Uterus Contrast Enhancement Patterns at Ct and Mr Padrões De Captação De Contraste Do Útero Em Tc E Rm

ACTA RADIOLÓGICA PORTUGUESA Maio-Agosto 2015 nº 105 Volume XXVII 43-50

Artigo de Revisão / Review Article

UTERUS CONTRAST ENHANCEMENT PATTERNS AT CT AND MR PADRÕES DE CAPTAÇÃO DE CONTRASTE DO ÚTERO EM TC E RM

Marta Morna Palmeiro1, Teresa Margarida Cunha1

1 Department of Radiology, Instituto Português Abstract Resumo de Oncologia de Lisboa Francisco Gentil Head of Department: José Venâncio, MD Unlike ultrasound and magnetic resonance Ao contrário da ecografia e da ressonância imaging (MRI), computed tomography (CT) is magnética (RM), a tomografia computadorizada not generally indicated as the first line imaging (TC) não é uma técnica de primeira linha technique in the study of female pelvic pathology. no estudo da patologia pélvica feminina. However, CT is often used to evaluate non- Contudo, a TC é frequentemente utilizada na gynecological pelvic pathology, in the emergency avaliação de patologia pélvica não ginecológica, Corresponding Author Address department or in a follow-up context, in which nomeadamente em contexto de urgência ou de the pelvic organs are encompassed. In these seguimento, na qual os órgãos ginecológicos Marta Morna Palmeiro situations, the contrast enhancement pattern são englobados. Nestas situações, o padrão Rua Dr. Aquiles Machado, Nº7 2ºDto of the uterine body and cervix may be difficult de captação de contraste endovenoso pelo 2745-074 Queluz to interpret and may simulate pathology, given corpo e colo do útero na TC pode ser de difícil e-mail: [email protected] the wide spectrum of enhancement patterns, interpretação e por vezes simular patologia, dado anatomic variations and underlying pathology. o amplo espectro de padrões de captação de In this article the authors review and illustrate contraste endovenoso, de variantes anatómicas uterine CT and MRI contrast enhancement e/ou de patologia subjacente. Received: 22/06/2015 patterns and possible pitfalls, in order to facilitate Neste artigo as autoras revêm e ilustram os Acceptance: 26/10/2015 the differentiation of normal and pathological padrões de captação de contraste endovenoso aspects of the uterus in CT. pelo útero em TC e RM e possíveis pitfalls, permitindo diferenciar os aspectos normais e Key-words patológicos do útero em TC.

Uterine body; Uterine Cervix; Computed Palavras-chave Tomography; Magnetic Resonance Imaging. Corpo do Útero; Colo do Útero; Tomografia Computadorizada; Ressonância Magnética.

Introduction after intravenous administration of gadolinium3,6,7, however they are not always consistent with those observed on CT. Ultrasound is the first-line technique in the study of the female pelvis, given its easy access, reduced cost and the 1- Anatomical Fundamentals absence of ionizing radiation1. Magnetic resonance imaging is a complementary technique to ultrasound, essentially Vascularization of the uterus is mainly performed by the reserved for the study of indeterminate female pelvic lesions uterine arteries, branches of the anterior division of the on ultrasound or CT scan. CT is not recommended as a first- internal iliac arteries (Fig. 1). In the broad ligament, after line test in the assessment of the female pelvis, due to its low crossing the ureter, the uterine arteries penetrate the sensitivity and specificity, as well as the effects of ionizing myometrium at the isthmus level. Bilaterally, a branch of radiation on the reproductive organs. the uterine artery has an upward path in the myometrium, Pelvic CT is performed for the study of various non- and afterwards in the thickness of the broad ligament, gynecological indications, in which the uterus and adnexal reaching the ovarian hilum, where it anastomoses with 8 structures are encompassed. Familiarization with normal branches of the ipsilateral ovarian artery . The other branch radiological aspects of internal genitals in CT prevents of the uterine artery shows a downward path, irrigating the diagnostic errors and unnecessary exams. There is a broad cervix, where it anastomoses with branches of the vaginal spectrum of intravenous contrast enhancement patterns artery, forming the azygos arteries located in the anterior resulting from various factors that may sometimes mimic and posterior wall of the vagina. Thus, the cervix has a pathology2,3. Unlike most abdominal organs, which have double vascularization, through the uterine arteries and the already been characterized in different phases after intravenous vaginal arteries. contrast administration4,5, there are few studies on uterine Several tortuous branches of the uterine artery penetrate contrast enhancement patterns on CT. These uterine contrast into the thickness of the myometrium, dividing and enhancement patterns have already been characterized by MRI distributing themselves circumferentially to form the

43 Fallopian tube Uterus

Endometrium Ovary Ovarian artery Arcuate posterior Round ligament artery

Uterine artery Uterine artery Arcuate anterior Internal iliac artery Basal arterioles artery Miometrium Vaginal arteries

Figure 1 – Illustration of the uterine vasculature. The tortuous basal arterioles vascularize the endometrium, are derived from the anterior and posterior arcuate arteries and undergo cyclic changes during the menstrual cycle, with involution during the proliferative phase and grow during the secretory phase.

anterior and posterior arcuate arteries, which anastomose in the anterior and posterior midline with the contralateral branches, and give rise to arterioles that penetrate the endometrium9,10,11. The aforementioned anastomoses of the uterine arteries and their branches with the ovarian and * vaginal arteries allow a greater and alternative vascular supply of the uterus, associated with a lower risk for lesion with + reduction of blood supply. x Uterine arteries show a dynamic appearance, varying according to the phase of the menstrual cycle, increasing in length, caliber and tortuosity in the secretory phase and decreasing in the proliferative phase.

2 - Uterus Normal Contrast Enhancement Patterns at CT Uterine Body The morphology of the uterus is documented with better anatomical detail with MRI in the sequence T212,13, where it is possible to identify its three layers: the hyperintense endometrium, the junctional zone or hypointense Figure 2 – Sagittal pelvic MRI T2 intersecting the major axis of the endometrial cavity shows the different layers constituting the anatomy of the internal myometrium, and the external myometrium with uterine body: the hyperintense endometrium lining the endometrial cavity intermediate signal intensity (Fig. 2). The endometrium (+), the low signal from the junctional zone or normal inner myometrium varies in thickness depending on hormonal stimulation and (full arrow) and thickened (x) in the uterine wall by adenomyosis, and the menstrual cycle stage. The junctional zone differs from the intermediate signal from the external myometrium (asterisk). The signal external myometrium, by the presence of cells with larger difference between the normal junctional zone and the outer myometrium 14,15 result of higher smooth muscle cell density in the junctional zone. In nucleus and smaller cytoplasm , giving it a lower signal the cervix, four layers can be identified inside out: a central hyperintense intensity than the rest of the myometrium. The junctional zone consisting of mucus (dashed arrow); which is also surrounded by a zone should have a thickness between 2 and 8 mm. hyperintense zone, endocervix constituted by mucosal surfaces (triangle); Differentiation between the uterine layers also depends which in turn is surrounded by the inner layer fibromuscular hypointense cervical stroma, which continues upwardly to the junctional zone of the on the hormonal activity status16. In pre-menarche and uterine body; and more externally a intermediate intensity zone of the menopausal women, the uterus is small, with undifferentiated outer layer of fibromuscular cervical stroma which continues with the outer uterine regions, resulting from the reduced serum estrogen myometrium. levels. During pregnancy, the junctional zone becomes more hyperintense, reducing the differentiation of the uterine On CT without intravenous contrast, the uterus is uniformly layers characteristic of the non-pregnant uterus at fertile age. hypodense, with a slightly more hypodense central zone Six months after delivery it is again possible to identify the corresponding to the endometrium. usual anatomy and layers that constitute the uterus17. There is little published literature about uterus contrast The presentation of the uterus in the dynamic MRI study enhancement patterns on CT. Kaur et al12 reported three is variable and depends on the acquisition phase after types of intravenous uterine contrast enhancement patterns intravenous contrast administration. Usually, the myometrium on CT: type 1, thin or thick subendometrial enhancement is homogeneous and hyperintense in the arterial and venous with or without enhancement by the external myometrium, phase, while the endometrium enhances later and slowly, observed at 30 to 120 seconds, common at childbearing age showing hypointensity compared to the myometrium (Fig. 3). (Fig. 4-7); type 2, progressive enhancement of the external

44 Figure 3 – Sagittal MRI pelvic T2 (left image) and sagittal dynamic study after intravenous administration of gadolinium sagittal T1 with fat saturation at 30, 60 and 80 seconds (the second to fourth images, respectively) show the normal presentation of the body and cervix. Throughout the dynamic study, the myometrium is presented hyperintense, while the endometrium and junctional zone, which have relatively hypointense at 30 and 60 seconds, show progressive enhancement over time. The endocervix enhances quickly, while the cervical stroma enhances gradually.

Type 1 Enhancement Pattern The etiologies of this diversity of intravenous contrast enhancement patterns by the uterus remain to be determined; however, age, menstrual status and parity are possible conditioning factors. Kaur et al. established the following explanations for uterine enhancement patterns: type 1, the thin layer of subendometrial enhancement could correspond to the junction of the basal Fine subendometrial Thick subendometrial Subendometrial and outer layer of the endometrium with the adjacent myometrium, myometrium and the thick layer of subendometrial enhancement would Type 2 Enhancement Type 3 Enhancement consist of the junctional zone18. The type 2 enhancement Pattern Pattern pattern may be related to myometrial vascularization, which is hyperintense in T2 MRI, corresponding to the higher number of smooth muscle cells and abundant microcirculation2. The slight to moderate type 3 enhancement pattern, may be related to decreased muscle mass and atheromatous changes2. CT shows a low sensitivity in the assessment of endometrial Diffuse myometrial Light diffuse myometrial Diffuse heterogeneous thickness, frequently overestimating it, being a common 19,20 and myometrial indication for complementary evaluation by ultrasound . Figure 4 – Illustration of uterine enhancement patterns of intravenous The differential diagnosis of endometrial changes is difficult contrast CT. by CT, namely late endometrial enhancement with non-pure fluid in the endometrial cavity, pyometra or hematometra19. myometrium with homogenization of all myometrium or diffuse enhancement, without subendometrial enhancement, Uterine Cervix observed during fertile age and menopause (Figures 4 and MR T2-weighted images allows to distinguish with good 8); and type 3, mild and diffuse enhancement, essentially resolution and detail the four layers that make up the visualized at menopause (Figures 4 and 9). Kaur et al. also cervix: the central zone of the cervix with mucus that is verified that type 1 enhancement was transient and had hyperintense; the endocervix with its mucous folds which diffuse enhancement of the myometrium in the late phases. is also hyperintense; the inner fibromuscular layer of the Yitta et al.13 described a fourth heterogeneous and multifocal hypointense stroma, which is in continuity with the junctional enhancement pattern of the entire myometrium (Fig. 4 and zone of the uterine body; and the external muscular layer of 10). the stroma of intermediate intensity, which continues with

Figure 5 – Follow-up CT of a patient with a history of cutaneous lymphoma. Axial plane (a) and sagittal plane reconstruction (b) in portal venous phase (70 seconds) show a standard subendometrial enhancement pattern type 1, with fine linear contrast enhancement by myometrium (arrows) externally delimiting the endometrial cavity (asterisk).

45 Figure 6 – Resectability assessment CT for a mixed left adnexal tumor in a 41-year-old patient. Axial plane (a) and coronal plane reconstruction (b) obtained at portal venous phase (70 seconds) show a standard enhancement pattern type 1 thick subendometrial pattern, with enhancing myometrium contrast band (arrows) externally delineating the endometrium (asterisk). (a) shows a left retro-uterine adnexal tumor surpassing the midline (T), the right ovary (O) unchanged.

Figure 7 – Entero-CT of a 51-years-old patient with a suspected inflammatory small bowel disease. Axial plane (a) and sagittal (b) and coronal (c) reconstructions obtained at portal venous phase (for 45 seconds), show a standard type 1 capture with contrast uptake in thin subendometrial band delimiting the endometrial cavity (arrow) representative of the junctional zone and a thin outer peripheral uptake subserosal myometrium (triangle) delineating internal serosa.

Figure 8 – Pelvic CT in the initial evaluation of an adnexal right lesion (T) of a 49-years-old patient. Sagittal (a) and coronal reconstructions (b) obtained at portal venous phase (70 seconds) show a standard enhancement pattern type 2 with normal diffuse uptake of contrast by myometrium. (B) Bladder.

Figure 9 – Follow-up CT of a 89-years-old patient with history of malignant cutaneous melanoma. Axial plane (a) and sagittal plane reconstruction (b), at portal venous phase (70 seconds), show a standard enhancement pattern type 3, with mild, diffuse and homogeneous uptake of myometrium by contrast, limiting the endometrial cavity (asterisk).

46 Figure 10 – Follow-up CT of a 55-years-old patient with a history of cutaneous malignant melanoma. Axial (a), sagittal (b) and coronal (c) plane reconstructions at portal venous phase (70 seconds), show an heterogeneous and diffuse myometrial enhancement pattern, being more difficult to distinguish the endometrial cavity (asterisk) from the adjacent myometrium. the external myometrium (Fig. 2)6,7,21. On dynamic MRI the endocervix presents a fast enhancement, as opposed to the patterns by the uterus may be identified in different vascular gradually enhancing cervical stroma (Fig. 3)21,22. phases on the same CT scan2, and may initially present As the uterine body, the CT contrast enhancement patterns a type 1 pattern and in a late phase a type 2 pattern. The of the uterine cervix are identical to those seen on MRI. enhancement pattern may also be diffuse at an early stage A stratified enhancement pattern of the cervix layers is and present a washout in a late phase. Anatomic variants and observed in the uterine body enhancement patterns 1 and vascular variations, may contribute to the different types of 2 at CT, but not in type 3 pattern2. The cervix stratified uterine enhancement. More studies are necessary to better enhancement pattern at CT is typically characterized by characterize these factors on uterus contrast enhancement low intense enhancement in the fibromuscular stroma patterns at CT. surrounding an intense circumferential central enhancement (probably related to the central predominance of mucous glands)2. The external fibromuscular layer of the stroma exhibits a stronger contrast enhancement than the inner fibromuscular layer, but less distinct than the central cervical mucosal layer. This contrast enhancement pattern at CT gives a target morphology on axial images (Fig. 11). The lesser enhancement of the internal fibromuscular layer of the stroma can be justified by the greater number of fibroblasts and muscle cells, which may be responsible for their relative hypodensity compared to the external layer21,22. The cervix presents a diffusely lower contrast enhancement compared to the uterine body (Fig. 12), establishing a well- defined and regular boundary between the two, which may be due to the greater amount of fibrous tissue in the cervix.

2.1 - Factors Influencing the Contrast Enhancement Figure 11 – Follow-up CT of a 52-years-old patient with history of Patterns of the Uterus at CT cutaneous malignant melanoma. Axial plane at portal venous phase (70 seconds), shows normal cervix enhancement pattern, with a target Technical factors and specificities of the examinee may morphology resulting from the inner circumferential intense enhancement of the cervical mucosa (arrow) surrounded by a less intense contrast contribute to this variety of uterus enhancement patterns enhancement of the inner fibromuscular stromal layer (asterisk), followed at CT. The rate of administration of intravenous contrast by a layer of higher uptake corresponding to the outer fibromuscular layer and cardiac output may influence the uterine body and cervix of the cervical stroma (triangle). enhancement patterns. Different contrast enhancement

Figure 12 – Follow-up CT of a 28-years-old patient with a diagnosis of Burkitt Lymphoma. Sagittal (a) and coronal (b) portal venous phase (70 seconds) acquisition, show diffuse and uniform enhancement of the myometrium, type 2, and different uptake by intravenous contrast body (M) and cervix (C) of the uterus, resulting in a well defined and regular line (arrow) between these two uterine segments. Dynamic MRI study after intravenous administration of gadolinium in the sagittal plane (c) of another patient shows different enhancement between the body of the uterus (M), which enhances light and diffusely, and the cervix (C), which enhances homogeneously and less intensely than the body.

47 3 - Pathological Patterns of Uterus Contrast myometrium corresponding to the junctional zone, and Enhancement at CT myometrial cysts with a diameter of less than 1 cm (Fig. 13).

Nabothian Cysts Infection Nabothian cysts are benign and correspond to retention cysts Cervicitis is a clinical diagnosis; however, radiological of the cervix, probably resulting from chronic inflammation. findings at CT, such as enlargement of the cervix, parametria They are frequently asymptomatic and accidentally detected densification, prominence of vascularization, increased at CT3,23. They are well-defined lesions of variable size, cervical contrast enhancement23,25, mucosal irregularities with water density, showing no contrast enhancement and the presence of gas bubbles (Fig. 14), may suggest its or peripheral or ring enhancement3. Agglomerates may diagnosis. Findings of infection extension, such as rectal wall occur. In the axial CT images, they can sometimes simulate thickening and enhancement, or other aspects visualized in distension of the cervical canal filled with liquid, but in the pelvic inflammatory disease, may also help in the diagnosis23. sagittal and coronal planes they appear as well defined cystic lesions and distinct from the cervical canal, which presents Malignancy intense enhancement3. Uterine cervix may simulate pathology at CT due to its orientation and its different contrast enhancement compared Adenomyosis to the body of the uterus. The evaluation of sagittal and Adenomyosis is a benign and relatively common entity in coronal reformatting often helps in the interpretation of which there is ectopic endometrial tissue in the myometrium, these findings26. Identification of the cervical canal and affecting women at reproductive age. At CT with intravenous its continuity with the endometrium can be very useful in contrast, adenomyosis may present heterogeneous the identification of normal cervix, as well as the presence enhancement mimicking a uterus after delivery. Wood led of a well-defined line limiting the myometrium with et al24 described the radiological characteristics adenomyosis marked contrast enhancement as opposed to the lower at CT, which are: enlarged uterus, thickening of the inner enhancement of the cervix. The cervical canal must not be

Figure 13 – CT of a 58-years-old patient recently diagnosed with a follicular lymphoma. Sagittal plane reconstruction (a) at portal venous phase (70 seconds), shows an enlarged uterus with the uterine fundus located above the promontory of sacrum, showing thickening of the junctional zone (J) and myometrial cysts (arrow). These findings were confirmed by ultrasound with transvaginal approach, where the identified feature presentation “rain shower” (b) aspects consistent with adenomyosis, leiomyoma is documenting even earlier intramural.

a b c

Figure 14 – Acute cervicitis in a 45-years-old woman with a diagnosis of Crohn’s disease and complaints of vaginal discharge. CT performed in portal venous phase (70 seconds), at axial plane (a) and the reconstructions in the sagittal (b) and coronal (c), show increased dimensions of the cervix (C), de- monstrating increased uptake of contrast, difficult individualization of endocervix, with decreased density difference from the myometrium (M) and of the line attenuation delimiting the neck and body of the uterus, associated with the densification of the surrounding fat planes (arrow ) and bilateral hydrosal- pinx (asterisk). 48 erased nor obliterated. A lesion of the cervix can obliterate the cervical canal and result in distension of the endometrial cavity. The subendometrial type 1 enhancement pattern may simulate endometrial pathology, when the radiologist is not familiar with the uterus enhancement patterns at CT. The interruption or irregularity of the uniform enhancement of the sub-endometrial region, the presence of myometrial or cervical invasion, or endometrial cavity dilatation (Figure 15 and 16), suggest underlying pathology.

Iatrogenic Patients subject to previous pelvic radiotherapy due to urogenital, digestive or other carcinomas may have atrophy of the external cervical os, more common in the menopausal phase, conditioning accumulation of contents and distension of the cervical canal and upstream endometrial cavity (Fig. 17), which can simulate pathology. The correct diagnosis is made with the clinical history.

Figure 15 – Cervical squamous cell carcinoma of a 42-years-old woman. Uterus After Childbirth CT axial plane in the portal venous phase (at 70 seconds) shows loss of CT can be used after childbirth, particularly in the study normal contrast uptake by the cervix (usually homogeneous and smaller in of unexplained fever and unspecific abdominal pain. The relation to the endometrium), as well as loss of the regular uptake of the postpartum uterus may simulate pathology, and the clinical endocervix, visualizing uptake (complete arrow), with loss of the regular line delimiting the hypodensity of the uterine cervix and the hyperdensity history as well as familiarization with the tomographic of the uterine body (incomplete arrow), and the presence of irregular and features of the uterus after delivery may guide towards the ill-defined endocervix.

Figure 16 – Mixed endometrial adenocarcinoma of the endometrioid and serous nature in 74-years-old woman. Sagittal (a) and coronal (b) CT reconstructions performed in the portal venous phase (at 70 seconds), show the homogenous and diffuse (asterisk) type 2 myometrial uptake pattern, interrupted in the posterior slope and on the left side of the uterine body and fundus by a tumor with soft tissue density and irregular borders (arrows), which invades the myometrium at this level. This tumor also extends to the endocervix and cervical stroma (triangle).

Figure 17 – Status after neoadjuvant chemoradiotherapy and surgery for a rectal carcinoma in a 73-years-old woman. CT performed in the portal venous phase (at 70 seconds) with reconstruction in the sagittal plane (a) and in the axial plane (b), show distension of the cervical canal (C) with water density, as well as less accentuated distension of endometrial cavity (asterisk), resulting from iatrogenic atrophy of the external os of the cervical canal (arrow) to radiogenic therapy. The radiological aspects favoring this diagnosis are the presence of vaginal air (triangle) immediately downstream to the external orifice of the cervical canal and the enhancement of the cervical mucosa that covers the cystic “structure”, as well as the clinical history. CT findings were confirmed by ultrasound (c).

49 correct diagnosis. Typically, the postpartum uterus is enlarged, Endometrial evaluation at CT should be performed in sagittal with a distended endometrial cavity for approximately 6 to 8 reconstructions19,20,25. weeks. The site of placenta implantation may demonstrate defects of the myometrium and increased contrast Conclusion enhancement. Prominent vessels may also be visualized in myometrial thickness. The hysterotomy scar may be irregular CT is a technique with low diagnostic acuity in uterine and hypodense, with lower contrast enhancement than the evaluation, however the uterus is frequently evaluated on adjacent myometrium. The presence of intrauterine air may CT performed for non-gynecological indications. Thus, be a normal finding in the first weeks after delivery, even in it is important to be familiar with the different forms the absence of infection27. Intrauterine clots are also likely to of presentation of the uterus in this method, which are occur in the immediate postpartum period28. The presence sometimes difficult to interpret. of intraperitoneal air is normal after a caesarean section, The uterine body and cervix present dynamic and diversified however it is pathological in a vaginal delivery. enhancement pattern at CT, depending on several factors, such as age, menstrual status and acquisition phase. 4 - Pitfalls In the presence of morphological alterations or atypical contrast enhancement of the uterus at CT, a directed study Endometrial thickness can easily be exaggerated in axial and by ultrasound or MRI should be suggested, since these are coronal at CT images, especially when the uterus is positioned the election techniques in the evaluation of internal genital in anteversion or retroversion, in which the endometrium organs. presents an oblique orientation and is often overestimated.

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