Abstract
Objective
To present the distribution of neurovascular and lymphatic vessels in uterine ligaments using 3D models based on the pathological staining of serial 2D sections of postoperative specimens.
Methods
Serial transverse sections of fresh uterine ligaments from a patient with stage IB1 cervical squamous cell carcinoma were studied using the computer-assisted anatomic dissection (CAAD) technique. The sections were stained with hematoxylin and eosin, Weigert elastic fibers, D2-40 and immunostainings (sheep anti-tyrosine hydroxylase and rabbit anti-vasoactive intestinal peptide). The sections were then digitalized, registered and reconstructed three-dimensionally. Then, the 3D models were analyzed and measured.
Results
The 3D models of the neurovascular and lymphatic vessels in uterine ligaments were created, depicting their precise location and distribution. The vessels were primarily located in the upper part of the ligaments model, while the pelvic autonomic nerves were primarily in the lower part; the lymphatic vessels were scattered in the uterine ligaments, without obvious regularity.
Conclusion
CAAD is an effective anatomical method to study the precise distribution of neurovascular and lymphatic vessels in uterine ligaments. It can present detailed anatomical information about female pelvic autonomic innervation and the spatial relationship between nerves and vessels and may provide a better understanding of nerve-sparing radical hysterectomy.
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References
Koh WJ, Abu-Rustum NR, Bean S, Bradley K, Campos SM, Cho KR, Chon HS, Chu C, Clark R, Cohn D, Crispens MA, Damast S, Dorigo O, Eifel PJ, Fisher CM, Frederick P, Gaffney DK, Han E, Huh WK, Lurain JR 3rd, Mariani A, Mutch D, Nagel C, Nekhlyudov L, Fader AN, Remmenga SW, Reynolds RK, Tillmanns T, Ueda S, Wyse E, Yashar CM, McMillian NR, Scavone JL (2019) Cervical cancer, version 3.2019, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 17:64–84. https://doi.org/10.6004/jnccn.2019.0001
van Gent MD, Romijn LM, van Santen KE, Trimbos JB, de Kroon CD (2016) Nerve-sparing radical hysterectomy versus conventional radical hysterectomy in early-stage cervical cancer. a systematic review and meta-analysis of survival and quality of life. Maturitas 94:30–38. https://doi.org/10.1016/j.maturitas.2016.08.005
Wang X, Chen C, Liu P, Li W, Wang L, Liu Y (2018) The morbidity of sexual dysfunction of 125 Chinese women following different types of radical hysterectomy for gynaecological malignancies. Arch Gynecol Obstet 297:459–466. https://doi.org/10.1007/s00404-017-4625-0
Balaya V, Rossi L, Cornou C, Ngô C, Bensaid C, Bats AS, Lecuru F (2017) Where does pelvic nerve injury occur during radical hysterectomy for cervical cancer? Gynecol Oncol 145:199–200
Sakamoto S, Takizawa K (1988) An improved radical hysterectomy with fewer urological complications and with no loss of therapeutic results for invasive cervical cancer. Baillieres Clin Obstet Gynaecol 2:953–962
Höckel M, Konerding MA, Peter Heuβel C (1998) Liposuction-assisted nerve-sparing extended radical hysterectomy: oncologic rationale, surgical anatomy, and feasibility study. Am J Obstet Gynecol 178:971–976. https://doi.org/10.1016/S0002-9378(98)70533-2
Höckel M, Horn LC, Hentschel B, Höckel S, Naumann G (2003) Total mesometrial resection: high resolution nerve-sparing radical hysterectomy based on developmentally defined surgical anatomy. Int J Gynecol Cancer 13:791–803. https://doi.org/10.1111/j.1525-1438.2003.13608.x
Aoun F, van Velthoven R (2015) Lower urinary tract dysfunction after nerve-sparing radical hysterectomy. Int Urogynecol J 26:947–957. https://doi.org/10.1007/s00192-014-2574-8
Kavallaris A, Hornemann A, Chalvatzas N, Luedders D, Diedrich K, Bohlmann MK (2010) Laparoscopic nerve-sparing radical hysterectomy: description of the technique and patients' outcome. Gynecol Oncol 119:198–201. https://doi.org/10.1016/j.ygyno.2010.07.020
van Gent MD, van den Haak LW, Gaarenstroom KN, Peters AA, van Poelgeest MI, Trimbos JB, de Kroon CD (2014) Nerve-sparing radical abdominal trachelectomy versus nerve-sparing radical hysterectomy in early-stage (FIGO IA2-IB) cervical cancer: a comparative study on feasibility and outcome. Int J Gynecol Cancer 24:735–743. https://doi.org/10.1097/IGC.0000000000000114
Kim HS, Kim TH, Suh DH, Kim SY, Kim MA, Jeong CW, Hong KS, Song YS (2015) Success factors of laparoscopic nerve-sparing radical hysterectomy for preserving bladder function in patients with cervical cancer: a protocol-based prospective cohort study. Ann Surg Oncol 22:1987–1995. https://doi.org/10.1245/s10434-014-4197-1
Chen C, Huang L, Liu P, Su G, Li W, Lu L, Wang L, Li X, Duan H, Zou C, Hatch K (2014) Neurovascular quantitative study of the uterosacral ligament related to nerve-sparing radical hysterectomy. Eur J Obstet Gynecol Reprod Biol 172:74–79. https://doi.org/10.1016/j.ejogrb.2013.09.035
Butler-Manuel SA, Buttery LD, A'Hern RP, Polak JM, Barton DP (2000) Pelvic nerve plexus trauma at radical hysterectomy and simple hysterectomy: the nerve content of the uterine supporting ligaments. Cancer 89:834–841. https://doi.org/10.1002/1097-0142(20000815)89:4%3c834:AID-CNCR14%3e3.0.CO;2-7
Kato T, Murakami G, Yabuki Y (2003) A new perspective on nerve-sparing radical hysterectomy: nerve topography and over-preservation of the cardinal ligament. Jpn J Clin Oncol 33:589–591
Kraima AC, Derks M, Smit NN, van de Velde CJ, Kenter GG, DeRuiter MC (2016) Careful dissection of the distal ureter is highly important in nerve-sparing radical pelvic surgery: a 3D reconstruction and immunohistochemical characterization of the vesical plexus. Int J Gynecol Cancer 26:959–966. https://doi.org/10.1097/IGC.0000000000000709
Moszkowicz D, Alsaid B, Bessede T, Penna C, Benoit G, Peschaud F (2011) Female pelvic autonomic neuroanatomy based on conventional macroscopic and computer-assisted anatomic dissections. Surg Radiol Anat 33:397–404. https://doi.org/10.1007/s00276-010-0773-7
Bertrand MM, Alsaid B, Droupy S, Benoit G, Prudhomme M (2013) Optimal plane for nerve sparing total mesorectal excision, immunohistological study and 3D reconstruction: an embryological study. Colorectal Dis 15:1521–1528. https://doi.org/10.1111/codi.12459
Kimmig R, Aktas B, Buderath P, Rusch P, Heubner M (2016) Intraoperative navigation in robotically assisted compartmental surgery of uterine cancer by visualisation of embryologically derived lymphatic networks with indocyanine-green (ICG). J Surg Oncol 113: 554–559. https://doi.org/10.1002/jso.24174
Bertrand MM, Macri F, Mazars R, Droupy S, Beregi JP, Prudhomme M (2014) MRI-based 3D pelvic autonomous innervation: a first step towards image-guided pelvic surgery. Eur Radiol 24:1989–1997. https://doi.org/10.1007/s00330-014-3211-0
Moszkowicz D, Alsaid B, Bessede T, Zaitouna M, Penna C, Benoit G, Peschaud F (2011) Neural supply to the clitoris: immunohistochemical study with three-dimensional reconstruction of cavernous nerve, spongious nerve, and dorsal clitoris nerve in human fetus. J Sex Med 8:1112–1122. https://doi.org/10.1111/j.1743-6109.2010.02182.x
Li P, Liu P, Chen C, Duan H, Qiao W, Ognami OH (2018) The 3D reconstructions of female pelvic autonomic nerves and their related organs based on MRI: a first step towards neuronavigation during nerve-sparing radical hysterectomy. Eur Radiol. https://doi.org/10.1007/s00330-018-5453-8
Thomeer MG, Gerestein C, Spronk S, van Doorn HC, van der Ham E, Hunink MG (2013) Clinical examination versus magnetic resonance imaging in the pretreatment staging of cervical carcinoma: systematic review and meta-analysis. Eur Radiol 23:2005–2018. https://doi.org/10.1007/10.1007/s00330-013-2783-4
Park JJ, Kim CK, Park SY, Park BK (2015) Parametrial invasion in cervical cancer: fused T2-weighted imaging and high-b-value diffusion-weighted imaging with background body signal suppression at 3 T. Radiology 274:734–741. https://doi.org/10.1148/radiol.14140920
Acknowledgements
This study has received funding by the National Natural Science Fund of China (81571422, 81370736), the National Science and Technology Support Program of China (2014BAI05B03), the National Natural Science Fund of Guangdong (2015A030311024), the Science and Technology Plan of Guangzhou (158100075), and the Foundation from the President of Nanfang Hospital of Southern Medical University (2015C015).
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PFL: protocol development, data collection and manuscript writing; HD: protocol development, data analysis and manuscript writing; JW: protocol development, data collection and manuscript writing; SPG: data analysis; GDS: data analysis; JYL: protocol development; LT: protocol development; YZ: protocol development; HJF: manuscript writing; PL: protocol development, data analysis and manuscript editing; CLC: protocol development, data analysis and manuscript editing.
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Li, P., Duan, H., Wang, J. et al. Neurovascular and lymphatic vessels distribution in uterine ligaments based on a 3D reconstruction of histological study: to determine the optimal plane for nerve-sparing radical hysterectomy. Arch Gynecol Obstet 299, 1459–1465 (2019). https://doi.org/10.1007/s00404-019-05108-w
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DOI: https://doi.org/10.1007/s00404-019-05108-w