Anat Cell Biol.  2022 Sep;55(3):330-340. 10.5115/acb.22.072.

Regions of the human renal artery: histomorphometric analysis

• Mompeó-Corredera B
• Hernández-Morera P
• Castaño-González I
• Quintana-Montesdeoca MdP
• Mederos-Real N

• KMID: 2533359
• DOI: http://doi.org/10.5115/acb.22.072

Abstract

The renal artery is frequently involved in the pathogenesis of vasculorenal diseases, and it is a target in kidney surgery and therapeutic techniques for refractory hypertension. However, few detailed structural studies on the human renal artery have been conducted. Using histocytochemistry, immunohistochemistry, and quantitative image analysis, the wall thickness, structure, smooth muscle cells, extracellular matrix, and proportion of elastic tissue in the tunica media of main human renal arteries were used estimated. Ninety-six tissue samples were collected from sections of the right and left main renal arteries. The results showed that the renal artery changed from an elastic vessel in its proximal segment to a muscular artery in its distal part. A critical characteristic of the renal artery was the presence of longitudinal smooth muscle cell formations in the tunica adventitia of middle and distal segments but not in the proximal part of the artery. In addition, the tunica adventitia of the renal artery showed a rich vascularization and the presence of numerous nerves profiles. The artery's regional structural and morphometric features explain that a particular arterial pathology is more frequent in a specific vessel sector than in others. In addition, those characteristics could determine a different therapeutic response attending to the arterial sector.

Keyword

Renal artery; Morphometry; Immunohistochemistry; Smooth muscle; Extracellular matrix

Figure

• 

  Fig. 1 Photomicrograph of the human renal artery wall. (A) Masson’s trichromic stain, proximal segment; (B) resorcin stain, proximal segment; (C) Masson’s trichromic stain, middle segment; (D) resorcin stain, middle; (E) Masson’s trichromic stain, distal segment; and (F) resorcin stain, distal segment (bar=100 μm). L, lumen; ti, tunica intima; tm, tunica media; ta, tunicaadventitia; iem, internalelastic lamina; eem, externalelastic lamina.

• 

  Fig. 2 Staining of nerve fibers with S100 in the adventitia and periadventitial tissue: (A) shows that most of the nerves are oriented transversely and run parallel to the vessels; (B) nerve fibers in the outer adventitia in relation to the vasa vasorum and transversely sectioned nerves are observed in the periadventitial tissue; (C) nerve fibers in relation to vasa vasorum transversely sectioned; (D) nerve fibers located in adventitial longitudinal vasa; (E) several nerve fibers are located in the vasa vasorum wall; (F) detail of a nerve fiber in the wall of a vasa vasorum longitudinally sectioned. Arrows indicate nerve fibers in the vasa vasorum wall. L, lumen; V, vein; AR, artery; ta, tunica adventitia; padv, periadventitial tissue; N, nerves. anti-S100 immunodetection. Bar in A: 200 μm, Bar in B: 100 μm, Bar in C–F: 10 μm.

• 

  Fig. 3 Photomicrograph of the human renal artery wall. (A) and (B) show actin staining samples. (C) and (D) show von Willebrand factor staining (Bar in A, C, D: 100 μm, Bar in B: 10 μm). (A) Bunches of longitudinally oriented smooth muscle cells (SMCs) are surrounded by elastic fibers in the adventitia; the formations have a fusiform morphology; some of them have vasa vasorum (VV); (B) detail of one of the SMCs bunches; (C) endothelial cell of VV in the adventitia; most of the vasa have a disposition parallel to the lumen; (D) shows dilated VV in the adventitia. Arrows indicate VV. In addition, some nerves are observed in periadventitial tissue. tm, tunica media; ta, tunica adventitia; padv, periadventitial tissue; lSMCs, longitudinal SMCs formation; e, elastic layer; N, nerves.

Reference

References

1. Dodd GD 3rd, Tublin ME, Shah A, Zajko AB. 1991; Imaging of vascular complications associated with renal transplants. AJR Am J Roentgenol. 157:449–59. DOI: 10.2214/ajr.157.3.1872225. PMID: 1872225.

2. Hughes RJ, Scoble JE, Reidy JF. 2004; Renal angioplasty in non-atheromatous renal artery stenosis: technical results and clinical outcome in 43 patients. Cardiovasc Intervent Radiol. 27:435–40. DOI: 10.1007/s00270-004-0135-0. PMID: 15383845.

3. Kim HJ, Do YS, Shin SW, Park KB, Cho SK, Choe YH, Choo SW, Choo IW, Kim DK. 2008; Percutaneous transluminal angioplasty of renal artery fibromuscular dysplasia: mid-term results. Korean J Radiol. 9:38–44. DOI: 10.3348/kjr.2008.9.1.38. PMID: 18253074. PMCID: PMC2627178.

4. Liang P, Hurks R, Bensley RP, Hamdan A, Wyers M, Chaikof E, Schermerhorn ML. 2013; The rise and fall of renal artery angioplasty and stenting in the United States, 1988-2009. J Vasc Surg. 58:1331–8.e1. DOI: 10.1016/j.jvs.2013.04.041. PMID: 23810297. PMCID: PMC3791161.

5. Townsend RR, Mahfoud F, Kandzari DE, Kario K, Pocock S, Weber MA, Ewen S, Tsioufis K, Tousoulis D, Sharp ASP, Watkinson AF, Schmieder RE, Schmid A, Choi JW, East C, Walton A, Hopper I, Cohen DL, Wilensky R, Lee DP, Ma A, Devireddy CM, Lea JP, Lurz PC, Fengler K, Davies J, Chapman N, Cohen SA, DeBruin V, Fahy M, Jones DE, Rothman M, Böhm M. 2017; Catheter-based renal denervation in patients with uncontrolled hypertension in the absence of antihypertensive medications (SPYRAL HTN-OFF MED): a randomised, sham-controlled, proof-of-concept trial. Lancet. 390:2160–70. DOI: 10.1016/S0140-6736(17)32281-X. PMID: 28859944.

6. Weber MA, Mahfoud F, Schmieder RE, Kandzari DE, Tsioufis KP, Townsend RR, Kario K, Böhm M, Sharp ASP, Davies JE, Osborn JW, Fink GD, Euler DE, Cohen DL, Schlaich MP, Esler MD. 2019; Renal denervation for treating hypertension: current scientific and clinical evidence. JACC Cardiovasc Interv. 12:1095–105. DOI: 10.1016/j.jcin.2019.02.050. PMID: 31221299.

7. Böhm M, Kario K, Kandzari DE, Mahfoud F, Weber MA, Schmieder RE, Tsioufis K, Pocock S, Konstantinidis D, Choi JW, East C, Lee DP, Ma A, Ewen S, Cohen DL, Wilensky R, Devireddy CM, Lea J, Schmid A, Weil J, Agdirlioglu T, Reedus D, Jefferson BK, Reyes D, D'Souza R, Sharp ASP, Sharif F, Fahy M, DeBruin V, Cohen SA, Brar S, Townsend RR. 2020; Efficacy of catheter-based renal denervation in the absence of antihypertensive medications (SPYRAL HTN-OFF MED Pivotal): a multicentre, randomised, sham-controlled trial. Lancet. 395:1444–51. DOI: 10.1016/S0140-6736(20)30554-7. PMID: 32234534.

8. Okamura K, Satou S, Setojima K, Shono S, Miyajima S, Ishii T, Shirai K, Urata H. 2018; Reduction of blood pressure following after renal artery adventitia stripping during total nephroureterectomy: potential effect of renal sympathetic denervation. Am J Case Rep. 19:567–72. DOI: 10.12659/AJCR.908891. PMID: 29765015. PMCID: PMC5983072.

9. Wright I. 1963; The microscopical appearances of human peripheral arteries during growth and aging. J Clin Pathol. 16:499–522. DOI: 10.1136/jcp.16.6.499. PMID: 14076367. PMCID: PMC480632.

10. Osborne-Pellegrin MJ. 1978; Some ultrastructural characteristics of the renal artery and abdominal aorta in the rat. J Anat. 125(Pt 3):641–52. PMID: 640965. PMCID: PMC1235630.

11. Janzen J, Lanzer P, Rothenberger-Janzen K, Vuong PN. 2000; The transitional zone in the tunica media of renal arteries has a maximal length of 10 millimetres. Vasa. 29:168–72. DOI: 10.1024/0301-1526.29.3.168. PMID: 11037713.

12. Janzen J. 2004; The microscopic transitional zone between elastic and muscular arteries. Arch Mal Coeur Vaiss. 97:909–14. PMID: 15521485.

13. Hinata N, Suzuki R, Ishizawa A, Miyake H, Rodriguez-Vazquez JF, Murakami G, Fujisawa M. 2015; Fetal development of the mesonephric artery in humans with reference to replacement by the adrenal and renal arteries. Ann Anat. 202:8–17. DOI: 10.1016/j.aanat.2015.07.005. PMID: 26335195.

14. Mompeó B, Maranillo E, García-Touchard A, Sanudo JR. 2019; The morphogenesis of the renal plexus: renal artery and sympathetic fibers. Clin Anat. 32:272–6. DOI: 10.1002/ca.23297. PMID: 30300460.

15. Abd Elrahim E. 2020; Computed tomography evaluation of renal artery morphometry in adults. The impact of age and gender. Saudi Med J. 41:34–7. DOI: 10.15537/smj.2020.1.24795. PMID: 31915792. PMCID: PMC7001056.

16. Singh G, Ng YK, Bay BH. 1998; Bilateral accessory renal arteries associated with some anomalies of the ovarian arteries: a case study. Clin Anat. 11:417–20. DOI: 10.1002/(SICI)1098-2353(1998)11:6<417::AID-CA8>3.0.CO;2-L. PMID: 9800922.

17. Satyapal KS, Haffejee AA, Singh B, Ramsaroop L, Robbs JV, Kalideen JM. 2001; Additional renal arteries: incidence and morphometry. Surg Radiol Anat. 23:33–8. DOI: 10.1007/s00276-001-0033-y. PMID: 11370140.

18. Standring S. 2008. Gray's anatomy. 40th ed. Churchill Livingstone;Edinburgh:

19. Lee HB, Yang J, Maeng YH, Yoon SP. 2019; Bilateral multiple renal arteries with an extra-aortic origin and quadruple testicular veins. Anat Cell Biol. 52:518–21. DOI: 10.5115/acb.19.159. PMID: 31949992. PMCID: PMC6952688.

20. Leloup AJ, Van Hove CE, Heykers A, Schrijvers DM, De Meyer GR, Fransen P. 2015; Elastic and muscular arteries differ in structure, basal NO production and voltage-gated Ca(2+)-channels. Front Physiol. 6:375. DOI: 10.3389/fphys.2015.00375. PMID: 26696904. PMCID: PMC4678217.

21. Borlotti A, Khir AW, Rietzschel ER, De Buyzere ML, Vermeersch S, Segers P. 2012; Noninvasive determination of local pulse wave velocity and wave intensity: changes with age and gender in the carotid and femoral arteries of healthy human. J Appl Physiol (1985). 113:727–35. DOI: 10.1152/japplphysiol.00164.2012. PMID: 22678965.

22. Matz RL, Schott C, Stoclet JC, Andriantsitohaina R. 2000; Age-related endothelial dysfunction with respect to nitric oxide, endothelium-derived hyperpolarizing factor and cyclooxygenase products. Physiol Res. 49:11–8. PMID: 10805400.

23. Dougherty G. 2009. Digital image processing for medical applications. Cambridge University Press;Cambridge: DOI: 10.1017/CBO9780511609657.

24. Cordeiro de Amorim R, Mirkin B. 2012; Minkowski metric, feature weighting and anomalous cluster initializing in K-Means clustering. Pattern Recognit. 45:1061–75. DOI: 10.1016/j.patcog.2011.08.012.

25. Shmmala FA, Ashour W. 2013; Color based image segmentation using different versions of K-Means in two spaces. Glob Adv Res J Eng Technol Innov. 1:30–41.

26. Witten IH, Frank E, Hall MA, Pal C. Witten IH, Frank E, Hall MA, Pal C, editors. 2016. Algorithms: the basic methods. Data Mining: Practical Machine Learning Tools and Techniques. 4th ed. Morgan Kaufmann Publishers;Cambridge: p. 91–160. DOI: 10.1016/B978-0-12-804291-5.00004-0.

27. Madri JA, Reidy MA, Kocher O, Bell L. 1989; Endothelial cell behavior after denudation injury is modulated by transforming growth factor-beta1 and fibronectin. Lab Invest. 60:755–65. PMID: 2659888.

28. Stehbens WE. 1960; Focal intimal proliferation in the cerebral arteries. Am J Pathol. 36:289–301. PMID: 13834049. PMCID: PMC1942204.

29. Yoro T, Burnstock G. 1973; Fine structure of "intimal cushions" at branching sites in coronary arteries of vertebrates. A scanning and transmission electron microscopic study. Z Anat Entwicklungsgesch. 140:187–202. DOI: 10.1007/BF00520330. PMID: 4748697.

30. Stary HC, Blankenhorn DH, Chandler AB, Glagov S, Insull W Jr, Richardson M, Rosenfeld ME, Schaffer SA, Schwartz CJ, Wagner WD, Wissler RW. 1992; A definition of the intima of human arteries and of its atherosclerosis-prone regions. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb. 12:120–34. DOI: 10.1161/01.ATV.12.1.120. PMID: 1731855.

31. Safian RD, Textor SC. 2001; Renal-artery stenosis. N Engl J Med. 344:431–42. DOI: 10.1056/NEJM200102083440607. PMID: 11172181.

32. Kato Y, Mizutani T, Otsuka N, Ezure H, Inoue Y. 2018; Quantitative analysis of the elastic fiber in the tunica media at the carotid bifurcation. Okajimas Folia Anat Jpn. 95:23–7. DOI: 10.2535/ofaj.95.23. PMID: 30504647.

33. Sindram D, Martin K, Meadows JP, Prabhu AS, Heath JJ, McKillop IH, Iannitti DA. 2011; Collagen-elastin ratio predicts burst pressure of arterial seals created using a bipolar vessel sealing device in a porcine model. Surg Endosc. 25:2604–12. DOI: 10.1007/s00464-011-1606-4. PMID: 21404086.

34. Kurzidim MH, Oeschger M, Sasse D. 1999; Studies on the vasa vasorum of the human renal artery. Ann Anat. 181:223–7. DOI: 10.1016/S0940-9602(99)80013-2. PMID: 10332527.

35. Kockx MM, Wuyts FL, Buyssens N, Van Den Bossche RM, De Meyer GR, Bult H, Herman AG. 1993; Longitudinally oriented smooth muscle cells in rabbit arteries. Virchows Arch A Pathol Anat Histopathol. 422:293–9. DOI: 10.1007/BF01608338. PMID: 8506622.

36. Ábraham A. 1969. Microscopic innervation of the heart and blood vessels in vertebrates including man. Pergamon Press;Oxford:

37. Mompeo B, Maranillo E, Garcia-Touchard A, Larkin T, Sanudo J. 2016; The gross anatomy of the renal sympathetic nerves revisited. Clin Anat. 29:660–4. DOI: 10.1002/ca.22720. PMID: 27090982.

38. Williams JK, Heistad DD. 1996; Structure and function of vasa vasorum. Trends Cardiovasc Med. 6:53–7. DOI: 10.1016/1050-1738(96)00008-4. PMID: 21232275.

39. Chistiakov DA, Ashwell KW, Orekhov AN, Bobryshev YV. 2015; Innervation of the arterial wall and its modification in atherosclerosis. Auton Neurosci. 193:7–11. DOI: 10.1016/j.autneu.2015.06.005. PMID: 26164815.