Is the pelviureteric junction an anatomical entity?

Is the pelviureteric junction an anatomical entity?

Journal of Pediatric Urology (2013) 9, 123e128 REVIEW ARTICLE Is the pelviureteric junction an anatomical entity? Mark D. Stringer*, Shahed Yassaie ...

421KB Sizes 0 Downloads 95 Views

Journal of Pediatric Urology (2013) 9, 123e128

REVIEW ARTICLE

Is the pelviureteric junction an anatomical entity? Mark D. Stringer*, Shahed Yassaie Department of Anatomy, Otago School of Medical Sciences, University of Otago, PO Box 913, Dunedin, New Zealand Received 22 May 2011; accepted 9 August 2011 Available online 15 September 2011

KEYWORDS Anatomy; Histology; Hydronephrosis; Renal pelvis; Ureter

Abstract Objective: The concept of the pelviureteric junction has existed for more than a century and yet there is no clear anatomical definition of this junction. This systematic review addresses the question of whether the human pelviureteric junction is a discrete anatomical entity. Methods: A systematic literature review was undertaken to investigate the normal gross and microscopic anatomy of the pelviureteric junction using the electronic databases MEDLINE, PubMed, Cochrane Library and Google Scholar. Results: In most individuals there is a gradual transition between the renal pelvis and ureter with no external features indicating the presence of a discrete pelviureteric ‘junction’. Internally, however, luminal mucosal folds are prominent in this region. There is no consensus on the arrangement of muscle fibers at the pelviureteric junction (which may be age-dependent) although some studies suggest a focal thickening in the muscle wall consistent with physiological observations suggesting a high pressure zone capable of regulating urine flow. Studies of innervation have shown no evidence of specialization at this site. Conclusions: There is some evidence that a pelviureteric region can be delineated anatomically and physiologically. However, although it may be a useful clinical concept, there is no sound anatomical basis for an actual pelviureteric junction. ª 2011 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved.

Introduction The concept of a ureteropelvic or pelviureteric junction (PUJ) is well established as a consequence of this region

* Corresponding author. Tel.: þ64 3 479 5992; fax: þ64 3 479 7254. E -m a i l a d d r e s s : m a r k . s t r i ng er @ a na t o m y. o ta g o . a c . nz (M.D. Stringer).

being a common site of urinary tract obstruction, especially in children [1], yet its anatomical basis is unclear. It is not recognized as a discrete entity in anatomical reference texts [2e4]. In the embryo, the region develops from the ureteric bud which also forms the adjacent pelvis and ureter, and so the PUJ does not represent a junction in any developmental sense [5]. Smooth muscle cells appear synchronously in the renal pelvis and ureter at about 12 weeks’ gestation [6]. Unlike the ureter, which undergoes recanalization after passing through a solid phase during early human gestation

1477-5131/$36 ª 2011 Journal of Pediatric Urology Company. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jpurol.2011.08.009

124 [7], the PUJ region probably remains patent throughout development [8]. So, is there any evidence that the human PUJ is a discrete anatomical entity? We have attempted to answer this question by undertaking a systematic review of the literature documenting the structure of the normal human PUJ. The aim of the review is not to analyze the multiple theories concerning the pathogenesis of PUJ obstruction, which broadly fall into structural (intrinsic or extrinsic obstruction) and functional disorders (abnormal smooth muscle function or impaired motility secondary to a deficiency of interstitial cells of Cajal), but instead to focus on the anatomy of the pelviureteric region to critically examine whether the concept of a pelviureteric junction is justified.

Search methods The electronic databases MEDLINE, PubMed, Cochrane Library and Google Scholar (first 10 pages) were searched for relevant English language articles. Search terms comprised “pelviureteral junction” or “ureteropelvic junction” or “pelviureteric junction” or “pelviureteral junction” AND “anatomy” OR “vascular” OR “histology” OR “endoscopy”. “Ureter” AND “anatomy” was searched separately. Papers containing original data were selected and relevant secondary references retrieved from bibliographies. The emphasis was on human studies because of functional differences in pyeloureteral activity between multicalyceal systems (human, pig) and unicalyceal systems (guinea pig, rabbit), and structural species differences in the arrangement of smooth muscle at the pelviureteric region [9]. The following represents a summary of the findings of this systematic review of the normal anatomy of the human pelviureteric region.

Gross anatomy In a study of 200 normal urograms, Jewett (1940) concluded that 14% had a region of discrete narrowing consistent with a PUJ [10]. In the majority of cases, the pelviureteric region was funnel-shaped with no discernible distinction between the renal pelvis and ureter. In a similar study of 500 supine pyelograms, Hanley (1959) found that approximately 90% of cases had a smooth funnel-shaped renal pelvis which merged imperceptibly with the ureter, but in the remainder the renal pelvis was rounded with a clearly definable PUJ [11]. Cadaver studies have yielded conflicting results. Cussen (1967) studied the post-mortem dimensions of 276 ureters from fetuses, infants and children who had no evidence of urinary tract pathology [12]. Defining the PUJ loosely as ‘the narrow site of transition from the larger caliber of the renal pelvis to the smaller caliber of the ureter’, he considered that this transition was usually ‘abrupt and obvious’ but acknowledged that in some specimens it was more gradual. Using a series of probes he determined that the internal diameter of the PUJ was the second narrowest point in the ureter after the ureterovesical junction. In a study of 41 PUJs from adults and children, Foote et al. (1970) were unable to identify the PUJ as a discrete site because of the smooth transition from pelvis to ureter [13].

M.D. Stringer, S. Yassaie In a smaller study, Shafik and Al-Sherif (1999) defined the PUJ as the ‘narrowest lower end of the renal pelvis at its junction with the ureter’ and concurred that it had no definable external features [14]. A gradual tapering of the renal pelvis into the ureter rather than a discrete transition is also evident on endoureteral sonography [15]. Thus, in the vast majority of cases, there are no external features that clearly define a pelviureteric ‘junction’. According to some authors, the PUJ region can be identified from its internal mucosal appearance. Murakumo et al. (1997) noted mucosal folds within seven non-obstructed PUJs removed from patients undergoing nephrectomy for transplant or tumor [16]. In a more systematic study of 25 cadavers, Shafik and Al-Sherif (1999) characterized the PUJ as a region containing ‘crowded mucosal folds’ forming an internal rosette [14]. Folds were smaller and fewer in the adjacent pelvis and ureter. Using this definition, they estimated the mean length of the PUJ as 6.2  1.4 mm (range 5e9 mm). This correlated with a high pressure zone recorded in healthy volunteers (see below).

Muscle wall As with other parts of the ureter, the wall of the pelviureteric region is composed of three layers: an outer adventitia, a smooth muscle layer interspersed with collagen bundles [16], and an inner mucosal layer consisting of urothelium overlying a lamina propria. The orientation of muscle fibers is controversial. From an analysis of PUJs obtained at autopsy from adults and children, Foote et al. (1970) reported a combination of circular, longitudinal and oblique muscle fibers at the PUJ [13]. They noted a gradual transition from a preponderance of circular muscle in the pelvis to a preponderance of longitudinal muscle in the upper ureter. Hanna et al. (1976) studied 28 normal ureters mostly from autopsies and commented that whilst the ureter had an inner longitudinal and outer circular muscle layer, the muscle layer of the PUJ was ill-defined [17]. Kench (1982) studied PUJs from 23 adult cadavers with no known urinary tract pathology and reported no difference in the basic arrangement of muscle between the pelvis and ureter, which was arranged in two poorly defined layers of variable thickness, an inner longitudinal spiral layer and an outer circular layer [18]. Murakumo et al. (1997) similarly reported a muscle coat organized into two layers but did not elaborate on the orientation of these layers [16]. In an elegant and detailed study of 12 autopsy specimens ranging in age from 1 month to adulthood, Kaneto et al. (1991) examined the three-dimensional arrangement of smooth muscle bundles at the PUJ (defined as the site where the uppermost ureter joins the funnel-shaped pelvis) [19]. These authors documented age-related changes in the orientation of muscle fibers. Circular muscle fibers predominated in infants. After 2 years of age, oblique muscle bundles were evident becoming progressively more dominant with increasing age. A thin inner longitudinal muscle layer was identified from 2 years of age. They concluded that the adult pattern of muscle bundles at the PUJ is dominantly one of an oblique mesh with a thin inner layer

Pelviureteric junction

125

of longitudinal muscle and a small proportion of circular fibers. However, in contrast to these findings, Shafik and AlSherif (1999) described two distinct muscle layers at the PUJ, a thicker outer circular muscle layer and an inner longitudinal layer; these muscle layers were distinct from the mixture of spiral and longitudinal fibers in the ureter and pelvis [14]. Not only is the orientation of muscle fibers at the PUJ controversial but so too is the existence of focal muscle thickening at this site. In a histologic study of ureters from embryos and stillborn fetuses, Jewett (1940) found no evidence of muscle thickening at the PUJ [10]. On the other hand, Kench (1982) observed an increase in muscle bulk at the presumptive PUJ in most specimens but provided no quantitative data [18]. Shafik and Al-Sherif (1999) reported a well formed circular muscle layer contributing to a focal increase in muscle thickness at the PUJ, consistent with an anatomic sphincter; these qualitative observations were based on 10 neonatal and 15 adult cadaver specimens [14]. In the absence of quantitative data on muscle thickness it is difficult to reconcile these different findings, although our own histologic observations in cadaver sections tend to support the concept of thicker muscle at the PUJ (Fig. 1). Apart from the study of muscle bundle orientation by Kaneto et al. (1991) [19], there has been only one quantitative analysis of muscle in the PUJ and adjacent urinary tract. In an autopsy study of 380 ureters from children and fetuses with macroscopically normal urinary tracts, Cussen (1967) found that the mean density of smooth muscle cells and the relative proportion of muscle in the wall were greatest in the mid-ureter, directly distal to the PUJ [20].

Normal vascular relationships Given the lack of external landmarks for a PUJ and the conflicting observations on muscle arrangement, do local vascular relationships help to define this junction? Two studies have systematically investigated the vascular relationships of the normal PUJ but neither clearly defined this junction. Sampaio (1998) studied endocasts of 546 kidneys from adult cadavers and noted that 65% had a prominent artery or vein closely related to the anterior surface of the pelviureteric region [21]. In almost a half of these cases this was a normal inferior segmental artery (not an accessory or aberrant artery) coursing anterior to the PUJ before entering the lower pole of the kidney. In 6% of cases there was an artery or vein crossing the posterior aspect of the PUJ; the posterior segmental artery accounted for approximately half of these vessels. In a separate analysis of 266 renal arteries, 7% had an accessory lower polar artery crossing anterior to the PUJ but in only a ‘few’ cases was this artery directly adjacent to the junction. The second study was a retrospective review of endoluminal sonography performed using a 6-Fr catheter in 141 patients with non-obstructed PUJs. Zeltser et al. (2004) found that 19% had a crossing vessel greater than 1 mm in diameter within 5 mm of the PUJ; 41% were anterior, 28% anterolateral, 24% anteromedial, and 7% posterior [22]. These authors attributed differences in their results from

Figure 1 Photomicrographic montage of a longitudinal section through the PUJ from an 87-year-old female cadaver with a macroscopically normal urinary tract (hematoxylin & eosin). Note the thicker muscle in the pelviureteric region.

those of Sampaio’s to differences in the definition of crossing vessels and technical aspects of the study.

Innervation, interstitial cells of Cajal and ‘P’ cells The fact that urine transport from the renal pelvis to the bladder can occur independently of an intact nervous system is apparent in the denervated transplanted kidney [23]. It is mediated by smooth muscle contraction and, in the normal kidney, modulated by an intact nervous system although the relative roles of these two components have been debated for many years [17,24,25]. In the last 30 years, numerous types of nerve fibers and associated neuropeptides have been found in the ureter, rekindling interest in the role of the nervous system [16,25,26]. Studies of human specimens using whole-mount immunohistochemistry have shown the presence of two intercommunicating nerve plexuses in the upper urinary tract: a prominent submucosal plexus and a more diffuse plexus within the smooth muscle layers [27]. Whilst some authors have found the proximal ureter to be less densely

126 innervated than its distal counterpart [26], others have reported a more uniform pattern of innervation throughout the renal pelvis and ureter [27]. These studies, and more detailed analyses of adrenergic, peptidergic, nitrergic, and cholinergic nerves [26,28], have not so far indicated that the PUJ region in humans has a specialized pattern of innervation. Potential pacemaker cells governing motility of the renal pelvis and ureter have received considerable attention in recent years. A popular concept is that pyeloureteral peristalsis is initiated and regulated by pacemaker cells within the calyceal walls [29]. Interstitial cells of Cajal (ICCs) are likely to serve this function since they are involved in the rhythmic propagation of peristaltic activity in the gastrointestinal tract where they were first characterized, acting as a bridge between nerve terminals and smooth muscle cells [30]. Solari et al. (2003) identified ICCs within the circular muscle layer of the PUJ in children, noting a markedly decreased density in specimens from children with PUJ obstruction [31]. Similar findings have been reported by others [32]. Both studies relied on c-kit immunohistochemistry alone for the identification of ICCs, which is potentially misleading, although the morphology of the cells in the report by Solari et al. [31] is consistent with more precise descriptions of ICCs. In a detailed immunohistochemical study, Metzger et al. (2004) recorded evidence of ICCs throughout the muscle layers and lamina propria of the collecting system in 56 specimens (mostly from patients with renal tumors) and noted a gradual reduction in their density from the renal pelvis distally [33]. In addition, some ICC-type cells were noted within the urothelium, but their density increased distally. Notley (1968) first identified the presence of a subpopulation of ’pale’ smooth muscle cells in the ureter and PUJ on transmission electron microscopy [34]. Hanna et al. (1976) characterized these ‘P cells’ ultrastructurally as having sparse mitochondria and myofilaments, and evidence of increased pinocytic activity; these cells were located predominantly in the PUJ region and the authors suggested that they may have a pacemaker function [17]. Dixon and Gosling (1982) subsequently confirmed the presence of two types of smooth muscle cell in the upper ureter and renal pelvis using light and electron microscopy: ‘typical’ smooth muscle cells were found throughout the upper ureter and pelvis and were rich in non-specific cholinesterase whereas ‘atypical’ smooth muscle cells were present only within the inner layer of smooth muscle in the renal pelvis and calyces and were considered to have a pacemaker function [35]. It is unclear from the literature whether P cells and ICCs have been adequately distinguished although some researchers have argued that atypical smooth muscle cells and ICCs form interconnected networks that both drive typical smooth muscle cells [29].

Physiologic studies Shafik and Al-Sherif (1999) measured intraluminal pressure in the renal pelvis and ureter in 13 supine anesthetized adults using a fluid perfused ureteric catheter inserted through a lower polar calyx [14]. Using a mechanized pull-through technique they recorded the following mean basal

M.D. Stringer, S. Yassaie pressures: renal pelvis 5.2  1.3 cmH2O (range 3e7); PUJ 11.8  2.3 cmH2O (range 9e15); and ureter 4.9  1.5cmH2O (range 3e8). The region of higher pressure at the PUJ extended over a mean distance of 6.9  1.5 mm and corresponded closely to the region of the ‘rosette’ like mucosa previously noted. Compliance at the PUJ (change in intraluminal pressure in response to change in intraluminal volume) was measured with a balloon catheter. Balloon distension resulted in a significant pressure increase which was abolished by injection of local anesthetic but not saline. The authors concluded that the pelviureteric region acts as a ‘physiologic sphincter’. The notion of a possible sphincter in the pelviureteric region is supported by limited experimental data in dogs which suggest that contraction at the PUJ prevents backflow during ureteric contraction [36]. Relaxation at the PUJ occurs in response to small increases in renal pelvic pressure. Experiments in dogs and pigs also highlight another physiologic mechanism in the PUJ region. In these animals, renal pelvic contractions occur every few seconds initiated by electrical activity arising from multiple pacemakers in the renal calyces [37e39]. At normal urine flow rates there is a partial block in the propagation of electrical activity at the PUJ whilst at higher flow rates this conduction block disappears, resulting in the propagation of every renal pelvic contraction [40]. Observations from cineradiographic studies of the pelvis and ureter indicate that this gatekeeper function of the PUJ region probably exists in humans too [13].

Other studies Numerous other studies have investigated specific tissue elements in specimens from patients (mostly children) with pelviureteric obstruction, most of which have included normal ureteropelvic tissue segments as controls. These investigations have focused on abnormalities in the arrangement [19], development [41], differentiation [42], and function [43] of smooth muscle cells; the distribution of c-Kit positive ICCs [31]; the type and arrangement of nerve fibers [26e29]; and the distribution of elastin [20,44] and collagen subtypes [16,45,46]. However, none of these studies provide additional evidence that the human PUJ is a discrete anatomical entity.

Conclusions The concept of the pelviureteric junction has been around for more than a century [47] reinforced undoubtedly by the striking appearance of hydronephrosis secondary to pelviureteric obstruction. The existence of a sphincter in this region is a similarly ancient notion [48]. However, the normal anatomy of the pelviureteric region is poorly defined. The definition of the PUJ is not just of academic interest because the length of this junction has been used to guide the extent of excision in congenital PUJ obstruction [49]. This review demonstrates that in most individuals there is a gradual transition between renal pelvis and ureter; prominent mucosal folds may characterize the internal site of transition more precisely. There is also evidence that the muscle wall in this region is thicker and

Pelviureteric junction the bundles orientated more circumferentially (although this may be age-dependent) consistent with physiological evidence of a high pressure zone capable of regulating antegrade and retrograde flow of urine. Thus, there is evidence to suggest that a pelviureteric region can be delineated anatomically and physiologically. Although the pelviureteric or ureteropelvic junction may be a useful clinical concept, there is no sound anatomical basis for its existence.

Conflict of interest The authors have to conflict of interest to declare.

Funding source This systematic review received no funding.

Ethical approval Not required.

References [1] Churchill BM, Feng WC. Ureteropelvic junction anomalies: congenital ureteropelvic junction problems in children. In: Gearhart JP, Rink RC, Mouriquand PDE, editors. Pediatric urology. 2nd ed. Philadelphia: Saunders Elsevier; 2010. p. 248e71. [2] FCAT (Federative Committee on Anatomical Terminology). Terminologia Anatomica. Stuttgart: Thieme; 1998. p. 64. [3] Standring S. Gray’s anatomy: the anatomical basis of clinical practice. 40th ed. Edinburgh: Churchill Livingstone; 2008. p. 1231. [4] Moore KL, Dalley AF, Agur AMR. Clinically oriented anatomy. 6th ed. Philadelphia: Lippincott Williams & Wilkins; 2010. p. 292. [5] Schoenwolf GC, Bleyl SB, Brauer PR, Francis-West PH. Larsen’s human embryology. 4th ed. Philadelphia: Elsevier Churchill Livingstone; 2009. pp. 486e487. [6] Matsuno T, Tokunaka S, Koyanagi T. Muscular development in the urinary tract. J Urol 1984;132:148e52. [7] Ruano-Gil D, Coca-Payeras A, Tejedo-Mateu A. Obstruction and normal recanalization of the ureter in the human embryo. Its relation to congenital ureteric obstruction. Eur Urol 1975; 1:287e93. [8] Alcaraz A, Vinaixa F, Tejedo-Mateu A, Fore ´s MM, Gotzens V, Mestres CA, et al. Obstruction and recanalization of the ureter during embryonic development. J Urol 1991;145:410e6. [9] Gosling JA, Dixon JS. Morphologic evidence that rhe renal calyx and pelvis control ureteric activity in the rabbit. Am J Anat 1971;130:393e408. [10] Jewett HJ. Stenosis of the ureteropelvic juncture: congenital and acquired. J Urol 1940;44:247e58. [11] Hanley HG. The pelvic-ureteric junction: a cine-pyelography study. Br J Urol 1959;31:377e84. [12] Cussen LJ. Dimensions of the normal ureter in infancy and childhood. Invest Urol 1967;5:164e78. [13] Foote JW, Blennerhassett JB, Wiglesworth FW, Mackinnon KJ. Observations on the ureteropelvic junction. J Urol 1970;104: 252e7. [14] Shafik A, Al-Sherif AM. Ureteropelvic junction: a study of its anatomical structure and function. Ureteropelvic junction sphincter? Eur Urol 1999;36:150e6.

127 [15] Bagley DH, Liu JB. Endoureteral sonography to define the anatomy of the obstructed ureteropelvic junction. Urol Clin North Am 1988;25:271e9. [16] Murakumo M, Nonomura K, Yamashita T, Ushiki T, Abe K, Koyanagi T. Structural changes of collagen components and diminution of nerves in congenital ureteropelvic junction obstruction. J Urol 1997;157:1963e8. [17] Hanna MK, Jeffs RD, Sturgess JM, Barkin M. Ureteral structure and ultrastructure. Part I. The normal human ureter. J Urol 1976;116:718e24. [18] Kench P. A morphometric study of the pelvi-ureteric junction and review of the pathogenesis of upper ureteric obstruction. Pathology 1982;14:309e12. [19] Kaneto H, Orikasa S, Chiba T, Takahashi T. Three-D muscular arrangement at the ureteropelvic junction and its changes in congenital hydronephrosis: a stereo-morphometric study. J Urol 1991;146:909e14. [20] Cussen LJ. The structure of the normal human ureter in infancy and childhood. A quantitative study of the muscular and elastic tissue. Invest Urol 1967;5:179e94. [21] Sampaio FJ. Vascular anatomy at the ureteropelvic junction. Urol Clin North Am 1998;25:251e8. [22] Zeltser IS, Liu JB, Bagley DH. The incidence of crossing vessels in patients with normal ureteropelvic junction examined with endoluminal ultrasound. J Urol 2004;172:2304e7. [23] Djurhuus VJC. Editorial comment. Eur Urol 1999;36:150e7. [24] Notley R. The structural basis for normal and abnormal ureteric motility. Ann R Coll Surg Engl 1971;49:250e67. [25] Wang Y, Puri P, Hassan J, Miyakita H, Reen DJ. Abnormal innervation and altered nerve growth factor messenger ribonucleic acid expression in ureteropelvic junction obstruction. J Urol 1995;154:679e83. [26] Edyvane KA, Trussell DC, Jonavicius J, Henwood A, Marshall VR. Presence and regional variation in peptidecontaining nerves in the human ureter. J Auton Nerv Syst 1992;39:127e37. [27] Nemeth L, O’Briain DS, Puri P. Demonstration of neuronal networks in the human upper urinary tract using confocal laser scanning microscopy. J Urol 2001;166:255e8. [28] Rolle U, Chertin B, Nemeth L, Puri P. Demonstration of nitrergic and cholinergic innervation in whole-mount preparations of rabbit, pig, and human upper urinary tract. Pediatr Surg Int 2002;18:315e8. [29] Lang RJ, Tonta MA, Zoltkowski BZ, Meeker WF, Wendt I, Parkington HC. Pyeloureteric peristalsis: role of atypical smooth muscle cells and interstitial cells of Cajal-like cells as pacemakers. J Physiol 2006;576:695e705. [30] Ahmadi O, Nicholson ML, Gould ML, Mitchell A, Stringer MD. Interstitial cells of Cajal are present in human extrahepatic bile ducts. J Gastroenterol Hepatol 2010;25:277e85. [31] Solari V, Piotrowska AP, Puri P. Altered expression of interstitial cells of Cajal in congenital ureteropelvic junction obstruction. J Urol 2003;170:2420e2. [32] Yang X, Zhang Y, Hu J. The expression of Cajal cells at the obstruction site of congenital pelviureteric junction obstruction and quantitative image analysis. J Pediatr Surg 2009;44: 2339e42. [33] Metzger R, Schuster T, Till H, Stehr M, Franke FE, Dietz HG. Cajal-like cells in the human upper urinary tract. J Urol 2004; 172:769e72. [34] Notley RG. Electron microscopy of the upper ureter and the pelvi-ureteric junction. Br J Urol 1968;40:37e52. [35] Dixon JS, Gosling JA. The musculature of the human renal calices, pelvis and upper ureter. J Anat 1982;135:129e37. [36] Shafik A. Pelviureteral inhibitory reflex and ureteropelvic excitatory reflex: role of the two reflexes in regulation of urine flow from the renal pelvis to the ureter. Neurourol Urodyn 1997;16:315e24.

128 [37] Morita T, Ishizuka G, Tsuchida S. Initiation and propagation of stimulus from the renal pelvic pacemaker in pig kidney. Invest Urol 1981;19:157e60. [38] Tsuchida S, Morita T, Harada T, Kimura Y. Initiation and propagation of canine renal pelvic peristalsis. Urol Int 1981; 36:307e14. [39] Griffiths DJ, Notschaele C. The mechanics of urine transport in the upper urinary tract. 1. The dynamics of the isolated bolus. Neurourol Urodyn 1983;2:155e66. [40] Djurhuus JC, Constantinou CE. Chronic ureteric obstruction and its impact on the coordinating mechanisms of peristalsis (pyeloureteric pacemaker system). Urol Res 1982;10: 267e70. [41] Jenkins D, Caubit X, Dimovski A, Matevska N, Lye CM, Cabuk F, et al. Analysis of TSHZ2 and TSHZ3 genes in congenital pelviureteric junction obstruction. Nephrol Dial Transplant 2010; 25:54e60. [42] Hosgor M, Karaca I, Ulukus C, Ozer E, Ozkara E, Sam B, et al. Structural changes of smooth muscle in congenital ureteropelvic junction obstruction. J Pediatr Surg 2005;40: 1632e6. [43] Cutroneo G, Arena S, Anastasi G, Cervellione RM, Grimaldi S, Di Mauro D, et al. Altered cytoskeletal structure of smooth

M.D. Stringer, S. Yassaie

[44]

[45]

[46]

[47]

[48]

[49]

muscle cells in ureteropelvic junction obstruction. J Urol 2011;185:2314e9. Kim DS, Noh JY, Jeong HJ, Kim MJ, Jeon HJ, Han SW. Elastin content of the renal pelvis and ureter determines postpyeloplasty recovery. J Urol 2005;173:962e6. Yoon JY, Kim JC, Hwang TK, Yoon MS, Park YH. Collagen studies for pediatric ureteropelvic junction obstruction. Urology 1998;52:494e8. Kim WJ, Yun SJ, Lee TS, Kim CW, Lee HM, Choi H. Collagen-tosmooth muscle ratio helps prediction of prognosis after pyeloplasty. J Urol 2000;163:1271e5. Poulakis V, Witzsch U, Schultheiss D, Rathert P, Becht E. History of ureteropelvic junction obstruction repair (pyeloplasty). From Trendelenburg (1886) to the present. Urologe A 2004;43:1544e59 [German with English abstract]. Begg RC. Physiological variations in pyelograms commonly interpreted as pathological; a revised standard of normality, with special reference to the cystoid theory. Br J Urol 1946; 18:176e88. Harish J, Joshi K, Rao KL, Narasimhan KL, Samujh R, Choudhary SK, et al. Pelviureteric junction obstruction: how much is the extent of the upper ureter with defective innervation needing resection? J Pediatr Surg 2003;38:1194e8.