 cc of saline was inflated to control the blood loss. The surgery lasted 23 minutes without any saline deficit recorded. After three hours from intervention the balloon was removed, no significant bleeding was observed and the patient was discharged after two hours of clinical monitoring. The pathologic assessment reported the following: "Vascular malformation formed by arterial and venous vessels dissociating smooth muscle fibers" (Figure 4). In order to evaluate vascularization and extent of the residual uterine mass, one month after intervention the patient was re-assessed by eco Color Doppler Transvaginal US and TC angiography. Both examinations did not show evidence of any mass or abnormal vascularity. Two months after intervention a second-look hysteroscopy confirmed the absence of residual mass and only an uneven thickening of fibrous consistence were found instead of pedicle. A coagulation of this endometrial area was accomplished. After 12 months from surgery no abnormal bleeding was recorded and no abnormalities were found at physical examination and transvaginal US.

Hysteroscopy imaging of uterine AVM has been described as normal appearing endometrium [11], pulsatile vessels bulging of the endometrial cavity [10] [12]and more frequently as highly vascular masses indistinguishable from Retained Products of Conception (RPOC) [8][9] [13]. On color Doppler US, RPOC [14], accreta [15] and subinvolution of the placental bed [5] share features common to AVMs, due to the high-flow and low-resistance characterizing placental blood flow [16]. In the majority of the reports, the diagnosis of AVMs was given only through US after termination of pregnancy and in several series an uneventful, spontaneous and fast resolution of AVM was detected [1] [3][5][7][17][18]. Therefore, several AVMs reported in literature were probably pregnancy-related complications instead of real structural vascular abnormalities [3] [7][16][18]. Far from pregnancy termination or in menopausal patients, in absence of the bias related to the persistence of a misleading placental blood-flow, AVMs are rarely reported [1][2][4][6][19]. Pathologic findings on uterine specimens or endometrial biopsies are rarely recorded as support of AVMs diagnosis [4] [12][13][17], due to either the expanding use of Uterine Artery Embolization (UAE) as primary therapy or to the belief that endometrial surgical instrumentation can worsen uterine bleeding [2][3] [7][14]. The treatment options for AVMs depend on clinical presentation. In asymptomatic patients or in case of non severe uterine bleeding, expectant management and medical hormone therapies or methylergometrine have shown to be effective. In anemic or hemodynamically unstable patients selective UAE is the preferred treatment of AVMs, especially in women who desire to preserve fertility. Other conservative surgical managements (less frequently reported) are laparotomy removal, laparoscopic bipolar coagulation and ligation of the uterine artery. Hysterectomy is suggested in cases of life threatening bleeding or when fertility preservation is not of concern [3]. To our knowledge, hysteroscopy resection was never reported for AVMs treatment. In the above presented patient, a diagnosis of AVM, was pathologically confirmed and it was probably originally related to past cesarean section. The US imaging detected an intrauterine mass mimicking a submucous myoma and showed polyp-like features at hysteroscopy-view. Before intervention, gray-scale US underestimated the vascular nature of the endometrial mass and color Doppler assessment was not applied. The electrosurgical resection of the lesion caused an unexpected excessive bleeding, poorly controlled by coagulating current and hampering its safe surgical removal even under hysteroscopy vision. In this case, the bleeding was stopped by an endometrial compressive device and the AVM was entirely removed by a single-step hysteroscopy surgery. This positive result was probably related to the favorable topography of AVM itself, mainly expanding within endometrial cavity and sparing myometrium.

Uterine arteriovenous malformations (AVMs) can present myoma-like or polyp-like features at ultrasound scan and hysteroscopy assessment, respectively. A color Doppler investigation should be always considered when the clinical background cannot safely exclude the above reported rare (but potentially life-threatening) cause of uterine hemorrhage. The experience presented confirms the common belief that in cases of suspected AVM, primary endometrial surgical instrumentation such as D&C and even hysteroscopy resection should be avoided or managed with extreme caution, due to the high risk of uterine hemorrhage.

We thank Mrs Elena Bosoni for language revision of the Manuscript.

1. Yazawa H, Soeda S, Hiraiwa T, et al. Prospective evaluation of the incidence of uterine vascular malformations developing after abortion or delivery. J Minim Invasive Gynecol 2013 May-Jun;20(3):360–7.   [CrossRef]   [Pubmed]    
2. Kim TH, Lee HH. Presenting features of women with uterine arteriovenous malformations. Fertil Steril 2010 Nov;94(6):2330.e7–10.   [CrossRef]   [Pubmed]    
3. Vijayakumar A, Srinivas A, Chandrashekar BM, Vijayakumar A. Uterine vascular lesions. Rev Obstet Gynecol 2013;6(2):69–79.   [Pubmed]    
4. Fleming H, Ostör AG, Pickel H, Fortune DW. Arteriovenous malformations of the uterus. Obstet Gynecol 1989 Feb;73(2):209–14.   [Pubmed]    
5. Timmerman D, Wauters J, Van Calenbergh S, et al. Color Doppler imaging is a valuable tool for the diagnosis and management of uterine vascular malformations. Ultrasound Obstet Gynecol 2003 Jun;21(6):570–7.   [CrossRef]   [Pubmed]    
6. Aiyappan SK, Ranga U, Veeraiyan S. Doppler Sonography and 3D CT Angiography of Acquired Uterine Arteriovenous Malformations (AVMs): Report of Two Cases. J Clin Diagn Res 2014 Feb;8(2):187–9.   [CrossRef]   [Pubmed]    
7. Grivell RM, Reid KM, Mellor A. Uterine arteriovenous malformations: a review of the current literature. Obstet Gynecol Surv 2005 Nov;60(11):761–7.   [CrossRef]   [Pubmed]    
8. Taylor E, Hitkari J. Hysteroscopic identification of a uterine arteriovenous malformation. J Obstet Gynaecol Can 2009 Dec;31(12):1117–8.   [Pubmed]    
9. Chittawar PB, Patel K, Agrawal P, Bhandari S. Hysteroscopic diagnosis and successful management of an acquired uterine arteriovenous malformation by percutaneous embolotherapy. J Midlife Health 2013 Jan;4(1):57–9.   [CrossRef]   [Pubmed]    
10. Rosa E Silva JC, de Aguiar FM, de Sá Rosa E Silva AC, Candido Dos Reis FJ, Poli Neto OB, Nogueira AA. Conservative management of large uterine arteriovenous malformation: case report. Fertil Steril 2008 Dec;90(6):2406–7.   [CrossRef]   [Pubmed]    
11. Corticelli A, Podestà M, Pedretti L, Papadia A, Francescangeli E, Valenzano M. Uterine arteriovenous malformation: a case report diagnosed by sonohysterography. Clin Exp Obstet Gynecol 2005;32(2):132–4.   [Pubmed]    
12. Scioscia M, Zantedeschi B, Trivella G, Fratelli N, Cosma S, Minelli L. A suggestive diagnosis of uterine arteriovenous fistula based on ultrasonography and hysteroscopy. Eur J Obstet Gynecol Reprod Biol 2012 Jan;160(1):116–7.   [CrossRef]   [Pubmed]    
13. Goyal S, Goyal A, Mahajan S, Sharma S, Dev G. Acquired uterine arteriovenous malformation developing in retained products of conception: a diagnostic dilemma. J Obstet Gynaecol Res 2014 Jan;40(1):271–4.   [CrossRef]   [Pubmed]    
14. Kamaya A, Petrovitch I, Chen B, Frederick CE, Jeffrey RB. Retained products of conception: spectrum of color Doppler findings. J Ultrasound Med 2009 Aug;28(8):1031–41.   [Pubmed]    
15. Takeda A, Koyama K, Imoto S, Mori M, Nakano T, Nakamura H. Conservative management of placenta increta after first trimester abortion by transcatheter arterial chemoembolization: a case report and review of the literature. Arch Gynecol Obstet 2010 Mar;281(3):381–6.   [CrossRef]   [Pubmed]    
16. Müngen E. Vascular abnormalities of the uterus: have we recently over-diagnosed them? Ultrasound Obstet Gynecol 2003 Jun;21(6):529–31.   [CrossRef]   [Pubmed]    
17. Rufener SL, Adusumilli S, Weadock WJ, Caoili E. Sonography of uterine abnormalities in postpartum and postabortion patients: a potential pitfall of interpretation. J Ultrasound Med 2008 Mar;27(3):343–8.   [Pubmed]    
18. Degani S, Leibovitz Z, Shapiro I, Ohel G. Expectant management of pregnancy-related high-velocity uterine arteriovenous shunt diagnosed after abortion. Int J Gynaecol Obstet 2009 Jul;106(1):46–9.   [CrossRef]   [Pubmed]    
19. Peitsidis P, Manolakos E, Tsekoura V, Kreienberg R, Schwentner L. Uterine arteriovenous malformations induced after diagnostic curettage: a systematic review. Arch Gynecol Obstet 2011 Nov;284(5):1137–51.   [CrossRef]   [Pubmed]