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A missing distal complex of the external and internal anal sphincters: a macroscopic and histologic study using Japanese and German elderly cadavers

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Abstract

The lower margin of the internal anal sphincter (IAS) is considered to lie on a J-shaped, subcutaneous part (SCP) of the external anal sphincter (EAS). The lower IAS is united with the J-shaped SCP to form a smooth-striated muscle complex. In the first part of this study, we ensured the presence of the J-shaped EAS in the lateral wall of the anal canal from 12 near-term fetuses. Second, in the lateral anal wall, the examination of the longitudinal section from 20 male and 24 female Japanese cadavers (72–95 years-old) demonstrated that the J-shaped EAS was lost in 15 (34%) due to the very small SCP. Third, we demonstrated that the J-shaped EAS was restricted in the latera anal wall using longitudinal histological sections of the anal canal from 11 male Japanese cadavers (75–89 years-old). Therefore, a site-dependent difference in the IAS–EAS configuration was evident. Finally, we compared a frequency of the lost J-shape between human populations using 10 mm-thick frontal slices from 36 Japanese and 28 German cadavers. The two groups of cadavers were compatible in age (a 0.2-years’ difference in males). The macroscopic observations revealed that the J-shaped EAS was absent from 13 (36%) Japanese and six (20%) German specimens, suggesting that the SCP degeneration occurred more frequent in elderly Japanese than elderly German individuals (p < 0.05). The distal IAS–EAS complex seemed to push residual feces out of the anal canal at a transient phase from evacuation to closure. The absence might be the first sigh of anal dysfunction.

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References

  1. Akervall S, Nordgren S, Fasth S, Oresland T, Pettersson K, Hultén L (1990) The effects of age, gender, and parity on rectoanal functions in adults. Scand J Gastroenterol 25:1247–1256. https://doi.org/10.3109/00365529008998561

    Article  CAS  PubMed  Google Scholar 

  2. Arakawa T, Murakami G, Nakajima F, Ohtsuka A, Goto T, Teramoto T (2004) Morphologies of the interfaces between the levator ani muscle and pelvic viscera with special reference to muscle insertion into the anorectum in elderly Japanese. Anat Sci Int 79:72–81. https://doi.org/10.1111/j.1447-073x.2004.00069.x

    Article  PubMed  Google Scholar 

  3. Arakawa T, Hayashi S, Kinugasa Y, Murakami G, Fujimiya M (2010) Development of the external anal sphincter with special reference to intergender difference: observations of mid-term fetuses (15–30 weeks of gestation). Okajimas Folia Anat Jpn 87:49–58. https://doi.org/10.2535/ofaj.87.49

    Article  PubMed  Google Scholar 

  4. Arakawa T, Hwang SE, Kim JH, Wilting J, Rodriguez-Vazquez JF, Murakami G, Hwang HP, Cho BH (2016) Fetal growth of the anal sinus and sphincters especially in relation to anal anomalies. Int J Colorectal Dis 31:493–502. https://doi.org/10.1007/s00384-015-2455-8

    Article  PubMed  Google Scholar 

  5. Brusa T, Abler D, Tutuian R, Gingert C, Haverhagen JT, Adamina M, Brügger LE, Büchler P (2018) Anatomy and mechanical properties of the anal sphincter muscles in healthy senior volunteers. Neurogasteoenterol Motil. https://doi.org/10.1111/nmo.13335

    Article  Google Scholar 

  6. Cazamier M, Terra MP, Stoker J, de Lange-de Klerk ES, Boeckxstaens GE, Mulder CJJ, Felt-Bersma RJF (2006) Atrophy and defects detection of the external anal Sphincter: comparison between three-dimensional anal endosonography and endoanal magnetic resonance imaging. Dis Colon Rectum 49:20–27. https://doi.org/10.1007/s10350-005-0220-8

    Article  Google Scholar 

  7. Frudinger A, Halligan S, Barttram CI, Price AB, Kamm MA, Winter R (2002) Female anal sphincter: age-related differences in asymptomatic volunteers with high-frequency endoanal US. Radiology 224:417–423. https://doi.org/10.1148/radiol.2242010985

    Article  PubMed  Google Scholar 

  8. Handa VL, Lockhart ME, Fielding JR, Bradley CS, Brubaker L, Cundiff GW, Ye W, Richter HE (2008) Racial differences in pelvic anatomy by magnetic resonance imaging. Obstet Gynecol 111:914–920. https://doi.org/10.1097/AOG.0b013e318169ce03

    Article  PubMed  PubMed Central  Google Scholar 

  9. Hieda K, Cho KH, Arakawa T, Fujimiya M, Murakami G, Matsubara M (2013) Nerves in the intersphincteric space of the human anal canal with special reference to their continuation to the enteric nerve plexus of the rectum. Clin Anat 26:843–854. https://doi.org/10.1002/ca.22227

    Article  PubMed  Google Scholar 

  10. Hornung BR, Telford KJ, Carlson GL, Mitchell PJ, Klarskov N, Kiff ES (2017) Use of anal acoustic reflectometry in the evaluation of men with passive fecal leakage. Dis Colon Rectum 60:521–526. https://doi.org/10.1097/DCR.0000000000000790

    Article  PubMed  Google Scholar 

  11. Hoyte L, Thomas J, Foster RT, Shott S, Jakab M, Weidner AC (2005) Racial differences in pelvic morphology among asymptomatic nulliparous women as seen on three-dimensional magnetic resonance images. Am J Obstet Gynecol 193:2035–2040. https://doi.org/10.1016/j.ajog.2005.06.060

    Article  PubMed  Google Scholar 

  12. Ishiyama G, Hinata N, Kinugasa Y, Murakami G, Fujimiya F (2014) Nerves supplying the internal anal sphincter: an immunohistochemical study using donated elderly cadavers. Surg Radiol Anat 36:1033–1042. https://doi.org/10.1007/s00276-014-1289-3

    Article  PubMed  Google Scholar 

  13. Jin ZW, Hata F, Jin Y, Murakami G, Kinugasa Y, Abe S (2015) The anococcygeal ligaments: cadaveric study with application to our understanding of incontinence in the elderly. Clin Anat 28:1039–1047. https://doi.org/10.1002/ca.22629

    Article  PubMed  Google Scholar 

  14. Jin ZW, Jin Y, Li XW, Murakami G, Rodríguez-Vázquez JF, Wilting J (2016) Perineal raphe with special reference to its extension to the anus: a histological study using human fetuses. Anat Cell Biol 49:116–124. https://doi.org/10.5115/acb.2016.49.2.116

    Article  PubMed  PubMed Central  Google Scholar 

  15. Jin ZW, Cho KH, Jang HS, Murakami G, Yamamoto M, Abe S (2017) Coccygeal body revisited: an immunohistochemical study using donated elderly cadavers. Anat Rec 300:1826–1837. https://doi.org/10.1002/ar.23615

    Article  CAS  Google Scholar 

  16. Kim JH, Kinugasa Y, Yu HC, Murakami G, Abe S, Cho BH (2015) Lack of striated muscle fibers in the longitudinal anal muscle of elderly Japanese: a histological study using cadaveric specimens. Int J Colorectal Dis 30:43–49. https://doi.org/10.1007/s00384-014-2038-0

    Article  PubMed  Google Scholar 

  17. Kinugasa Y, Arakawa T, Abe S, Ohtsuka A, Suzuki D, Murakami G, Fujimiya M, Sugihara K (2011) Anatomical reevaluation of the anococcygeal ligament and its surgical relevance. Dis Colon Rectum 54:232–237. https://doi.org/10.1007/DCR.0b013e318202388f

    Article  PubMed  Google Scholar 

  18. Kinugasa Y, Arakawa T, Abe H, Abe S, Cho BH, Murakami G, Sugihara K (2012) Anococcygeal raphe revisited: a histological study using mid-term human fetuses and elderly cadavers. Yonsei Med J 53:849–855. https://doi.org/10.3349/ymj.2012.53.4.849

    Article  PubMed  PubMed Central  Google Scholar 

  19. Kinugasa Y, Arakawa T, Abe H, Rodríguez-Vázquez JF, Murakami G, Sugihara K (2013) Female longitudinal anal muscles or conjoint longitudinal coats extend into the subcutaneous tissue along the vaginal vestibule: a histological study using human fetuses. Yonsei Med J 54:778–784. https://doi.org/10.3349/ymj.2013.54.3.778

    Article  PubMed  PubMed Central  Google Scholar 

  20. Lestar B, Penninckx F, Rigauts H, Kerremans R (1992) The internal anal sphincter can not close the anal canal completely. Int J Colorectal Dis 7:159–161. https://doi.org/10.1007/BF00360358

    Article  CAS  PubMed  Google Scholar 

  21. Lunniss PJ, Phillips RK (1992) Anatomy and function of the anal longitudinal muscle. Br J Surg 79:882–884. https://doi.org/10.1002/bjs.1800790908

    Article  CAS  PubMed  Google Scholar 

  22. Mittal RK, Bhargava V, Sheean G, Ledgerwood M, Sinha S (2014) Purse-string morphology of external anal sphincter revealed by novel imaging techniques. Am J Physiol Gastrointest Liver Physiol 306:G505-514. https://doi.org/10.1152/ajpgi.00338.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Motohashi O, Suzuki M, Shida N, Umezawa T, Ohtoh Y, Sakurai Y, Yoshimoto T (1995) Subarachnoid haemorrhage-induced proliferation of leptomeningeal cells and deposition of extracellular matrices in the arachnoid granulations and subarachnoid space. Acta Neurochir 136:88–91. https://doi.org/10.1007/BF01411441

    Article  CAS  PubMed  Google Scholar 

  24. Murad-Regadas SM, Regadas FS, Rodriguez LV, Kenmoti VT, Fernandes GO, Buchen G, Regadas Filho FS (2012) Effect of vaginal delivery and ageing on the anatomy of the female anal canal assessed by three-dimensional anorectal ultrasound. Colorectal Dis 14:1521–1527. https://doi.org/10.1111/j.1463-1318.2012.03033.x

    Article  CAS  PubMed  Google Scholar 

  25. Nagata I, Murakami G, Suzuki D, Furuya K, Koyama M, Ohtsuka A (2007) Histological features of the rectoveginal septum in elderly women and a proposal for posterior vaginal repair. Int Urogynecol J 18:863–868. https://doi.org/10.1007/s00192-006-0249-9

    Article  Google Scholar 

  26. Nielsen MB, Pedersen JF (1996) Changes in the anal sphincter with age: an endosonographic study. Acta Radiol 37:357–361. https://doi.org/10.1177/02841851960371P175

    Article  CAS  PubMed  Google Scholar 

  27. Penninckx F, Lester B, Kerremans R (1992) The internal anal sphincter: mechanisms of control and its role in maintaining anal continence. Baillieres Clin Gastroenterol 6:193–214. https://doi.org/10.1016/0950-3528(92)90027-c

    Article  CAS  PubMed  Google Scholar 

  28. Petros PE, Ulmsten U (1997) Role of the pelvic floor in bladder neck opening and closure I: muscle forces. Int Urogynecol J 8:74–80. https://doi.org/10.1007/BF02764822

    Article  CAS  Google Scholar 

  29. Regadas FS, Murad-Regadas SM, Lima DM, Silva FR, Barreto RG, Souza MH, Regadas Filho FS (2007) Anal canal anatomy showed by three-dimensional anorectal ultrasonography. Surg Ensosc 21:2207–2211. https://doi.org/10.1007/s00464-007-9339-0

    Article  Google Scholar 

  30. Rociu E, Stoker J, Eijkemans MJ, Laméris JS (2000) Normal anal sphincter anatomy and age- and sex-related variations at high-spatial-resolution endoanal MR imaging. Radiology 217:395–401. https://doi.org/10.1148/radiology.217.2.r00nv13395

    Article  CAS  PubMed  Google Scholar 

  31. Sasaki H, Hinata N, Kurokawa K, Murakami G (2015) Supportive tissues of the vagina with special reference to a fibrous skeleton in the perineum: a review. Open J Obstetr Gynecol 15:42. https://doi.org/10.1186/s12894-015-0034-5

    Article  Google Scholar 

  32. Sboarina A, Minicossi A, Segattini C, Leopardi F, Lombardo F, Passeri V, Scudo G, Bencivenga M, Fenzi A, Cordiano C (2012) Shape and volume of internal anal sphincter showed by three-dimensional anorectal iltrasonography. Eur J Radiol 81:1479–1482. https://doi.org/10.1016/j.ejrad.2011.04.024

    Article  CAS  PubMed  Google Scholar 

  33. Sǿrensen G, Liao D, Lundby L, Fynne L, Buntzen S, Gregersen H, Laurberg S, Krogh K (2014) Distensibility of the anal canal in patients with idiopathic fecal incontinence: a study with the functional lumen imaging probe. Neurogasteoenterol Motil 26:255–263. https://doi.org/10.1111/nmo.12258

    Article  Google Scholar 

  34. Uchimoto K, Murakami G, Kinugasa Y, Arakawa T, Matsubara A, Nakajima Y (2007) Rectourethralis muscle and pitfalls of anterior perineal dissection abdominoperineal resection and intersphincteric resection for rectal cancer. Anat Sci Int 82:8–15. https://doi.org/10.1111/j.1447-073X.2006.00161.x

    Article  PubMed  Google Scholar 

  35. Williams PL (1995) Gray’s anatomy, 38th edn. Churchill Livingstone, London, pp 1780–1782

    Google Scholar 

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Acknowledgements

We thank Dr. M. Yamamoto and Dr. K. Kitamura of Tokyo Dental College and Mrs. A. Ahrbecker and Mrs. I. Hettwer-Steeger of Georg-August-University for their excellent technical assistance in preparing the macroscopic cadaveric slices.

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Authors and Affiliations

  1. Division of Surgery, Ishiyama Proctology Hospital, Sapporo, Japan

    Gentaro Ishiyama

  2. Department of Anatomy, Jeonbuk National University Medical School, 20 Geunji-ro, Deokjin-gu, Jeonju, 54907, Korea

    Ji Hyun Kim & Ok Hee Chai

  3. Department of Anatomy, School of Medicine, Georg-August-Universität Gőttingen, Gőttingen, Germany

    Christoph Viebahn & Jőrg Wilting

  4. Division of Internal Medicine, Jikou-Kai Clinic of Home Visit, Sapporo, Japan

    Gen Murakami

  5. Emeritus Professor of Akita University School of Medicine, Akita, Japan

    Hiroshi Abe

  6. Department of Anatomy, Tokyo Dental College, Tokyo, Japan

    Shinichi Abe

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  1. Gentaro Ishiyama
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Contributions

Conceptualization: GI, JHK, GM, JW. Data acquisition: JHK, GI, HA. Data analysis: GM, CV, JW, HA. Drafting of the manuscript: GM, JHK, GI. Critical revision: GM, OHC, CV, JW, HA, SA. All authors approved the final version of the manuscript.

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Correspondence to Ji Hyun Kim.

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Ishiyama, G., Kim, J.H., Chai, O.H. et al. A missing distal complex of the external and internal anal sphincters: a macroscopic and histologic study using Japanese and German elderly cadavers. Surg Radiol Anat 43, 775–784 (2021). https://doi.org/10.1007/s00276-020-02606-4

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