Junctional Zone in Infertile Women: A Three-dimensional Ultrasound Study

Abstract

Objective To analyze the interobserver and intraobserver reproducibility of the visualization and continuity of the juncional zone (JZ) by three-dimensional (3D) ultrasound in infertile women, and to evaluate the sociodemographic, hormonal, and structural factors that influence these assessments.

Methods A prospective study conducted at the Assisted Reproductive Technology Unit of Hospital Senhora da Oliveira, in the city of Guimarães, Portugal. Transvaginal 3D ultrasonography was performed, and 2 volumes were generated per case. Two observers who were blinded to each other's work analyzed these volumes, choosing the best coronal section. Four months later, one of the observers performed the same methodology. The JZ visualization was classified as optimal, satisfactory, and unsatisfactory, and the JZ continuity, as continuous and discontinuous. The interobserver and intraobserver agreements were analyzed. The influence of hormonal, structural, and sociodemographic factors on the JZ was evaluated.

Results In total, 65 women were included in the present study. The interobserver reproducibility was substantial for JZ visualization and continuity (k = 0.635 and 0.753 respectively), and the intraobserver reproducibility was very good for JZ visualization and continuity (k = 0.884 and 0.816 respectively). Trilaminar endometrial pattern was associated with optimal JZ visualization (p = 0.012). The increase of 1 unit in the level of serum estradiol represents a 9.9% decrease in the odds of unsatisfactory visualization of the JZ (odds ratio [OR] = 0.9; 95% confidence interval [95%CI] = 0.814–0.996; p = 0.042). Endometriosis increases the odds of unsatisfactory visualization by 24 times (OR = 23.7; 95%CI = 1.262–437.057; p = 0.034). The prevalence of discontinuous JZs was of 60%. Myomas and endometriosis were associated with discontinuous JZs (p = 0.034 and 0.016 respectively).

Conclusion The assessment of JZ visualization and continuity by 3D ultrasound is reproducible enough to be used in the clinical practice.

Resumo

Objetivo Analisar a reprodutibilidade inter e intraobservador da visualização e continuidade da zona juncional (ZJ) por ecografia tridimensional (3D) em mulheres inférteis, e avaliar os fatores sociodemográficos, hormonais e estruturais que afetam essas avaliações.

Métodos Um estudo prospectivo conduzido no Centro de Procriação Medicamente Assistida do Hospital Senhora da Oliveira, em Guimarães, Portugal. Foi realizada ecografia transvaginal 3D e gerados 2 volumes por caso. Dois observadores, cegos às avaliações um do outro, analisaram os volumes obtidos e escolheram o melhor corte coronal. Após quatro meses, a mesma análise foi realizada por um dos observadores. A visualização da ZJ foi classificada como ótima, satisfatória e não satisfatória, e a continuidade, como contínua ou descontínua. Foram avaliadas as reprodutibilidades inter e intraobservador. A influência de fatores sociodemográficos, hormonais e estruturais na ZJ foi analisada.

Resultados No total, 65 mulheres foram incluídas no presente estudo. A reprodutibilidade interobservador foi substancial para a visualização e continuidade da ZJ (k = 0,635 e 0,753, respetivamente). A reprodutibilidade intraobservador foi muito boa para a visualização e continuidade da ZJ (k = 0,884 e 0,816, respetivamente). Endométrio trilaminar associou-se à visualização ótima da ZJ (p = 0.012). O aumento de 1 unidade no nível de estradiol diminuiu a chance de visualização não satisfatória da ZJ em 9,9% (razão de probabilidades [RP] = 0,9; intervalo de confiança de 95% [CI95%] = 0,814–0,996; p = 0,042). Endometriose aumentou a chance de visualização não satisfatória da ZJ em 24 vezes (RP = 23,7; CI95% =  1,262–437,057; p = 0,034). A prevalência de ZJs descontínuas foi de 60%. Miomas e endometriose associaram-se a ZJs descontínuas (p = 0,034 e 0,016, respetivamente).

Conclusão A avaliação da visualização e continuidade da ZJ por ecografia 3D é reprodutível, podendo ser utilizada na prática clínica.

Keywords

3D ultrasound - junctional zone - reproducibility - infertility - associated factors

Palavras-chave

ecografia 3D - zona juncional - reprodutibilidade - infertilidade - factores associados

Contributions

Vanessa Silva and Flávia Ramos participated in the study design, collection, analysis, and interpretation of data, writing of the article and critical review of the intellectual content. Filipa Brás, Ricardo Santos and Sofia Dantas participated in the participant recruitment, interpretation of data, and writing of the article. Rui Miguelote participated in the study design, participant recruitment, orientation, and critical review of intellectual content. All authors have read and approved the final version of the manuscript to be published.

• References

• 1 Saravelos SH, Jayaprakasan K, Ojha K, Li TC. Assessment of the uterus with three-dimensional ultrasound in women undergoing ART. Hum Reprod Update 2017; 23 (02) 188-210 . Doi: 10.1093/humupd/dmw040
• 2 Kashgari F, Oraif A, Bajouh O. The uterine junctional zone. Life Sci J 2015; 12 (12) 101-106
• 3 Brosens I, Derwig I, Brosens J, Fusi L, Benagiano G, Pijnenborg R. The enigmatic uterine junctional zone: the missing link between reproductive disorders and major obstetrical disorders?. Hum Reprod 2010; 25 (03) 569-574 . Doi: 10.1093/humrep/dep474
• 4 Lesny P, Killick SR. The junctional zone of the uterus and its contractions. BJOG 2004; 111 (11) 1182-1189 . Doi: 10.1111/j.1471-0528.2004.00350.x
• 5 de Vries K, Lyons EA, Ballard G, Levi CS, Lindsay DJ. Contractions of the inner third of the myometrium. Am J Obstet Gynecol 1990; 162 (03) 679-682 . Doi: 10.1016/0002-9378(90)90983-e
• 6 Ijland MM, Evers JL, Dunselman GA, van Katwijk C, Lo CR, Hoogland HJ. Endometrial wavelike movements during the menstrual cycle. Fertil Steril 1996; 65 (04) 746-749 . Doi: 10.1016/s0015-0282(16)58207-7
• 7 IJland MM, Evers JL, Dunselman GA, Volovics L, Hoogland HJ. Relation between endometrial wavelike activity and fecundability in spontaneous cycles. Fertil Steril 1997; 67 (03) 492-496 . Doi: 10.1016/s0015-0282(97)80075-1
• 8 Fanchin R, Righini C, Olivennes F, Taylor S, de Ziegler D, Frydman R. Uterine contractions at the time of embryo transfer alter pregnancy rates after in-vitro fertilization. Hum Reprod 1998; 13 (07) 1968-1974 . Doi: 10.1093/humrep/13.7.1968
• 9 Leyendecker G, Kunz G, Herbertz M, Beil D, Huppert P, Mall G. et al. Uterine peristaltic activity and the development of endometriosis. Ann N Y Acad Sci 2004; 1034: 338-355 . Doi: 10.1196/annals.1335.036
• 10 Bulletti C, De Ziegler D, Polli V, Del Ferro E, Palini S, Flamigni C. Characteristics of uterine contractility during menses in women with mild to moderate endometriosis. Fertil Steril 2002; 77 (06) 1156-1161
• 11 Puente JM, Fabris A, Patel J, Patel A, Cerrillo M, Requena A. et al. Adenomyosis in infertile women: prevalence and the role of 3D ultrasound as a marker of severity of the disease. Reprod Biol Endocrinol 2016; 14 (01) 60 . Doi: 10.1186/s12958-016-0185-6
• 12 Exacoustos C, Luciano D, Corbett B, De Felice G, Di Feliciantonio M, Luciano A. et al. The uterine junctional zone: a 3-dimensional ultrasound study of patients with endometriosis. Am J Obstet Gynecol 2013; 209 (03) 248.e1-248.e7 . Doi: 10.1016/j.ajog.2013.06.006
• 13 Naftalin J, Jurkovic D. The endometrial-myometrial junction: a fresh look at a busy crossing. Ultrasound Obstet Gynecol 2009; 34 (01) 1-11 . Doi: 10.1002/uog.6432
• 14 Naftalin J, Hoo W, Nunes N, Mavrelos D, Nicks H, Jurkovic D. Inter- and intraobserver variability in three-dimensional ultrasound assessment of the endometrial-myometrial junction and factors affecting its visualization. Ultrasound Obstet Gynecol 2012; 39 (05) 587-591 . Doi: 10.1002/uog.10133
• 15 Maged AM, Ramzy AM, Ghar MA, El Shenoufy H, Gad Allah SH, Wahba AH. et al. 3D ultrasound assessment of endometrial junctional zone anatomy as a predictor of the outcome of ICSI cycles. Eur J Obstet Gynecol Reprod Biol 2017; 212: 160-165 . Doi: 10.1016/j.ejogrb.2017.03.035
• 16 Lee C, Jurkovic D. Clinical presentation and investigation: the ‘‘one-stop’' clinic, endometrial sampling, hysteroscopy, vaginal ultrasound. In: Lee C, Jurkovic D. Uterine cancer. New York, NY: Taylor and Francis; 2005: 91-105
• 17 Van den Bosch T, Dueholm M, Leone FP, Valentin L, Rasmussen CK, Votino A. et al. Terms, definitions and measurements to describe sonographic features of myometrium and uterine masses: a consensus opinion from the Morphological Uterus Sonographic Assessment (MUSA) group. Ultrasound Obstet Gynecol 2015; 46 (03) 284-298 . Doi: 10.1002/uog.14806
• 18 Chamié LP, Blasbalg R, Pereira RM, Warmbrand G, Serafini PC. Findings of pelvic endometriosis at transvaginal US, MR imaging, and laparoscopy. Radiographics 2011; 31 (04) E77-E100 . Doi: 10.1148/rg.314105193
• 19 Altman DG. Practical statistics for medical research. London: Chapman and Hall; 1991. Book review of Ashby D. Stat Med 1991; 10 (10) 1635-1636 . Doi: 10.1002/sim.4780101015
• 20 Rasmussen CK, Glavind J, Madsen LD, Uldbjerg N, Dueholm M. Repeatability of junctional zone measurements using 3-dimensional transvaginal sonography in healthy fertile women. J Ultrasound Med 2016; 35 (07) 1497-1508 . Doi: 10.7863/ultra.15.06086
• 21 Hauth EA, Jaeger HJ, Libera H, Lange S, Forsting M. MR imaging of the uterus and cervix in healthy women: determination of normal values. Eur Radiol 2007; 17 (03) 734-742 . Doi: 10.1007/s00330-006-0313-3
• 22 Hoad CL, Raine-Fenning NJ, Fulford J, Campbell BK, Johnson IR, Gowland PA. Uterine tissue development in healthy women during the normal menstrual cycle and investigations with magnetic resonance imaging. Am J Obstet Gynecol 2005; 192 (02) 648-654 . Doi: 10.1016/j.ajog.2004.07.032
• 23 Fleischer AC, Kalemeris GC, Entman SS. Sonographic depiction of the endometrium during normal cycles. Ultrasound Med Biol 1986; 12 (04) 271-277 . Doi: 10.1016/0301-5629(86)90336-4
• 24 Larsen SB, Lundorf E, Forman A, Dueholm M. Adenomyosis and junctional zone changes in patients with endometriosis. Eur J Obstet Gynecol Reprod Biol 2011; 157 (02) 206-211 . Doi: 10.1016/j.ejogrb.2011.03.003
• 25 Wiczyk HP, Janus CL, Richards CJ, Graf MJ, Gendal ES, Rabinowitz JG. et al. Comparison of magnetic resonance imaging and ultrasound in evaluating follicular and endometrial development throughout the normal cycle. Fertil Steril 1988; 49 (06) 969-972 . Doi: 10.1016/s0015-0282(16)59946-4
• 26 McCarthy S, Tauber C, Gore J. Female pelvic anatomy: MR assessment of variations during the menstrual cycle and with use of oral contraceptives. Radiology 1986; 160 (01) 119-123 . Doi: 10.1148/radiology.160.1.3715022
• 27 Exacoustos C, Brienza L, Di Giovanni A, Szabolcs B, Romanini ME, Zupi E. et al. Adenomyosis: three-dimensional sonographic findings of the junctional zone and correlation with histology. Ultrasound Obstet Gynecol 2011; 37 (04) 471-479 . Doi: 10.1002/uog.8900
• 28 Leyendecker G, Kunz G, Noe M, Herbertz M, Mall G. Endometriosis: a dysfunction and disease of the archimetra. Hum Reprod Update 1998; 4 (05) 752-762 . Doi: 10.1093/humupd/4.5.752
• 29 Yeniel O, Cirpan T, Ulukus M, Ozbal A, Gundem G, Ozsener S. et al. Adenomyosis: prevalence, risk factors, symptoms and clinical findings. Clin Exp Obstet Gynecol 2007; 34 (03) 163-167
• 30 Gordts S, Brosens JJ, Fusi L, Benagiano G, Brosens I. Uterine adenomyosis: a need for uniform terminology and consensus classification. Reprod Biomed Online 2008; 17 (02) 244-248 . Doi: 10.1016/s1472-6483(10)60201-5
• 31 Tocci A, Greco E, Ubaldi FM. Adenomyosis and ‘endometrial-subendometrial myometrium unit disruption disease’ are two different entities. Reprod Biomed Online 2008; 17 (02) 281-291 . Doi: 10.1016/s1472-6483(10)60207-6
• 32 Bazot M, Fiori O, Darai E. Adenomyosis in endometriosis--prevalence and impact on fertility. Evidence from magnetic resonance imaging. Hum Reprod 2006; 21 (04) 1101-1102 , author reply 1102–1103. Doi: 10.1093/humrep/dei448
• 33 Munro MG, Critchley HO, Fraser IS. ; FIGO Menstrual Disorders Working Group. The FIGO classification of causes of abnormal uterine bleeding in the reproductive years. Fertil Steril 2011; 95 (07) 2204-2208 , 2208.e1–2208.e3
• 34 Brosens I, Kunz G, Benagiano G. Is adenomyosis the neglected phenotype of an endomyometrial dysfunction syndrome?. Gynecol Surg 2012; 9 (02) 131-137 . Doi: 10.1007/s10397-011-0723-3
• 35 Yazbek J, Ameye L, Testa AC, Valentin L, Timmerman D, Holland TK. et al. Confidence of expert ultrasound operators in making a diagnosis of adnexal tumor: effect on diagnostic accuracy and interobserver agreement. Ultrasound Obstet Gynecol 2010; 35 (01) 89-93 . Doi: 10.1002/uog.7335