Orientation of the Uterine Fundus in Reference ... - Wiley Online Library

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ORIGINAL RESEARCH

Orientation of the Uterine Fundus in Reference to the Longitudinal Axis of the Body A 3-Dimensional Sonographic Study Khaled Sakhel, MD, Elena Sinkovskaya, MD, PhD, Sharon Horton, RDMS, Hind Beydoun, PhD, Suneet P. Chauhan, MD, Alfred Z. Abuhamad, MD Video online at www.jultrasoundmed.org

Objectives—The aim of this pilot study was to measure the angle of rotation of the uterus at the fundus from horizontal using 3-dimensional sonography in women presenting for annual gynecologic examinations. Methods—A total of 51 patients participated in the study. All patients underwent transvaginal sonography, and 3-dimensional volumes were acquired. The cervicouterine angle and the angle of rotation at the fundus were measured. Results—The uteri were noted to be anteverted in 64.7%, retroverted in 25.5%, and euverted in 9.8%. They were noted to be pointing toward the right side of the pelvis in 49.0%, to the left side in 39.2%, and at the midline in 11.8%. The median cervicouterine angle was 122° (interquartile range [IQR], 105°–137°). The median angle of rotation at the fundus away from horizontal in either a clockwise or counterclockwise direction on the transverse B-plane was 10.4° (IQR, 7.1°–19.0°), with a maximal angle of 43°, and on the coronal C-plane, it was 10.0° (IQR, 3.0°–20.0°), with a maximal angle of 43°. Noneuverted uteri were more likely to be rotated at the fundus. Conclusions—Our study reveals that, contrary to traditional thinking, the uterus can be rotated at the fundus in relation to the body (z-axis) along the longitudinal axis of the cervical canal. Key Words—fundus; gynecologic ultrasound; intrauterine device; rotation, 3-dimensional sonography; uterus

Received May 1, 2013, from the Department of Obstetrics and Gynecology (K.S., E.S., S.H., S.P.C., A.Z.A.) and Graduate Program in Public Health (H.B.), Eastern Virginia Medical School, Norfolk, Virginia USA. Revision requested May 15, 2013. Revised manuscript accepted for publication June 11, 2013. Address correspondence to Khaled Sakhel, MD, Department of Obstetrics and Gynecology, Eastern Virginia Medical School, 825 Fairfax Ave, Suite 310, Norfolk, VA 23507 USA. E-mail: [email protected] Abbreviations

IQR, interquartile range; IUD, intrauterine device; 3D, 3-dimensional doi:10.7863/ultra.33.2.323

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ittle is known about the orientation of the fundus of the uterus in reference to the longitudinal axis of the body. Traditionally, the endometrial cavity is assumed to be in the horizontal position in relation to women’s bodies whenever blind procedures are performed in the uterus, such as intrauterine device (IUD) insertions, endometrial biopsies, and dilation and curettage. However, this assumption may not be true, and the fundus of the uterus may be rotated one way or another in relation to the horizontal plane (Figure 1). It has been shown that up to 17% of patients with IUDs in place have malpositioned IUDs (Figure 2).1 How and why IUDs become malpositioned is difficult to ascertain and could be multifactorial. However, if the uterus is rotated at the fundus, then blind deployment of the IUD in a horizontal fashion may, at least in theory, result in malpositioning.

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Sakhel et al—3D Sonographic Study of the Orientation of the Uterine Fundus

The uterus is a 3-dimensional (3D) organ that is suspended in the pelvic cavity by the ovarian, round, broad, cardinal, and uterosacral ligaments. The advent of 3D sonography has provided the capability to visualize the uterus from different anatomic planes.2 During 3D sonography, a volume of data is acquired and then displayed in the 3 orthogonal planes; midsagittal, transverse, and coronal. Although it provides valuable information on the normal and abnormal anatomic conditions of the uterus, 3D sonography can also show the spatial orientation of the uterus in relation to other pelvic organs. The aim of this pilot study was to measure the angle of rotation of the uterus at the fundus from horizontal using 3D sonography in women presenting for annual gynecologic examinations. Figure 1. Schematic showing transverse images of the uterus at the fundus. The endometrial cavity at the fundus is aligned horizontally (A), dextro-rotated (B), and levo-rotated (C).

Figure 2. Malpositioned IUD with one arm inside the myometrium (arrow).

Materials and Methods This prospective study received approval from the Institutional Review Board of Eastern Virginia Medical School. Between March 2010 and March 2011, patients who presented to the outpatient office for routine annual gynecologic health maintenance were invited to participate. Inclusion criteria included women aged 18 to 40 years with a normal uterus who were not pregnant and who were willing and able to undergo a transvaginal sonographic examination. The exclusion criteria included pregnancy at the time of the examination, a known history of large (>3 cm) fibroids, a known history of severe dyspareunia or the inability to tolerate transvaginal sonography, a history of a müllerian anomaly, and an IUD in place. The patients’ demographics were collected, including age, gravidity, parity, prior abdominal surgery, prior cesarean delivery, and last menstrual period. The patients underwent transvaginal gynecologic pelvic sonography with a Voluson E8 ultrasound system (GE Healthcare, Milwaukee, WI) using a 5–9-MHz transducer. One sonographer (S.H.) performed all of the sonographic examinations, and 1 physician (K.S.) rendered the volumes. The sonographic examinations were performed as follows. The patient was placed in the neutral supine lithotomy position on the examination table after voiding. The transvaginal probe was inserted into the vagina up to the level of the cervix and then withdrawn just slightly to avoid pressure on the cervix. The transvaginal probe was maintained with the reference point at the 12-o’clock position. Threedimensional volumes were acquired (Figure 3) and rendered using 4D View software (GE Healthcare) on static volume contrast imaging. Volumes were obtained with an Figure 3. The 3 orthogonal planes on 3D sonography.

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angle of acquisition of 120° and the acquisition box placed outside the lateral borders of the uterus. The uterine measurements, including length (from the serosa of the fundus to the external cervical os), height (serosa to serosa and perpendicular to the endometrial lining), and cervical length (from the inner os to the external os), were obtained on the sagittal A-plane. The cervicouterine angle was also measured on the sagittal plane (Figure 4). The uterine width (serosa to serosa) was measured on the transverse Bplane. The spatial orientation of the uterus was described in 3 dimensions. On the x-axis, the uterus was designated as pointing to the right, left, or middle. On the y-axis, it was designated as anteverted, retroverted, or euverted depending on how the uterine fundus was pointing in relation to the supine body. Then the rotation of the fundus of the uterus on the z-axis was measured. The angle of rotation at the fundus was measured by 2 methods. First it was measured on the transverse B-plane using the 3-point angle measurement (Figure 5) function of 4D View version 7.0 software. Then it was measured on the coronal C-plane image by z-rotating so the fundus was at the top of the image. Then, while the y-rotation funcFigure 4. Measurement of the cervicouterine angle.

Figure 5. Measurement of the uterine orientation angle on the transverse B-plane, revealing a counterclockwise rotation (arrow).


tion was held, the uterus was rotated around the y-axis clockwise or counterclockwise, obtaining the most optimal image showing both cornua, and the angle of the rotation was noted (Video 1). Descriptive and bivariate analyses were performed with SAS version 9.3 software (IBM Corporation, Chicago, IL). Summary statistics included interquartile ranges (IQRs) for continuous variables and percentages for categorical variables. Spearman rank correlation coefficients were calculated for the uterine length, angle of rotation at the fundus, and cervicouterine angle. The Kruskal-Wallis test was used to examine overall differences across groups, and pair-wise comparisons were performed with the Wilcoxon rank sum test. P < .05 was considered statistically significant.

Results The study was offered to 53 eligible women who met the inclusion criteria, and 51 consented to participate. The cohort’s demographics showed a median age of 27.0 years (IQR, 22–32 years); gravidity and parity were 2 (IQR, 0– 3) and 1 (IQR, 0–2), respectively (Table 1). The median uterine length, height, width, cervical length, and endometrial thickness are shown in Table 2. The uteri were noted to be anteverted in 64.7%, retroverted in 25.5%, and euverted in 9.8%. They were noted to be pointing toward the right side of the pelvis in 49.0%, to the left side in 39.2%, and at the midline in 11.8%. The median cervicouterine angle was 122° (IQR, 105°–137°). The median angle of rotation at the fundus away from horizontal in either a clockwise or counterclockwise direction on the transverse B-plane was 10.4° (IQR, 7.1°–19.0°), with a maximal angle of 43°, and on the coronal C-plane, it was 10.0° (IQR, 3.0°–20.0°), with a maximal angle of 43°. Measurement of the clockwise or counterclockwise angle of rotation at the fundus on B and C showed a statistically significant correlation (r = 0.74; P < .0001). The cohort was divided into 3 groups with respect to anteverted, retroverted, and euverted uteri (Table 3). The Kruskal-Wallis test was used to examine overall differences across the 3 groups. There was a significant difference in the mean angle of rotation at the fundus as measured on the B-plane (P = .01), which approached significance as measured on the C-plane (P = .06) across the 3 groups. When a pair-wise analysis was performed using the Wilcoxon rank sum test, there was no statistically significant difference in the mean angle of rotation at the fundus between anteverted and retroverted uteri as measured on B (P = .36) or C (P = .16). There was, however, a statisti-

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Table 1. Patient Demographics Median Age (IQR), y

Median Gravidity (IQR)

Median Parity (IQR)

Median BMI (IQR), kg/m2

Patients With Prior Abdominal Surgery, n (%)

Patients With Prior Cesarean, n (%)

Patients With Fibroids, n (%)

28 (22–33) 28 (25–30) 22 (22–22) 27.0 (22–32)

1 (1–4) 3 (1–3) 2 (1–2) 2 (0–3)

1 (0–2) 1 (1–2) 1 (1–2) 1 (0–2)

28 (24–33) 29 (21–37) 27 (26–31) 28.3 (23.5–33.6)

4 (7.8) 3 (5.8) 4 (7.8) 11 (21.6)

5 (9.8) 3 (5.8) 4 (7.8) 12 (23.5)

3 (5.8) 1 (1.9) 0 4 (7.8)

Uterus Anteverted Retroverted Euverted Total

BMI indicates body mass index.

cally significant difference in the mean angle of rotation at the fundus between anteverted and euverted uteri as measured on B (P = .01) but not C (P = .13). When retroverted uteri were compared to euverted uteri, there was also a significant difference in the mean angle of rotation at the fundus as measured on both B (P = .005) and C (P = .003). There was no correlation between the uterine length and the angle of rotation of the fundus or the cervicouterine angle (r = 0.04; P = .77; r = 0.17; P = .24, respectively). When the cohort was analyzed by the presence or absence of fibroids, there was no statistically significant difference in the angle of rotation at the fundus (Table 4).

Discussion The advent of 3D sonography as an imaging technique has introduced an enhanced understanding and appreciation of the spatial relationships of pelvic structures. In addition, structures that have been imaged in 2 dimensions have regained their 3D identity. The importance of this innovation in clinical practice is just unraveling1 and is especially true with respect to the uterus, which is involved in many procedures that are performed blindly. The goal of our pilot study was to look at the 3D configuration of the uterus especially at the fundus to see whether there could be rotation along the z-axis or along the longitudinal axis of the cervical canal. Table 2. Sonographic Measurements Measurement

Median (IQR)

Uterine length, cm Uterine height, cm Uterine width, cm Cervical length, cm Endometrial thickness, cm Cervicouterine angle, ° Mean ARF on B, ° Mean ARF on C, °

7.4 (6.9–8.9) 3.9 (3.3–4.4) 4.9 (4.6–5.6) 3.3 (3.0–3.8) 0.8 (0.4–1.0) 122 (105–137) 10.4 (7.1–19.0) 10.0 (3.0–20.0)

ARF indicates angle of rotation at the fundus.

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Office procedures involving the uterus have become commonplace. Such procedures include endometrial biopsy, dilation and curettage, and IUD placement. Intrauterine devices are a form of long-acting reversible contraception, which also includes contraceptive implants. Worldwide, IUDs are the most common form of reversible birth control, with 169 million users. Most IUD users (80%) are in Asia.3 In the United States, the proportion of IUD users increased from 1.3% in 2002 to 5.5% (2.1 million women) between 2006 and 2008.4,5 The American College of Obstetricians and Gynecologists has recently endorsed the use of long-acting reversible contraception, especially in adolescents.6 It is therefore likely that the trend of increased use of long-acting reversible contraception will continue to rise in the United States. Complications of IUDs include perforation, malpositioning, expulsion, abnormal uterine bleeding, and infection. Intrauterine device placement into the uterine cavity is a blind procedure. The clinician is blind to the fundal orientation of the uterine cavity with respect to the body Table 3. Uterine Angle of Rotation at the Fundus on the B- and CPlanes as a Function of the Position of the Uterus on the y-Axis Uterus Anteverted Retroverted Euverted Total

n (%)

Median ARF on B (IQR), °

Median ARF on C (IQR), °

33 (64.7) 13 (25.5) 5 (9.8) 51 (100)

14.0 (9.5–17.6) 14.0 (10.0–22.1) 0 (0.0–0.0) 10.4 (7.1–19.0)

10.0 (2.0–19.0) 14.0 (10.0–23.0) 2.0 (2.0–3.0) 10.0 (3.0–20.0)

ARF indicates angle of rotation at the fundus. Table 4. Uterine Angle of Rotation at the Fundus on the B- and CPlanes as a Function of the Presence or Absence of Uterine Fibroids Fibroids

n (%)

Median ARF on B (IQR), °

Median ARF on C (IQR), °

Presence Absence

4 (7.8) 47 (92.2)

10.0 (2.0–20.0) 16.5 (10.0–21.0)

10.2 (6.0–19.0) 16.5 (12.0–20.5)

ARF indicates angle of rotation at the fundus.




or the cervical canal. It has been traditionally assumed that the uterine cavity is in the neutral horizontal (9- to 3o’clock) position at the fundus (along the z-axis). The commonly cited textbook Comprehensive Gynecology7 does not actually have a section on the insertion technique for IUDs. Other gynecologic textbooks as well as the manufacturers’ instructions for insertion of IUDs only allude to knowledge of the position of the uterus (anteverted, retroverted, or straight) but do not mention the possibility of rotation at the fundus.8–12 The assumption here is that the uterus is in the neutral position with respect to the z-axis at the fundus; hence, loading of the IUD into the applicator is also in the neutral horizontal position. The product insert of one of the manufacturers goes as far as stating “Rotate the insertion tube so that the horizontal arms of the T and the long axis of the blue flange lie in the same horizontal plane. Now pass the loaded insertion tube through the cervical canal until (the IUD) just touches the fundus of the uterus. The blue flange should be at the cervix in the horizontal plane.”12 The arms of the IUD, once deployed, open into what is assumed to be the fundus of endometrial cavity, which lies in the neutral horizontal position on the z-axis. This assumption may be erroneous, and the cavity at the fundus may be dextro- or levo-rotated (on the z-axis) along the long axis of the cervical canal, in which case the deployed arms of the IUD may open into the myometrium. Malpositioning of IUDs within the uterus may cause impingement of one or both arms into the myometrium, rotation of the IUD within the cavity, or expulsion down into the cervix. The true rate of malpositioned IUDs in the general population is not known. However, a retrospective study by Benacerraf et al1 on patients who presented for sonography and who were noted to have an IUD in place revealed that 16.8% were malpositioned. The proportion of patients with malpositioned IUDs who had symptoms of either bleeding or pain was as great as 75%. Intrauterine devices may also be associated with complete perforations into the abdominopelvic cavity, with an incidence of approximately 1.3 per 1000 insertions,13 and can be found in the bowel, bladder, ovary, broad ligament, and omentum.14–16 A 4-country multicenter international retrospective study on the safety of levonorgestrel-releasing IUDs over 17 years revealed 701 perforations, with only 8.5% of cases recognized clinically immediately at the time of insertion.17 Intrauterine device expulsions are rare and have been estimated to occur in 3% to 5% of women, but the rate is higher in adolescents, ranging from 5% to 22%. Risk factors for expulsion include younger age, prior IUD expulsion, and nulliparity.18–20


Could IUD malpositioning, perforation, and expulsion be related to the initial insertion procedure and specifically to the 3D configuration of the uterus? A review of the literature (1956–2012) was done on the PubMed and MEDLINE PLUS Databases using the key words “uterine fundal rotation,” “uterine 3D rotation,” and “angle rotation uterine” showed that this study is the first that attempted to measure the angle of rotation at the fundus. Our study reveals that, contrary to traditional thinking, the uterus can be rotated at the fundus in relation to the body and along the longitudinal axis of the cervical canal. The median rotation from horizontal in the cohort was 10.0°, and the proportion of women with a uterine fundal rotation of at least 20° was 21.5%. The maximum angle of rotation noted in this cohort was 72°, which means that potentially if an IUD were to be placed in the traditional fashion, the arms would open directly into the myometrium. The median cervicouterine angle was 122°, since most of the uteri were anteverted. We theorized that it was possible that the longer the uterus, the greater the chance of rotation at the fundus. However, no such correlation was noted based on our study. What are the potential implications of such findings? First of all, this information can be used for future research on the 3D configuration of the uterus but especially for research involving IUD malpositioning. Whether knowledge of the angle of rotation at the fundus could help in the insertion of IUDs and whether this knowledge could decrease the risk of malpositioned IUDs are some questions that would require further studies. Ideally, a study with sufficient power can be designed to prospectively compare the angle of rotation at the fundus with the risk of malpositioned IUDs. In addition, our study found that whenever the uterus was in an anteverted or retroverted position, it was associated with more rotation at the fundus. It is not possible to state the clinical importance of such a finding. Perhaps, however, it may be inferred that noneuverted uterine positions may be at a higher risk of malpositioned IUDs. This information is also important for patients whose pelvic examinations are not adequate, such as those with central obesity, and the orientation of the uterus is not well assessed. The strengths of this study were its originality is using 3D sonographic manipulation to measure spatial orientation angles as well as establishment of a protocol for measurement of the angle of rotation at the fundus. This information could be used in future studies on the use of the angle of rotation at the fundus in procedures as well as the effects of the menstrual cycle, the use of the tenaculum, and preprocedure sonography on the risk of malpositioned IUDs.

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The limitations of this study included the fact that the patients were not all at the same time in their menstrual cycles. In addition, there may have been an interobserver difference in the measurement of the angle. Also, many questions remain unanswered, including whether application of the tenaculum alters the angle of rotation at the fundus. In addition, this study did not address whether sonography should be performed before or right after every IUD insertion, which should be answered by a prospective randomized trial. However, when patients are symptomatic, sonography should be performed to ensure proper placement. In conclusion, the uterus, being a 3D organ, may be rotated at the fundus, and knowledge of such a rotation may be vital to the safe and successful completion of procedures that involve the uterus.

9.

References

14.

1.

2.

3.

4.

5.

6.

7.

8.

328

Benacerraf BR, Shipp TD, Bromley B. Three-dimensional ultrasound detection of abnormally located intrauterine contraceptive devices which are a source of pelvic pain and abnormal bleeding. Ultrasound Obstet Gynecol 2009; 34:110–115. Sakhel K, Benson CB, Platt LD, Goldstein SR, Benacerraf BR. Begin with the basics: role of 3-dimensional sonography as a first-line imaging technique in the cost-effective evaluation of gynecologic pelvic disease. J Ultrasound Med 2013; 32:381–388. United Nations, Department of Economic and Social Affairs, Population Division. World contraceptive use 2010. United Nations website. http://www.un.org/esa/population/publications/wcu2010/WCP_20 10/Data.html. Accessed January 7, 2014. Centers for Disease Control and Prevention. Use of contraception in the United States, 1982–2008. Centers for Disease Control and Prevention website. http://www.cdc.gov/nchs/data/series/sr_23/sr23_029.pdf. Accessed November 23, 2011. American College of Obstetricians and Gynecologists. Long-acting reversible contraception: implants and intrauterine devices. ACOG Practice Bulletin No. 121. Obstet Gynecol 2011; 118:184–196. American College of Obstetricians and Gynecologists. Adolescents and long-acting reversible contraception: implants and intrauterine devices. ACOG Committee Opinion No. 539. Obstet Gynecol 2012; 120:983– 988. Mishell DR. Family planning. In: Katz VL, Lentz GM, Lobo RA, Gershenson DM (eds). Comprehensive Gynecology. 5th Ed. Philadelphia PA: Mosby Elsevier; 2007:275–326. Fritz MA, Speroff L. Intrauterine contraception. In: Clinical Gynecologic Endocrinology and Infertility. 8th ed. Philadelphia PA: Lippincott Williams &Wilkins; 2011:1095–1120.

10.

11.

12.

13.

15.

16. 17.

18. 19.

20.

Hoffman BL, Schorge JO, Schaffer JI, et al. Contraception and sterilization. In: Hoffman BL, Schorge JO, Schaffer JI, et al (eds). Williams Gynecology. 2 ed. New York, NY: McGraw-Hill; 2012. http://www.accessmedicine.com/content.aspx?aID=56694594. Accessed April 24, 2013. Kimble TD, Archer DF. Long-acting reversible contraception. In: Sakhel K, Lukban JC, Abuhamad AZ (eds). Practical Guide to Office Procedures in Gynecology and Urogynecology. New Delhi, India: Jaypee Bros; 2013:83–96. Bayer Healthcare. Highlights of prescribing information. Bayer Healthcare website. http://labeling.bayerhealthcare.com/html/products/pi/ Mirena_PI.pdf. Accessed April 19, 2013. ParaGard. ParaGard T 380A intrauterine copper contraceptive. ParaGard website. http://hcp.paragard.com/images/ParaGard_info.pdf. Accessed April 19, 2013. Van Houdenhoven K, Van Kaam KJAF, Van Grootheest AC, Salemans TH, Dunselman GA. Uterine perforation in women using a levonorgestrel-releasing intrauterine system. Contraception 2006; 73:257– 260. Rosenblatt R, Zakin D, Stern WZ, Kutcher R. Uterine perforation and embedding by intrauterine device: evaluation by US and hysterography. Radiology 1985; 157:765–770. Ozdemir H, Mahmutyazicioglu K, Tanriverdi H, Gundogdu S, Savranlar A, Ozer T. Migration of an intrauterine contraceptive device to the ovary. J Clin Ultrasound 2004; 32:91–94. Heinonen PK, Merikari M, Paavonen J. Uterine perforation by copper intrauterine device. Eur J Obstet Gynecol Reprod Biol 1984; 17:257–261. Van Grootheest K, Sachs B, Harrison-Woolrych M, Caduff-Janosa P, van Puijenbroek E. Uterine perforation with the levonorgestrel-releasing intrauterine device: analysis of reports from four national pharmacovigilance centres. Drug Saf 2011; 34:83–88. Deans EI, Grimes DA. Intrauterine devices for adolescents: a systematic review. Contraception 2009; 79:418–423. Lyus R, Lohr P, Prager S. Use of the Mirena LNG-IUS and Paragard Cu T 380A intrauterine devices in nulliparous women. Board of the Society of Family Planning. Contraception 2010; 81:367–371. Thonneau P, Almont T, de La Rochebrochard E, Maria B. Risk factors for IUD failure: results of a large multicentre case-control study. Hum Reprod 2006; 21:2612–2616.
