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Wo m e n s I m a g i n g C l i n i c a l O b s e r v a t i o n s

Surapaneni and Silberzweig Hysterosalpingography After Cesarean Section Womens Imaging Clinical Observations

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W O M E N S IMAGING

Cesarean Section Scar Diverticulum: Appearance on Hysterosalpingography


OBJECTIVE . The purpose of this study was to characterize the frequency and appearance of hysterotomy defects on hysterosalpingography in patients with a history of cesarean section. materials AND METHODS . We reviewed the hysterosalpingograms of 150 wom en with a history of cesarean section. The incidence, location, and appearance of defects at the expected location of a hysterotomy scar were evaluated. RESULTS . Of the 148 patients with history of cesarean section and technically adequate hysterosalpingograms, 89 (60%) had defects that were in the expected location of a hystero tomy incision. Fifty-eight (65%) of the diverticula were focal outpouchings, and 31 (35%) were thin linear defects. Forty-eight (54%) of the diverticula were located at the lower uterine cavity, 32 (36%) at the uterine isthmus, and nine (10%) at the upper endocervical canal. CONCLUSION . A diverticulum at the lower uterine cavity, uterine isthmus, or upper endocervical canal is a common finding on hysterosalpingography in patients with a history of cesarean section. ysterosalpingography is a com monly performed examination in the evaluation of women with in fertility. As the rates of cesarean sections performed in the United States have increased over the past several decades [1], more women are undergoing hysterosalpin gography who have a history of cesarean sec tion. A defect within the lower uterine cavity in patients with a history of cesarean section has been described [2]. In this study, we evaluate the frequency and appearance of uterine cavity anatomic defects on hystero salpingography in patients with a history of cesarean section. Materials and Methods
Between March 2003 and May 2006, 3,739 patients were referred for diagnostic hystero salpingography. A study cohort of 150 women (mean age, 37 years; age range, 2747 years) was identified retrospectively to have undergone cesarean section before hystero salpingography. The patients were identified by means of a data base developed from an intake questionnaire admini stered to all patients undergoing hystero salpingo g raphy. Indications for hystero salpingog raphy referral included infertility (n = 148) and evaluation before reversal of tubal ligation (n = 2). Five patients with a history of cesarean section

Krishna Surapaneni1 James E. Silberzweig2


Surapaneni K, Silberzweig JE

Keywords: cesarean section, hysterosalpingography DOI:10.2214/AJR.07.2916 Received July 22, 2007; accepted after revision November 5, 2007.
1 Department of Radiology, Long Island College Hospital, Brooklyn, NY. 2 Department of Radiology, St. Lukes-Roosevelt Hospital Center, 1000 Tenth Ave., 4th Floor, New York, NY 10019. Address correspondence to J. E. Silberzweig (jsilberz@chpnet.org).

AJR 2008; 190:870874 0361803X/08/1904870 American Roentgen Ray Society

had undergone hystero salpingography twice and one patient, three times. Hystero salpingography was performed under fluoroscopy in an outpatient office setting typically between day 5 and day 11 of the menstrual cycle at least 24 hours after menses had ceased. Prophylactic antibiotics were prescribed at the discretion of the referring gynecologist. Prophy lactic antibiotics were otherwise not rou tinely prescribed unless the patient had a history of heart murmur that required subacute bacterial endo carditis (SBE) prophylaxis. The patients were routinely premedi cated with oral ibuprofen 600 mg before the procedure. A urine pregnancy test (QuickVue One-Step hCG Urine Test, Quidel) was performed imme diately before hysterosalpingography. Hysterosal pingography was performed in a standard fashion using sterile technique. The patient was placed in a lithotomy position and a vaginal speculum was inserted. After cleansing the external os with povidone-iodine solution, the cervical os was cannulated with a hystero salpingography balloon catheter (H/S Catheter, CooperSurgical; Silicone Balloon HSG Catheter, Cook; HSG & HyCoSy Catheter, Rocket Medical). A cervical tenaculum was not used. The balloon catheter was inflated within the endocervical canal or lower uterine cavity and contrast material injection was performed with C-arm fluoroscopic control (OEC 9800, GE Healthcare). Standard hystero salpingography was

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Hysterosalpingography After Cesarean Section


performed using iopromide (Ultravist-300 [300 mg I/mL], Bayer HealthCare). The balloon catheter was not routinely placed in the uterine cavity because it may prevent or obscure opacification of underlying pathology in the lower uterine segment. A combination of pulse fluoroscopy (eight frames per second) and continuous fluoroscopy was used with automated exposure control. Static image capture was achieved by use of the fluoro scopic last-image-hold feature. Images of early and maximal opacification of the uterine cavity, fallo pian tubes, and peritoneal contrast spillage were obtained. Oblique and craniocaudal C-arm angu lations were used to obtain an en face view of the uterine cavity and fallopian tubes and for detailed evaluation of any abnormal findings. Fluoroscopy was performed using a 33-cm field of view. Selective salpingography was performed in patients with proximal fallopian tube occlusion. A completion image was obtained after removal of the balloon catheter to assess for abnormalities in the lower uterine cavity and endocervical canal that may have been obscured by the presence of the balloon catheter. Selected static images were transferred to a PACS for review. Of the 150 patients with a history of cesarean section, two patients had inadequate contrast opacification of the isthmusendocervical canal during hysterosalpingography and were therefore excluded. The defects were categorized by location (lower uterine segment, uterine isthmus, upper endocervical canal), side (right, left, bilateral, small midline), and size. Defect size was cate gorized by the craniocaudal dimension of the defect: thin linear, small (< 5 mm), medium (59 mm), or large (> 9 mm). Measurements were made by using the electronic calipers on the PACS, with the hystero salpingo graphy catheter shaft width serving as a reference distance. This retrospective HIPAA-compliant study was performed after the institutional review board deemed the study exempt from review and not to require patient informed consent.

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46%), bilateral (n = 41, 46%), and midline (n = 7, 8%). One patient with a small triangularshaped outpouching defect had an associated prominence of the superior aspect of the defect resulting in narrowing at the uterine isthmus (Fig. 5). The appearance of the lower uterine cavity and endocervical canal in the six pa tients who had undergone multiple hysterosal pingography examinations did not change from initial to subsequent examinations. Discussion Hysterosalpingography is an important component in the diagnostic evaluation of the infertile woman. The number of hystero salpingography examinations performed has significantly increased in recent years, likely due to the trend for women delaying preg nancy until later in life and the popularity of technical advances achieved in reproductive medicine [2]. Cesarean section is the most commonly performed surgical procedure involving the uterus in the fertile women [1], with the low transverse incision being the most common type of uterine hysterotomy. In the interpre tation of a hysterosalpingogram, awareness of the appearance of the cesarean scar defect is important in avoiding misdiagnosing the scar for underlying pathology or normal vari ants such as prominent cervical glands, post myomectomy diverticulum, synechiae, and focal adenomyosis [2, 3]. Prominent cervical glands may appear as tubular symmetric structures that arise from both walls of the endocervical canal. The walls of the endocervical canal can either be smooth or corrugated in appearance, which represent the mucosal furrows known as pli cae palmatae. Cervical glands may vary in appearance according to the individual pa tient and the phase of the menstrual cycle. The characteristic appearance of cervical glands as small tubular structures arising from both cervical walls helps in differenti ating them from cesarean section scars. Postmyomectomy diverticula will general ly appear as small unilateral outpouching at the site of resection. Correlation with surgical history and location of the diverticula are dif ferentiating factors that help distinguish this from a cesarean section scar defect. Gartners duct cysts are remnants of the wolffian duct that fail to normally resorb in women. These ducts can be unilateral or bi lateral and are generally only seen if they communicate with the uterine cavity. They appear as long tubular structures that run

parallel to the uterine cavity and occasional ly can have a focal segment of saccular or cystic dilatation [3]. Visualization of a long contrast-filled tubular duct parallel to the uterus and possibly extending from a region of cystic dilatation is more characteristic of a Gartners duct cyst and allows differentiation from a cesarean scar diverticulum. Adenomyosis is a pathologic condition as sociated with ectopic endometrial extension into the myometrium. If the ectopic endome trial tissue communicates with the uterine cavity, adenomyosis can have the appearance of contrast-filled diverticula extending into the myometrium. Women with adenomyosis most often will present with pelvic pain, and generally these patients are diagnosed via sonography or MRI. Asymptomatic women evaluated for infertility may be incidentally diagnosed with adenomyosis on hysterosal pingography. Differentiating asymptomatic adenomyosis from a cesarean section scar will depend on location of the defect because the latter are confined to the lower uterine cavity endocervical canal, whereas adenomyosis can occur anywhere along the uterine cavity. TABLE 1: Uterine Anatomic Defects Secondary to Prior Cesarean Section
Parameter History of cesarean section (n = 148) Presence of defect in patients with history of cesarean section Absence of defect in patients with history of cesarean section Site of cesarean section diverticulum (n = 89) Lower uterine cavity Uterine isthmus Upper endocervical canal Side of cesarean section diverticulum (n = 89) Right-sided uterine defect Left-sided uterine defect Bilateral defect Small midline defect Appearance of cesarean section diverticulum (n = 89) Linear Small bulbous or triangular Medium bulbous Large bulbous 31 (35) 39 (44) 11 (12) 8 (9) 22 (25) 19 (21) 41 (46) 7 (8) 48 (54) 32 (36) 9 (10) 89 (60) 59 (40) No. (%)

Results Of the 148 patients with history of cesar ean section and technically adequate hystero salpingograms, 89 (60%) were found to have anatomic uterine defects that were in the ex pected location of a hysterotomy incision (Table 1). The diverticula appeared as focal outpouch ings (n = 58, 65%) (Figs. 13) and as thin linear defects (n = 31, 35%) (Fig. 4). The diverticula were located at the lower uterine segment (n = 48, 54%), at the uterine isthmus (n = 32, 36%), and at the upper endocervical canal (n = 9, 10%). The defects were unilateral (n = 41,

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Surapaneni and Silberzweig

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Fig. 1 Hysterosalpingogram in 40-year-old woman shows medium-sized cesarean section scar defect arising from left lower uterine cavity wall (arrow ).

Fig. 2 Hysterosalpingogram in 40-year-old woman shows large cesarean section scar defect at uterine isthmus (arrows ).

Fig. 3 Hysterosalpingogram in 43-year-old woman with anteverted uterus shows large cesarean section scar defect at upper endocervical canal (arrow ).

Fig. 4 Hysterosalpingogram in 37-year-old woman shows linear cesarean section scar defect at uterine isthmus (arrows ).

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Fig. 5 Hysterosalpingogram in 42-year-old woman with small defect in upper right endocervical canal with associated prominence of superior aspect of defect, resulting in narrowing at uterine isthmus (arrow ).

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Sixty percent of patients in our study with a history of cesarean section were found to have anatomic defects readily apparent on hystero salpingography. Ninety percent of these ce sarean section scar defects were located in the lower uterine cavity or uterine isthmus. The most common appearance of the defect was as a linear defect or small outpouching. Among patients with a small defect, one patient had an associated prominence of the superior as pect of the defect resulting in narrowing at the uterine isthmus that projected into the con trast-filled lumen (Fig. 5). This type of defect has been described as an overhang of con gested endometrium above the scar recess, which has been seen on histopathologic evalu ation of the cesarean scar [4]. A steep oblique or lateral view may be helpful in better defin ing this particular cesarean section scar be cause certain defects can be obscured on a frontal view. In comparison with hysterosalpingograph ic diagnosis of cesarean scar defects, Reg nard et al. [5] detected a similar rate of cesar ean section scars (57.5%) via saline contrast sonohysterography. One clear limitation of hysterosalpingography is the inability to pre cisely measure myometrial thickness and the size of the scar, both of which can be readily characterized via sonohysterography. Reg

nard et al. measured the residual myometri um within the defect and quantified the extent of thinning and classified the most severe de fects (those in which the depth was at least 80% of the anterior myometrium) as scar de hiscence [5]. In their series of 33 patients, they found a 6% rate of dehiscence, which is significantly higher than the reported rate of uterine rupture (0.4%) [5]. Coupled with the relatively common finding of a scar defect in patients with prior cesarean section (57.5%), it can be inferred that the mere presence of a defect is likely of little clinical significance unless myometrial thickness is quantified and dehiscence as defined by Regnard et al. [5] is identified. Further studies examin ing the relationship between myometrial thickness and long-term follow-up of these defects are warranted to assess the risks as sociated with severe myometrial thinning. The reason certain patients have anatomic defects after cesarean section while other pa tients do not is unclear. Fabres et al. [6] sug gested that the defect may be related to the suture material used, the suturing technique itself, or a combination of both. It is presumed that the most ischemic technique and slowest reabsorbable suture would be the worst com bination and thus likely to produce a cesarean scar defect. Accumulation of blood or mucous

in the scar may potentially obscure the defect on hysterosalpingography. The clinical significance of a cesarean section scar defect is most often benign, al though several authors have reported compli cations associated with the defect with re spect to the very rare ectopic scar pregnancy and as a potential cause of intermenstrual bleeding [612]. Pregnancy after prior ce sarean delivery requires attention during follow-up and subsequent pregnancy because of the potential risk of developing an ectopic pregnancy in the cesarean scar tissue and po tential uterine rupture during labor [79]. The presence of a cesarean section scar has been implicated as an underrecognized cause of abnormal uterine bleeding in pre menopausal women. Abnormal uterine bleeding is often associated with functional disorders of the menstrual cycle or intrauter ine abnormalities such as polyps, submucous myomas, and endometrial hyperplasia. In many instances, these abnormalities cannot be identified, and some authors have sug gested that the presence of a cesarean section scar is responsible [4]. Thurmond et al. [10] identified nine patients by sonohysterogra phy with abnormal uterine bleeding second ary to a cesarean section scar. Fabres et al. [6] examined 92 premenopausal patients with abnormal bleeding and found a high correlation on transvaginal sonography (with hysteroscopic correlation) between bleed ing disturbances and the presence of a cesarean section scar. In addition, they found that larger scars corresponded to heavier and longer bleed ing episodes. Menada Valenzano et al. [11] ex amined 217 women in a case-control study and found a significantly higher rate of abnormal uterine bleeding in patients who had a cesarean section versus vaginal delivery. In addition, they found a stronger correlation between ab normal intermenstrual bleeding and women who had cesarean sections 510 years prior than those whose surgeries were more recent. Thus, awareness of the presence of a cesarean section scar may help referring clinicians with diagnostic information that can elucidate the cause of abnormal uterine bleeding in pre menopausal women. One limitation of this study is the lack of follow-up of patients who were found to have

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Surapaneni and Silberzweig cesarean section scar defects. The retrospec tive nature of this study limited evaluation of prospective potential symptoms experienced by patients such as abnormal uterine bleed ing and problems associated with subsequent pregnancies. In the intake questionnaire ad ministered to all patients before hysterosal pingography, the patient was not asked to list current clinical symptoms, if present. In ad dition, the patient was not asked for the pre cise number of prior cesarean sections. With out knowing the number of prior cesarean sections a patient had undergone, we were unable to evaluate the relationship between the size of the defect and the number of prior cesarean sections. Waniorek [12] has shown that the severity of the scar is directly pro portional to the number of cesarean sections. Another limitation of this study was the lack of correlation between a cesarean scar de fect detected on hysterosalpingography with evidence for quantifiable myometrial thin ning. Further investigation correlating the hysterosalpingogram scar defect with fol low-up sonohysterography, MRI, or histo pathologic measurement of myometrial thickness is warranted. Hysterosalpingography is an important component in the evaluation of the infertile patient. To the best of our knowledge, this is the first large-scale characterization in the English-language literature of the incidence, location, and appearance of uterine scar de fects secondary to prior cesarean section on hysterosalpingography. Patients who have had a cesarean section will exhibit anatomic abnormalities in the lower uterine segment [9]. The presence and location of a cesarean section scar may rarely impact patient care with respect to potential uterine perforation during instrumentation and the rare occur rence of a cesarean scar ectopic pregnancy after in vitro fertilization. In addition, the presence of a cesarean section scar may rep resent a cause of abnormal uterine bleeding, a common gynecologic complaint. The clini cal significance of the scar in asymptomatic women is most likely benign, although fur ther investigation is needed to establish this. Thus, the presence of an anatomic uterine defect in patients with a history of cesarean section is a common, expected finding with a relatively typical appearance and location. References
1. Ecker JL, Frigoletto FD Jr. Cesarean delivery and the riskbenefit calculus. N Engl J Med 2007; 356:885888 2. Simpson WL, Beitia LG, Mester J. Hysterosalpin gography: a reemerging study. RadioGraphics 2006; 26:419431 3. Ubeda B, Paraira M, Alert E, Abuin RA. Hystero salpingography: spectrum of normal variants and nonpathologic findings. AJR 2001; 177:131135 4. Morris H. Surgical pathology of the lower uterine segment caesarean section scar: is the scar a source of clinical symptoms? Int J Gynecol Pathol 1995; 14:1620 5. Regnard C, Nosbusch M, Fellemans C, et al. Ce sarean section scar evaluation by saline contrast sonohysterography. Ultrasound Obstet Gynecol 2004; 23:289292 6. Fabres C, Aviles G, De La Jara C, et al. The ce sarean delivery scar pouch: clinical implications and diagnostic correlation between transvaginal sonography and hysteroscopy. J Ultrasound Med 2003; 22:695700 7. Jarvela IY, Sladkevicius P, Kelly S, Ojha K, Campbell S, Nargund G. Cesarean delivery scar. Ultrasound Obstet Gynecol 2002; 19:632633 8. Maymon R, Halperin R, Mendlovic S, et al. Ecto pic pregnancies in caesarean section scars: the 8 year experience of one medical centre. Hum Reprod 2004; 19:278284 9. Ash A, Smith A, Maxwell D. Caesarean scar pregnancy. BJOG 2007; 114:253263 10. Thurmond AS, Harvey WJ, Smith SS. Cesarean section scar as a cause of abnormal vaginal bleed ing: diagnosis by sonohysterography. J Ultrasound Med 1999; 18:1316 11. Menada Valenzano M, Lijoi D, Mistrangelo E, Costantini S, Ragni N. Vaginal ultrasonographic and hysterosonographic evaluation of the low transverse incision after caesarean section: corre lation with gynaecological symptoms. Gynecol Obstet Invest 2006; 61:216222 12. Waniorek A. Hysterography after cesarean section for evaluation of suturing technic. Obstet Gynecol 1967; 29:192199

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