REVIEW ARTICLE |
https://doi.org/10.5005/jp-journals-10009-2003 |
Transvaginal Assessment of the Cervix
1,2Faculty of Medical Sciences, Goce Delchev University, Stip; IVF Centre, Re-Medika, Skopje, North Macedonia
Corresponding Author: Zorancho Petanovski, Faculty of Medical Sciences, Goce Delchev University, Stip; IVF Centre, Re-Medika, Skopje, North Macedonia, Phone: +38972443114, e-mail: zoranco.petanovski@ugd.edu.mk
Received: 17 July 2023; Accepted: 15 November 2023; Published on: 28 December 2023
ABSTRACT
Cervix is an important part of the uterus in obstetrics because that anatomical part withstands the pressure of the pregnant uterus until the moment of childbirth. Many mechanisms play a role in the beginning of labor, and it is fascinating how it is a harmonized mechanism. Unfortunately, under the influence of various factors, it leads to preterm labor (PTL) or preterm premature rupture of the fetal membranes (PPROM). Ultrasound is an ideal tool in detecting the status of the cervix during pregnancy. Vaginal ultrasound has shown better sensitivity and predictability than abdominal ultrasound. Regarding vaginal ultrasonography of the cervix in gynecology, recent studies show the effectiveness of vaginal ultrasound in the detection of cervical pathology. Not only in detection but transvaginal ultrasound (TVU), especially new techniques such as three-dimensional (3D) color Doppler, also helps clinicians in choosing the right therapeutic approach for malignant diseases of the cervix.
How to cite this article: Petanovski Z, Petanovska Kostova E. Transvaginal Assessment of the Cervix. Donald School J Ultrasound Obstet Gynecol 2023;17(4):309–316.
Source of support: Nil
Conflict of interest: None
Keywords: Cervical length, Color Doppler sonography, Funneling, Preterm labor, Preterm premature rupture of the fetal membranes, Sludge, Transvaginal ultrasonography
This paper is to be published as Zorancho Petanovski, Emilija Petanovska Kostova: Transvaginal assessment of the cervix. In: Asim Kurjak, Jose Bajo Arenas, Zorancho Petanovski. Donald School Textbook of Transvaginal Sonography, 4th edition. Jaypee Brothers, New Delhi, 2023.
INTRODUCTION
The cervix is the anatomical part of the uterus, the topographically distal part of the body of the uterus. Histologically, the cervix is composed of predominantly fibrous tissue, unlike the muscular tissue of the uterus. The endocervical canal runs from the internal ostium to the external ostium of the cervix. Transvaginal ultrasonography is a great tool in the hands of gynecologists in detecting pathology of the cervix, either in obstetrics or in gynecology. Measuring the length of the cervix and detecting its shortening is essential in the early diagnosis of possible preterm labor (PTL). On the other hand, pathology of the cervix in gynecology, such as inflammatory changes but also malignant changes, is increasingly evolving transvaginal ultrasonography as an initial diagnostic method.
OBSTETRICS
According to the World Health Organization, the definition of premature birth is when it occurs before 37 completed weeks of gestation. The problem of prematurity is very serious all over the world, namely prematurity significantly increases perinatal mortality and morbidity. Prematurity is a risk factor for more than half of neonatal deaths. Children born prematurely have a higher risk of developing pathologies in the neonatal period and in early childhood, such as vision problems, cerebral palsy, lung problems, and mental retardation.1 Factors for the risk of occurrence of premature birth are—the very young age of the pregnant woman, but also the age of the pregnant woman over 35 years old, socioeconomic conditions, and life habits.2
Bleeding during pregnancy, spontaneous rupture of the amniotic membranes, infections during pregnancy, infection due to chorioamnionitis, bacteriuria, current bacterial vaginosis, cervical insufficiency, uterine congenital anomalies, fibroids, previous excisional cervical treatment,3 multifetal gestation, fetal anomaly, and polyhydramnios, are risk factors for PTL.4
All this speaks of the importance of preventing the occurrence of PTL, that is, recognizing the risk factors for its occurrence and selecting pregnant women in the risk group for the occurrence of PTL.
The role of the cervix during pregnancy is to keep the distal part of the uterus closed, and in addition to the fact that the uterus grows enormously during pregnancy compared to the period before pregnancy. Under the influence of biochemical endogenous substances at the end of pregnancy, the cervix also changes its elasticity, becomes softer, and shortens its length. These changes are necessary for the next phase, which is the dilation of the cervix, the beginning of childbirth, which results in the birth of a new individual. In certain situations (infections during pregnancy are the most frequent), this process takes place even before the due date, and thus PTL occurs.
ULTRASOUND
Studies conclude that the shortening of the length of the cervix and its softening is a very important sign that indicates the risk of PTL. There are several explanations about the mechanism for the shortening of the cervix. One is the weakness of the cervix itself, that is, cervical insufficiency, which can be the result of trauma, surgical procedures, congenital anomalies, and/or weakness of the connective tissues of the cervix. It is difficult to detect cervical shortening in early pregnancy, except in some cases (surgical treatment, trauma, etc.), because by the 14th week of gestation, almost all women, even the most high-risk, have a normal cervical length (CL) in the first trimester.5
Second, another hypothesis is that a short CL is due to an inflammatory or infectious process as there is a strong association between a short CL on transvaginal ultrasound (TVU) and infection. Despite the fact that the shortening of the cervix is an indicator for PTL, the exposure of the membranes to ascending infection seems to be the crucial precipitating factor as even a short closed cervix with a length of <10 mm can result in a term pregnancy.6
The recent studies have shown that the majority of asymptomatic women with CL <25 mm before 24 weeks have some contractions, more than controls with a normal cervix. It is unclear whether contractions cause the short CL, are a result of the short cervix, or whether these two factors are working synergistically.5
Regarding the measurement of the length of the cervix by ultrasound, there are generally two approaches, and that is length measurement by abdominal ultrasound or endovaginal ultrasound. The negative side of abdominal ultrasound in measuring the length of the cervix is that the bladder often needs to be filled to obtain a good image resulting in elongation of the cervix, patient discomfort, and fetal parts can obscure the cervix, especially after 20 weeks, the distance from the probe to the cervix results in degraded image, especially in obesity patients, with sensitivity in the detection of PTL of 8.2%.7,8
Transvaginal ultrasound (TVU), in measuring the length of the cervix, is superior to transabdominal ultrasound and has a significantly higher sensitivity.8,9
Certain specifics in performing TVU are very important to avoid unnecessary mistakes. This technique is performed in the following situations—patient’s empty bladder, the transvaginal transducer is placed into the anterior fornix until the cervix is visualized while avoiding excessive pressure on the anterior cervical lip because excessive pressure resulting in mask of opening the internal os and elongate the cervix due to compression. A longitudinal view of the cervix should be obtained, and the image of the cervix needs to fill at least one-half of the ultrasound screens (Fig. 1). The amniotic fluid in the lower uterine segment is assessed, and then the lowest edge of the empty maternal bladder. It is very important to allow enough time for examination to view dynamic changes like uterine contractions, which can likewise mimic the appearance of funneling of the internal cervical os with a normal residual CL (Figs 2 and 3). Early pregnancy can cause difficulty in differentiation lower uterine segment from the endocervical canal because the gestational sac has not reached a sufficient size to completely expand the lower part of the uterus (Fig. 4).10
Fig. 1: Two-dimensional (2D) transvaginal view of the cervix and lower uterine segment; cervical canal length (blue xs) right position of external os (green xs); cervix (red arrow); fetal head (blue arrow); bladder (yellow arrow)
Fig. 2: Transvaginal ultrasound (TVU) in measuring the length of the cervix—curved cervix
Fig. 3: Transvaginal ultrasound (TVU) in measuring the length of the cervix—same case but excessive pressure on the anterior cervical lip resulting elongate the cervix due to compression
Fig. 4: Transvaginal ultrasound (TVU) in measuring the length of the cervix et early pregnancy—difficulty in differentiation lower uterine segment from the endocervical canal, because the gestational sac has not reached a sufficient size to completely expand the lower part of the uterus
In the sagittal section, the length of the cervix is measured longitudinally from the internal ostium to the external ostium of the cervical canal (Fig. 5). The situation of curved cervix is different. Then, the line of the cervical canal is measured from the internal ostium to the curve and then to the external canal, and the sum is taken as the final line (Fig. 6). This is often the case with long cervixes, while it is not the case with shortened ones, which are important in the assessment of PTL.10
Fig. 5: Transvaginal ultrasound (TVU) in measuring the length of the cervix in the sagittal section—the length of the cervix is measured longitudinally from the internal ostium to the external ostium of the cervical canal
Fig. 6: Transvaginal ultrasound (TVU) in measuring the length of the of curved cervix, the line of the cervical canal is measured from the internal ostium to the curve and then to the external canal and the sum is taken as the final line
The CL varies according to the gestational age. The median CL is 38.5 mm before 21 weeks vs 37–35 mm at 21–32 weeks vs 33 mm after 32 weeks of pregnancy.10,11
Measurement of CL by TVU is a good predictor of preterm birth. From a clinical point of view, a cutoff of <25 mm in the length of the cervix after 24 weeks of pregnancy is indicative of PTL. The greater the shortening of the length of the cervix, the greater the chances of developing PTL. Women with a CL of <25 mm and contractions have twice the incidence of PTL than women with a CL of <25 mm but no contractions.12,13
Regarding the measurement of the length of the cervix during pregnancy, the patients are divided into two groups—low-risk women are screened once at 18–24 weeks of gestation, and high-risk population usually begins screening at about 16 weeks of gestation, and the frequency depends on the measurement result and serial screening is effective in this population.14
FUNNELING
The definition of funneling is detected separation of the internal axis of the cervical canal. The funneling width >5 mm is a significant risk factor for adverse perinatal outcome. There are findings from the literature that funneling can be an early sign of cervical insufficiency.15,16
The role of vaginal ultrasound is to define the type and shape of cervical funneling in order to detect the risk of developing PTL. There are two forms of cervical funneling, V shape or U shape, taking into account that the T shape of the area between the endocervical zone and the uterine cavity is taken as a normal finding. The differences between these two types are that V-shaped funnel has a depth without significant width, unlike the U-shaped funnel, which has the width as an important parameter and represents almost complete endocervical effacement. U-shaped funneling has a higher risk of preterm delivery. However, when funneling is present with a normal residual CL, it is usually related to a contraction of the lower uterine segment and has little to no clinical significance (Figs 789).10,17
Fig. 7: Transvaginal ultrasound (TVU) of cervical funneling
Fig. 8: Transvaginal ultrasound (TVU) of cervical funneling—the U-shaped funnel has the width as an important parameter and represents almost complete endocervical effacement (yellow arrows)
Fig. 9: Transvaginal ultrasound (TVU) of cervical funneling—the U-shaped funnel and rest CL < 2.5 cm
SLUDGE
By definition, sludge is present of hyperechogenic material floating freely within the amniotic fluid near the cervix observed by vaginal ultrasound.18
It is considered that in the first half of pregnancy, the material that is detected comes from blood clots or inflammatory process (intraamniotic microbial biofilm has been proposed before), unlike the second half of pregnancy when the material can come from a maturational process (meconium, vernix).19,20
The intraamniotic sludge is related to unfavorable neonatal outcomes. That sludge is a risk marker for PTL, as well as an independent risk factor for high-risk patients, such as those with short cervix (Fig. 10).20
Fig. 10: Transvaginal ultrasound (TVU) of cervical sludge—the U-shaped funnel, sludge (green xs) and almost not visible rest CL
THE “MOON SIGN”
An orderly status of the cervix in the second trimester of pregnancy is a very important prerequisite for term labor. In contrast to this, the findings of cervical scarring and funneling is a risk factor for PTL and preterm premature rupture of the fetal membranes (PPROM); even about half of these patients will still deliver at term.21,22
The ultrasound finding of separation of the fetal membranes, that is, the finding that the fetal membranes do not descend into the funneling but remain at the level of the internal ostium, is a very important sign that shows the risk of PROM. This can be especially detected in large funnels in the form of funnels.22,23
The space between the cervix and the fetal membranes resembled a moon crescent, and the term “moon sign” describes the sonographic finding of localized fetal membrane separation in combination with U-shaped funneling of the cervix and shortened CL (Fig. 11).21,24
Fig. 11: Transvaginal ultrasound (TVU) of cervical “moon sign”—the space between the cervix and the fetal membranes resembled a moon crescent; fetal membranes (yellow arrow); funneling (red arrow)
Conclusion
Measuring the length of the cervix up to the 14th week of pregnancy does not have any special significance. After that transition, ultrasound findings of shortening of the cervix, funneling, and sludge bring the moon sign, and bring valid information about the risk of PROM and PTL.
GYNECOLOGY
Measurement and evaluation of the cervix in gynecology is not as frequent as in obstetrics. However, ultrasound can detect changes in the cervix even during the first examination. Detection of retention cysts on the cervix, that is, Ovula Nabothy nonneoplastic cystic lesions that occur in relation to the uterine cervix. The finding of nabothian cysts on the cervix is very frequent; around 12% are detected at the first examination. They are most often associated with chronic inflammation of the cervical canal. They are thought to form as a result of the healing process of chronic cervicitis and represent mucinous cysts due to obstruction from an overgrowth of squamous epithelium. The transformation zone of the cervix is in a continuous process of repair, and squamous metaplasia and inflammation may block a gland orifice.25
The transformation zone of the cervix is in a continuous process of repair, and squamous metaplasia and inflammation may block a gland orifice. On two-dimensional (2D) ultrasound, they appear as round hypoechoic formations, while three-dimensional (3D) ultrasound shows the exact topographic location, while 3D shows that there is no intracystic color Doppler finding, which is differentially diagnostic from other findings, primarily malignant changes of the cervix.
These cysts are usually small and asymptomatic, but in rare cases, they can reach the size of several centimeters and even have the appearance of a multicystic formation on the cervix. There is an association between nabothian cysts and infertility in women (Figs 12A1212D).26
Figs 12A to D: Three-dimensional (3D) TVU of cervical nabothian cyst (yellow arrows)
CERVICAL CANCER
According to the Global Cancer Statistics reports, cervical cancer ranks fourth both in terms of incidence and mortality. The most common cause is infection with the human papillomavirus with high-risk strains. This is a serious problem today, despite the fact that there is an established system for the prevention and early detection of cervical cancer [Papanicolaou (PAP)].27–29
Regarding the histology of cervical cancer, squamous cell carcinoma (SCC) and adenocarcinoma (AC) are the most common histological subtypes.30
The spread of cervical cancer is by lymphatic, hematogenous dissemination or direct extension. Preoperative diagnosis and spread status of cervical cancer are essential to choose the appropriate treatment.31
Vaginal or transrectal ultrasound detected different appearances in AC vs squamous cell cancer. Namely, in AC, the ultrasound image shows an isoechoic or hyperechoic pattern relative to the surrounding stroma, unlike SCC, where the image of the change is hypoechoic (Figs 13 and 14).32
Fig. 13: Transvaginal ultrasound (TVU) of cervical SCC—the image of the change is hypoechoic (yellow arrow)
Fig. 14: Transvaginal ultrasound (TVU) of cervical AC—the ultrasound image shows an isoechoic or hyperechoic pattern relative to the surrounding stroma (red arrow)
Some studies bring information that new techniques, especially 3D vaginal color Doppler, detect the difference in blood flow in normal women and in women with precancerous lesions or invasive cancers. The time of volume acquisition (FI), the number of vessels within the volume of interest (VI), and both blood flow and vascularization (VFI) were all significantly higher in the cervical precancerous and cancer lesions groups than in controls (p < 0.001).33,34
Tumor volume measurement is very important in assessing the staging and prognosis of patients with cervical cancer. 3D vaginal ultrasonography is dominant over the 2D technique. Tumor volume measurement of intratumoral vascularization showed that 3D Virtual Organ Computer-aided AnaLysis Power Doppler (VOCAL-PD) is superior to 2D ultrasound for calculating tumor volume and vascularization when the tumor is >2.5 cm and shows a complex vascularization in women with stage 1B1 cervical cancer.35
Detection of new angiogenesis and the amount of vessels within the tumor (scanty-moderate or abundant) is very important in the diagnosis, staging, and prognosis of cervical cancer. Tumors with abundant vascularization were significantly associated with parametrial involvement, lymph-vascular space involvement, pelvic lymph node metastases, etc. (Figs 15A and B).
Figs 15A and B: (A) Transvaginal 2D color Doppler ultrasound of cervical carcinoma—rich vascularization with linear, scanty-moderate vascular pattern of the blood vessels in SCC; (B) Rich vascularization with abundant vascular pattern of the blood vessels et AC
Three-dimensional (3D) color Doppler provides an excellent image of the vascular network of the tumor. It is interesting that this network of blood vessels is more linear in squamous carcinoma and translesional “water flow” sign in AC (Figs 16A and B, Figs 17A and B).36–38
Figs 16A and B: Transvaginal 3D power color Doppler ultrasound in SCC—rich vascularization with linear network of blood vessels
Figs 17A and B: Transvaginal 3D power color Doppler ultrasound of AC—rich vascularization with translesional “water flow” sign vascular pattern of the blood vessels
CONCLUSION
Ultrasound, particularly new techniques such as 3D/4D ultrasound and 3D/4D color Doppler, provide excellent insight into the pathology of the cervix. Preoperative examination provides useful data in terms of an adequate therapeutic approach in malignant diseases of the cervix.
REFERENCES
1. WHO: recommended definitions, terminology and format for statistical tables related to the perinatal period and use of a new certificate for cause of perinatal deaths. Modifications recommended by FIGO as amended October 14, 1976. Acta Obstet Gynecol Scand 1977;56(3):247–253. PMID: 560099
2. Caughey AB, 2007. Definition, incidence, significance and demographic characteristics of preterm birth. [online] UpToDate. Available from: http://www.uptodate.com/contents/demographicfactors-inpreterm-birth [Accessed June 2018].
3. Crane JM, Delaney T, Hutchens D. Transvaginal ultrasonography in the prediction of preterm birth after treatment for cervical intraepithelial neoplasia. Obstet Gynecol 2006;107(1):37–44. DOI: 10.1097/01.aog.0000192169.44775.76
4. Robinson JN, Norwitz E, 2007. Risk factors for preterm labor and delivery. [online] UpToDate. Available from: https://www.uptodate.com/contents/preterm-birth-risk-factors-and-interventions-for-riskreduction. [Accessed Jun 2018].
5. Mella MT, Berghella V. Prediction of preterm birth: cervical sonography. Semin Perinatol 2009;33(5):317–324. DOI: 10.1053/j.semperi.2009.06.007
6. O’Hara S, Zelesco M, Sun Z. Cervical length for predicting preterm birth and a comparison of ultrasonic measurement techniques. Australas J Ultrasound Med 2013;16(3):124–134. DOI: 10.1002/j.2205-0140.2013.tb00100.x
7. Hernandez-Andrade E, Romero R, Ahn H, et al. Transabdominal evaluation of uterine cervical length during pregnancy fails to identify a substantial number of women with a short cervix. J Matern Fetal Neonatal Med 2012;25(9):1682–1689. DOI: 10.3109/14767058.2012.657278
8. Hassan SS, Romero R, Berry SM, et al. Patients with an ultrasonographic cervical length < or =15 mM have nearly a 50% risk of early spontaneous preterm delivery. Am J Obstet Gynecol 2000;182(6):1458–1467. DOI: 10.1067/mob.2000.106851
9. Berghella V, Bega G, Tolosa JE, et al. Ultrasound assessment of the cervix. Clin Obstet Gynecol 2003;46(4):947–962. DOI: 10.1097/00003081-200312000-00026
10. Belics Z, Papp Z. Ultrasonographic assessment of the cervix for prediction of spontaneous preterm birth in singleton pregnancies. Donald School J Ultrasound Obstet Gynecol 2021;15(1):49–63. DOI: 10.5005/jp-journals-10009-1683
11. Greco E, Gupta R, Syngelaki A, et al. First-trimester screening for spontaneous preterm delivery with maternal characteristics and cervical length. Fetal Diagn Ther 2012;31(3):154–161. DOI: 10.1159/000335686
12. Chandiramani M, Shennan AH. Premature cervical change and the use of cervical cerclage. Fetal Matern Med Rev 2007;18(1):25–52. DOI: 10.1017/S0965539507001878
13. Romero R, Nicolaides K, Conde-Agudelo A, et al. Vaginal progesterone in women with an asymptomatic sonographic short cervix in the midtrimester decreases preterm delivery and neonatal morbidity: a systematic review and metaanalysis of individual patient data. Am J Obstet Gynecol 2012;206(2):124. e1–124.e19. DOI: 10.1016/j.ajog.2011.12.003
14. Conde-Agudelo A, Romero R. Predictive accuracy of changes in transvaginal sonographic cervical length over time for preterm birth: a systematic review and metaanalysis. Am J Obstet Gynecol 2015;213(6):789–801. DOI: 10.1016/j.ajog.2015.06.015
15. Podobnik M, Bulié M, Smiljanicé N, et al. Ultrasonography in the detection of cervical incompetency. J Clin Ultrasound 1988;13(6):383–391. DOI: 10.1002/jcu.1870160604
16. Michaels WH, Montgomery C, Karo J, et al. Ultrasound differentiation of the competent from the incompetent cervix: prevention of preterm delivery. Am J Obstet Gynecol 1986;154(3):537–546. DOI: 10.1016/0002-9378(86)90598-3
17. Berghella V, Owen J, MacPherson C, et al. Natural history of cervical funneling in women at high risk for spontaneous preterm birth. Obstet Gynecol 2007;109(4):863–869. DOI: 10.1097/01.AOG.0000258276.64005.ce
18. Buyuk GN, Oskovi-Kaplan ZA, Kahyaoglu S, et al. Echogenic particles in the amniotic fluid of term low-risk pregnant women: does it have a clinical significance? J Obstet Gynaecol 2021;41(7):1048–1052. DOI: 10.1080/01443615.2020.1834520
19. Ventura W, Nazario C, Ingar J, et al. Risk of impending preterm delivery associated with the presence of amniotic fluid sludge in women in preterm labor with intact membranes. Fetal Diagn Ther 2011;30(2):116–121. DOI: 10.1159/000325461
20. Romero R, Schaudinn C, Kusanovic JP, et al. Detection of a microbial biofilm in intraamniotic infection. Am J Obstet Gynecol 2008;198(1):135.e1–135.e5. DOI: 10.1016/j.ajog.2007.11.026
21. Rozenberg P, Gillet A, Ville Y. Transvaginal sonographic examination of the cervix in asymptomatic pregnant women: review of the literature. Ultrasound Obstet Gynecol 2002;19(3):302–311. DOI: 10.1046/j.1469-0705.2002.00645.x
22. Hartmann K, Thorp JM Jr, McDonald TL, et al. Cervical dimensions and risk of preterm birth: a prospective cohort study. Obstet Gynecol 1999;93(4):504–509. DOI: 10.1016/s0029-7844(98)00497-9
23. McLaren J, Taylor DJ, Bell SC. Increased concentration of pro-matrix metalloproteinase 9 in term fetal membranes overlying the cervix before labor: implications for membrane remodeling and rupture. Am J Obstet Gynecol 2000;182(2):409–416. DOI: 10.1016/s0002-9378(00)70232-8
24. Devlieger R, Scherjon SA, Oepkes D, et al. Ultrasound visualization of fetal membrane detachment at the uterine cervix: the ’moon sign’. Ultrasound Obstet Gynecol 2003;22(4):431–432. DOI: 10.1002/uog.234
25. Casey PM, Long ME, Marnach ML. Abnormal cervical appearance: what to do, when to worry? Mayo Clin Proc 2011;86(2):147–150; quiz 151. DOI: 10.4065/mcp.2010.0512
26. Katz VL, Lobo RA, Lentz G, et al. Compresive Gynecology, 5th edition. Philadelphia, PA: Mosby/Elsevier; 2007. pp. 437–438.
27. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018;68(6):394–424. DOI: 10.3322/caac.21492
28. Small W Jr, Bacon MA, Bajaj A, et al. Cervical cancer: a global health crisis. Cancer 2017;123(13):2404–2412. DOI: 10.1002/cncr.30667
29. Crosbie EJ, Einstein MH, Franceschi S, et al. Human papillomavirus and cervical cancer. Lancet 2013;382(9895):889–899. DOI: 10.1016/S0140-6736(13)60022-7
30. Cohen PA, Jhingran A, Oaknin A, et al. Cervical cancer. Lancet 2019;393(10167):169–182. DOI: 10.1016/S0140-6736(18)32470-X
31. Bhatla N, Aoki D, Sharma DN, et al. Cancer of the cervix uteri. Int J Gynaecol Obstet 2018;143(Suppl 2):22–36. DOI: 10.1002/ijgo.12611
32. Epstein E, Di Legge A, Måsbäck A, et al. Sonographic characteristics of squamous cell cancer and adenocarcinoma of the uterine cervix. Ultrasound Obstet Gynecol 2010;36(4):512–516. DOI: 10.1002/uog.7638
33. Belitsos P, Papoutsis D, Rodolakis A, et al. Three-dimensional power Doppler ultrasound for the study of cervical cancer and precancerous lesions. Ultrasound Obstet Gynecol 2012;40(5):576–581. DOI: 10.1002/uog.11134
34. Wang HR, Lin Y, Zhang XY, et al. Transvaginal color doppler sonography combined with colposcopy for diagnosis of early stage cervical cancer and precancerous lesions. J Biol Regul Homeost Agents 2018;32(1):123–126.
35. Daskalakis G, Diamantopoulos D, Theodora M, et al. 3D vocal power Doppler sonography for the estimation of tumor volume and vascularization in stage IB1 cervical cancer. Arch Gynecol Obstet 2018;298(3):617–222. DOI: 10.1007/s00404-018-4842-1
36. Petanovski Z, Medjedovic E, Kurjak A. 2023 Difficult cases in Obstetrics and Gynecology Text book od Jan Donald scool in press.
37. Pannain GD, Pereira AMG, Rocha MLTLFD, et al. Amniotic sludge and prematurity: systematic review and meta-analysis. Rev Bras Ginecol Obstet 2023;45(8):e489–e498. DOI: 10.1055/s-0043-1772189
38. Testa AC, Ferrandina G, Moro F. PRospective Imaging of CErvical cancer and neoadjuvant treatment (PRICE) study: role of ultrasound to predict partial response in locally advanced cervical cancer patients undergoing chemoradiation and radical surgery. Ultrasound Obstet Gynecol 2018;51(5):684–695. DOI: 10.1002/uog.17551
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