The Use of the Seromuscular Layer of an Ileal Loop for Ureteral Replacement

THE JOURNAL OF UROLOGY

Vol. 88, No. 6 December 1962 Copyright © 1962 by The Williams & Wilkins Co. Printed in U.S.A.

THE USE OF THE SEROMUSCULAR LAYER OF AN !LEAL LOOP FOR URETERAL REPLACEME~T KHALIL TORBEY

AND

WYLA;\;"D F. LEADBETTER

From the Department of Urology, Jl!Iassachusctts General Hospital, Boston, J"\!Iass.

Many attempts have been made experimentally and clinically to replace the ureter by means of tissue fashioned to form a tube: vessels, skin flaps, bladder tubes or fallopian tubes. Replacement of the ureter with ileum marks a new step in reconstructive surgery. The principle of this replacement is based upon the related properties of the ileum and the ureter, upon their anatomical structure and their peristaltic activity. Though the ileum and the ureter have some resemblance and exchangable properties, they are different in many ways, i.e. larger diameter of the ileum and the presence of ileal mucosa (a glandular mucous membrane which absorbs and secretes mucus). 'Wnen transplanted to replace the ureter the intestinal mucus lining remains active and secreting. To obviate these difficulties and render the ileum more suitable as a substitute, Shoemaker1 used a reversed intestinal loop graft, an intestine everted so as to provide a serous lining on the inside, and left the mucous membrane coating the outside of the segment. Thus, he provided a smooth, inactive surface in contact with the flow of urine but left an active secreting surface in contact with the tissues and the posterior abdominal wall . .i\focus accumulated, initiating infection, which was followed by scarring and deformity of the segment. When he stripped the everted loop of its mucous membrane to avoid side-effects, the raw surface led to damaging and deforming adhesions. Benefiting from the experience of Shoemaker, Martin 2 returned to the original idea of an ileal loop graft, but this time stripped of its mucous membrane and cut down in size. To encourage Accepted for publication May 28, 1962. This research was supported by a grant to surgery from the ";\;" ational Institute of Health. 1 Shoemaker, W. C.: Reversed seromuscular grafts in urinary tract reconstruction. J. Ural., 74: 453-475, 1955. 2 Martin, L. S., Duxbury, J. H. and Leadbetter,

W. F.: Uroepithelial lined small bowel as a ureteral substitute. Surg., Gynec. & Obst., 108: 439-449, 1959. 746

growth of bladder transitional epithelium, he covered the internal raw surface of the graft with multiple patch grafts of vesical mucosa. The patches were placed 1 cm. apart and a splint was used for several weeks to facilitate total coverage with transitional epithelium. His later followup report showed that multiple strictures are liable to develop in the small, raw areas left between patches, especially if a few of the mucosa! patches did not take on the intestinal wall. This led to secondary multiple diverticula in the replaced segment. The basic principles were the necessity of securing a continuous, living, smooth, non-active and non-secreting lining to the intestinal segment, and leaving a serous coYer on the outside. Clinically, the ileum has been used in full thickness to replace the ureter with poor results. The width of the lumen provided a reservoir for stagnation of urine and the mucosa remained active. We solved the two main problems of width and urothelial coverage of the inner layer of the ilea! segments stripped of its mucosa by the technique to be described below. This was developed during our studies on the utilization of different types of intestinal loops in uroplastic procedures. 3 • 4 The procedure is done in 2 stages: 1) The isolated ilea! segment is stripped of its mucosa, sutured to the bladder, reconstructed around a mold and brought through the skin to secure total transitional epithelial coverage; 2) simple anastomosis of the distal end with the remaining portion of the collecting system of the kidney is made when the intestinal segment 3 Torbey, K.: Urinary continence and normal urination provided by urethral and sphincter substitution with a special seromuscular segment of ileum in male and female dogs. J. Ural., 82:

717-732, 1960. 4 Torbey, K. and Leadbetter, W. F.: Urinary

continence and normal urination provided by urethral and sphincter substitution with a special seromuscular segment of ileum in male and female dogs. (Motion picture film presented at meeting of American Urological Association, Inc., Chicago, May 16-19, 1960.)

URETER\L REPLACEME="f"r

Fm. 1. 1, Remaining seromuscular layer after stripping, A; Payer's patches removed by knife ing, B; shin)' surface of mucosa! membrane and mucosa stripped, C; whole thickness of intestine its mucosa, D. /2, Glandular intestinal mucosa, A; mucosa! membrane, B; cleavage plane between membrane ti,nd submucosa, C; submucosa, D; muscularis, E (a 1 longitudinal fibers, a 11 tranverse fibers), serosa, B'

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K. TORBEY AND '\V. F. LEADBETTER

in its entire length, its mucosa scratched at one place to afford a holding point and then the entire layer is easily peeled off with a smooth forceps. The loop is subsequently reconstructed with a continuous suture around a mold consisting of a Foley catheter inserted in the bladder through the loop and out to the skin through the stoma. The intestinal segment is then brought down to the level of the bladder and implanted on its posterior surface close to one of the ureteral openings (fig. 2). Implantation of the grafted loop obliquely through the bladder wall to secure a tunnel and prevent later upward reflux of urine was onlv partially successful because of the thickness the intestine. The sutures taken between the grafted loop and the bladder invoked onlv the seromuscular layers. 5 " The other end of the ilea! loop is then brought out to the skin and fashioned to form a stoma at the lateral part of the anterior abdominal wall. Closure of the abdomen was done in a routine way.

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Fm. 2. Anastomosis between ileal segment and bladder. Segment ready for partial replacement. A, il_eal segment. B, bladder. C, arcade of vascular1zat10n. Hemostat is on skin end of ileal segment already disconnected from skin anastomosis. has been proven to be covered by transitional epithelium. TECHNIQUE

Under intravenous nembutal anesthesia the abdomen of a dog was opened through a midline incision. An intestinal loop is selected of suitable length, slightly longer than the dog's ureter, about 30 cm. from the ileocecal junction. The intestines are carefully packed off and the loop is isolated by the usual technique, preserving its arterial arcade vascular supply. The next step is a delicate and essential part of the procedure. The mucous membrane of the isolated ileal loop has to be stripped completely down to the submucous layer (fig. 1). We have found that this is best achieved by temporary clamping of the blood supply to the isolated loop,4 which produces multiple small submucous hemorrhages that will lift up the mucousmembrane and determine an easy plane of cleavage for the mucosa. 5 Therefore, the intestinal loop is opened along its antimesenteric borders 5 Torbey, K. and Leadbetter, W. F.: One year followup after ureteral and bladder replacement in dogs. To be published.

MUCOSAL REGENERA'fION ON TRANSPLANTED ILEAL LOOP

Five days following operation the bladder mucous membrane begins to gro,Y on the internal surface of the intestinal loop. The histological changes involved in this regeneration have been followed both in ureteral replacements and in similar urethroplastic operations. 3 lVfucosal regrowth occurs at the rate of 1 cm./day after the first postoperative week but can be hastened bv the use of a pediculated ,·esical mucous men~brane flap (fig. 3). To obtain the flap, the distended bladder is opened on its posterior surface by an incision that cuts only through its seromuscular !aver. A cleavage plane is then readily demarcatei separating the vesical mucous membrane from the bladder muscle which can be extended laterallY or anteriorly as far as desired. The bladder is then emptied and the selected Viidth and length of mucous membrane cut off to form a pediculated flap that is turned up to cover the inside lining of the intestinal loop. It is secured in place by a few sutures of 00000 plain or chromic catgut and in cases of partial ureteral replacement can be so constructed as to completely cover the grafted intestinal loop. The mucosal regeneration, at first carefully

749

URETERAL REPLACEMENT

(I)

(2)

Fm. 3. 1, Regeneration without pediculated bladder mucosa flap. A, bladder. B, pedicle. C, lumen of ileum covered with urothelium. 2, Pediculated bladder mucosa flap 1 week after surgery adherent to seromuscular layer of ileum progressing to cover it completely. A, bladder. B, bladder mucosa. C, intestinal wall and musculature. D, seromuscular layer of ileum not covered with mucosa. followed by weekly biopsies of the lining of the transplanted loop through its stoma, proved so constant and reliable that the biopsies were soon found unnecessary. Simple inspection of the skin end of the loop at the predicted time was sufficient to determine the readiness of the graft for final anastomosis. The regeneration is a progressive covering of the ileal segment from the bladder to the skin surface. FINAL ANASTOMOSIS

Whenever mucosal coverage of the grafted loop is found to be complete, approximately 5 weeks after the first operative stage, the time varying with the length of the segment, the second stage or final anastomosis is performed. This consists, in the dog, of ureteral resection,

partial or complete, and ureterointestinal anastomosis after freeing the grafted loop from the skin. In patients, the damaged ureter would, of course, have been resected during the first stage and a temporary nephrostomy carried out to allow suitable drainage and treatment during mucosal regeneration. The anastomosis can be performed either by suturing the proximal end of the ureter or the pelvis itself to the side of the upper end of the ileal loop. One could also invaginate the stump of the ureter in the intestinal loop as an end-toend anastomosis approximating only the seromuscularis of both organs. Both methods were satisfactory and no leakage of urine developed with either; however, our preference is for the former because of lesser chance of stenosis.

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FIG. 4. Fourteen months' total ureteral replacement with ileum. A, urethra. B, bladder. C, smooth surface of ileum and bladder mucosa. D, pedicle. E, hypertrophied single kidney. Hemostat used to stretch ileum, displaying regeneration. RESULTS

Functional results. The operation was carried out in 12 dogs. In eight, the intestinal loop was selected with an arterial arcade vascular supply and in the other four a "single vessel loop" was used. 3 Of the first 8 dogs, six had total ureter replacement and two partial lmver end replacement. The functional results as determined by urinary output, urinalysis, indigo carmine excretion, renal tests, electrolyte determinations and excretory urography were excellent. None of the dogs died during a 14 months' followup period and those who were sacrificed at the end of that time were found to have normal kidneys and pelves. The \"esical mucous lining of the grafted ileal loop was complete and smooth at both ends of the bladder and pelvic mucosa respectively. Two dogs were followed for a period of 8 months after contralateral nephrectomy (figs. 4 and 5). The only functioning organ was the compensatory hypertrophic kidney correspond-

FIG. 5. Total ureteral replacement, 14 months postoperatively and 8 months after removal of contralateral kidney, shows total length of ureter and pelvis replaced in 2-stage procedure. Notice thickness of kidney parenchyma and shape of calyces, showing no dilatation and diameter of ileum. Ileum is overcapping remaining stump of pelvis. Urography, using 90 per cent miokane, done on full bladder shows lumen of ureter after excess intake of fluid. ing to the transplanted ureter. There were no changes in the blood chemistry or urine of these dogs. The other four suffered from the high resistance which the tonic single vessel loop opposed to the flow of urine. 3 Hydronephrosis which rapidly became infected developed in all, and a nephrectomy was necessary for survival (fig. 6). Anatomical results. In the 8 dogs with the usual arterial arcade loop transplant, the anatomical results ,vere evaluated by pyelography during life and later at autopsy. In all cases the smooth continuity of the lumen from the ureteral stump to the grafted loop, evident on radiography, was confirmed at autopsy. The only abnormality detected on cystography ,ms the presence of reflux which has been unavoidable in all our cases of ureteral replacements.

URETERAL RffiPLACEMENT

This satisfactory alignment of the ilt al loop with the resected end of the ureter is insured the molding effect of the catheter inserted in the loop at the time of the first stage. The catheter is chosen of such a size as to correspond a]Jproximately to twice the diamcte: of the animal's ureter. The intestinal loop observed later to haYe fitted itself to the molcl without narrowing it surgically. Thr catheter prevents collapse of the looJJ and obliteration ut its lumen adhesion of its raw inner but also adjusts the loop to the desired size for later ureteral anastomosis (figs. 7 am! 8). Histological results. The regeneration of the vesical mucous membrane on the intestinal raw surface has been studied not only in relatio11 t(,. these urctcral replacements, but alsc ill conm,c··· tion with urethral replacement mentioned previously. Our statements are based on obsern,tions in more than 80 dogs. Evidence ,1as erecl either by sacrificing the animals 111 the lattPr cases at appropriate times or hy mucosa! 1

FIG. G. Partial replacement of lower end of ureter, 2-st age procedure. Sample fixed in formalin. A, intestinal pedicle formed of single vessel, contracted. B, hydroureter developed in 2 weeks. C, huge pelvis and destroyed kidney pa.renchyma due to resistance of segment to flow of urine.

FrG. 7. 1, Surgical sample (i weeks postoperatively. Width of ilea! segment molded iuouncl 8GF catlw1 er and regeneration of bladder mucosa on ileum. A, intestinal pedicle. B, width of intestine arnl bladder .mucosa regenerating on its surface. C, bladder wall and mucosa. 2, Surgical sample (i weeks posioperntively. Ileum molded around 22F catheter. Compare with ti,runi 7-1. A, bladder. B, intestinal wall with regeneration of bladder mucosa on its surface. After total regeneration, diameter of ileum remains same unless obstruct.ion occurs.

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the regenerated mucosa was composed of several layers of typical vesical cells firmly adherent to the intestinal submucosa (fig. 13). EVALUATION OF OPERATION

Fw. 8. A, urethra. B, bladder emptied of its contents. C, total replacement of ureter with ileal segment 14 months after transplant on single kidney. Contralateral kidney was removed surgically at time of replacement. D, pedicle of ileal replacement with its arcade sectioned accidentally at time of removal of specimen. E, continuity of ileum. Notice difference in size of normal ileum and diameter of replacement molded around 20F catheter.

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r

through the stoma of the loop in the ureteral operations. Five days following operation, the vesical mucosa is observed to grow steadily at an average rate of 1 cm./day. Its growth pattern was found to conform to the following histological steps: During the first week (beginning from the fifth postoperative day) the only change noticed was the occurrence of multiple small submucous hemorrhages and swelling of the submucosal layer (figs. 9 and 10). This was followed during the next week by the growth of a single layer of racket cells (fig. 11). The following week multiplication of this layer to a transitional 3 to 4 layered epithelium occurred, still fragile and easily peeled off (fig. 12). During the final week

Though our technique involves a 2-stage procedure, we think that it is more reliable and safer than 1-stage operations. It is needless to point out both the theoretical and practical advantages of an ileal loop lined with vesical mucosa, as compared to a full-thickness, full width intestinal graft with chances of infection, electrolyte re-absorption and mucus secretion. In comparison with the multiple patch graft technique reported earlier, 5 the 2-stage procedure advocated here offers greater security. Because of the cutaneous opening of the loop, the mucosa] regeneration can be followed by direct observation and the time of anastomosis decided upon correctly according to the unavoidable individual variations. In the former approach, however, the removal of the intestinal splint is decided by over-all averages which may or may not apply. Some of the patch grafts might not take, leaving a larger raw surface to be covered. This raw surface area is the cause of stricture and subsequent diverticula formation. Therefore, the chances of success of the procedure depend on a splint which could accidently be displaced or removed without the possibility of being replaced. In our procedure the molding of the ileal loop on the Foley catheter allows enough time for the intestine to fit itself to the required size for adequate anatomosis with the different types of ureters encountered. After regeneration of the transitional epithelium on the ileal segment is complete, strictures are unlikely to occur. If the Foley catheter proves too mobile or is accidentally displaced, not only is it easily replaced through the cutaneous opening, but more importantly, its introduction does not peel the newly regenerated mucosa. Because the vesical mucous membrane is growing as a continuous sheet and does not depend on patch grafts to cover raw surfaces, displacement of the catheter is of no serious import if promptly replaced. In the patch graft technique, however, displacement of the catheter or its excessive mobility or its blind early removal will lead to slipping of some of the patches with the high probability of adhesions and strictures developing with secondary diverticula. 5

FIG. \J. Seromuscular layers of ileum immediately after stripping. Comprue with figure 1, 2. A, rnb mucosa. B, rnuscularis.

Fm. 10. 11, swelling in submucosa and coverage of this submucosal layer with gelatinous subskrnee which pealed off after fixation in formalin. Surgical sample 5 days postoperatively. B, muscnbris

75:3

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K. TORBEY AND W. F. LEADBETTER

FIG. 11. Two weeks postoperatively. A, from right to left implantation on gelatinous substance of one layer of racket cells. On right, many layers had grown because of proximity to bladder. B, submucosal layer still swelling. C, intestinal musculature. In summary, 2-stage replacement of the ureters with the seromuscular layers of an ileal loop has proved, in our hands, to be an effective and successful procedure in dogs. It illustrates the po~sibility of surface contact regeneration of transitional epithelium on the seromuseular layer .· ot the stripped ileal segment and the possibility of the ileum to adapt itself to a desired width. It also illustrates a faster method of epithelial regeneration or total coverage of the ileum with a pediculated flap of bladder mucosa.

This epithelial lining is an added property which makes the ileum more suitable for replacement of urinary organs. Ureteral replacement should not be done with a single vessel loop. REFERENCES ANNIS, D.: The use of the isolated ileal segment in urology. Brit. J. Urol., 28: 351-362, 1956. BrTKER, M. P.: Les uretero-ileo-plasties. J. d'urol., 60: 474-540, 1954.

CE ND RON, J.: Chirurgie reconstructive de l'uretere. Remplacement par un segment d'ileon a Lumiere Retrecie. These, Paris, 1955.

URETERAL REPLACEMENT

Fm. 12. Closeup of 4-week specimen. ready formed. B, submucosal layer.

75.J

A, several layers of transitional cell epithelium ul

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{ 1) FIG. 13. 1, Transverse section. 2, Longitudinal section. A, transitional epithelium described in figure 12. B, submucosa. C, muscularis with longitudinal and transverse bundles ("1-B). D, serosa.

URI,TERAL liEPLACJDMENT

C:rnERr, J.: Bladder enlargement through ileocystoplasty. J. Urol., 70: GOO, 1953. C1BERT, J., lhTRA:\'D, L., FORET, J. AND SOLER, A.: La petite vessie des tuberculeux urinaires, donnees anatomiques et physio-pathologiques, leurs incidences sm la technique et les inclicat ions de l 'ileocystoplastic. J. d 'nrol., 60:. 125-143, 195'1. CouYELAJRE, R.: La petite vessie des tuberculeux genitourinaires essai de classification: places Pt variantes des cysto-intestino-pl as ties. J. d'urol., 56: :381-434, 1950. Ccn;YELAIRE, R. · Rur Jes ressources du greffon intestinal en urologie. iVIem. Ac. Chirurgie, 82: G7 4---677, 195G.

CoL'Yl,LAfRE, R. L'ureterostomie cutanee n'est plus une infirmit{, definitive. J. d'urol., 59: :358-:37fi, 1953. DAn;.;, D. JVI. · The process of ureteral repair; a recapitulation of the splinting question. J. Urol., 79: 215, Hl58. FER CT ussoN, J. D. · Massive hydronephrosis treated b>· the interposition of an ilea] graft between renal pelvis and bladder. Brit. J. Urol., 28: ;384-386, l\J5G. FEY, B., BrTKER, M. P. AND LEGRAIN, M.: Etude experimentale du retentissemcnt renal de l'uretero-ileopbstie chez le chien. Congres de l' Association Francaise d 'urologie, Paris, 195G.

FEY, B. AND LEGRAIK. M. · Perturbations elec.t rolytiqtws dans · l 'insuffisance renale en urologie. J. d'urol., 60: 803-Slli, 1954. GOODWIN, w. E., WINTER, C. C. A:',JD TURNER, R. D.: Replacement of the ureter by small intestine: Clinical application and results of the "ilea! ureter". J. Urol., 81: 40G, 195!). HORTON, C. E. A:-,JD Po LITANO, Y .. TJ reteral reconstruction with split skin grafts; an experimental study. Plast. & Reconstruct. Surg., 15: 2fil-273, HJ55 HL'FBIAN, W. L., J\kCoRKLE, H.F. AND PERSKY, L.: Ureternl regeneration following experimental segmental resection. ,J. U rol., 75: 79G, 1956.

Kn,s, R.: Sur 21 cas d 'ileo-cystoplastie. Mem. Acad. chir., 82: 62\l-G42, 1956. E\-ss, R. · L'ileo-ureteroplastie totale dans le trnitement rles hydronephroses geantes. J. d'urol., 63: 732-742, 1957. R., LEGRA!:\[, 1\1., BITKER, lVI. AND PERRIN, : Etude du retentissement sur la fonction renale des plasties intestinales de la voie excretrice urinaire. J. d'urol., 64: 187-200, 1958.

LAPrnEs, J.: Mechanism of electrolyte inbalance following ureterosigmoid transplantation. Surg., Gynec. & Obst., 93: G\H-704, 1951. LEGRAIN, M. · Troubles humoraux par contact de l'urine et cl'une muqueuse intestinale . .J. d'nrnl., 61: 360-372, 1955.

LoRD, J. W., .IR., :+rEFKo, P. L. ANO STJ<;vFJ,,,., A. R .. On bridging a gap in the uret.er by means of a free fascia! transplant over straight vitallinm tube. J. Fro!., 49: 2-Hl, 1943.

MARTIN, L. S.: Uroepithelial lined ileat segnrnnt a bladder replacement; experimental obser . vations ancl brief review of the iiternlun,. J. U rol., 82: c:r3-G50, 1959. McDEmIOTT, W. V., JR.: Diversion of urine to the intestines as a factor in coma. _N'ew Eng . .J. Med., 256: 460-462, lVIELNtKOWF, A. E.: Sur le reimplacement ck l'uretere par une anse isolee de l 'intestin grele Rev. clin. d'urol., 1: GOl, 1912. :'-srsREN, R.: Reconstruction of the uret.er. J lnternat. Coll. Surg., 3: 99, 19-tO. OnEL, H. JVI., FERRIS, D. 0. AND PmrnsTLEY Further observations of the tern of the blood after bilateral moidostom:v. J. Urol., 65: JOl3-1020, PYRAH, L. ::'\.: The use of the ileum in urolog:,· Brit. J. Urol., 28: 3rrn-38:3, 1956. PYRAH, L. N.: Use of segments of mnall and intestine in urological surgen·, with reference to problems of ureterocolic nnast.omosis. J. Urol., 78: G83, 1957 RTCKHA1I, P. P.: The use of the isolated iloal in pediatric urology. Brit. J. Grol., 28: 401, 1956.

ROSENBERG, M. L. AND IlAHU:N, c;. A.· Auto genous vein grafts and venous valves ureter al surgery; an experirncn1 al studc• J. Urol., 70: 434, 195:-l. RovINEsco, I.: Recherches experiment ales sur l'uretPro-ilcoplastie avec greffon ilea.I sern musculaire. J. d'urol., 63: 256-2(i5, 1957. SANDERR, A. R. AND Sc:HEil\, C. J.: The epitheliui morphology of antogenous gn,fts when utilized as ureternl and vesical m1bstitutes in the e;,perimental animal. ,J. Urol. 75: G5U 195(1. SCHEIN, C. J., SAi\DER8, A. R.. AND HuRwJT'I', Experimental reconstruction of ureters, substitution of autogenous pedicled tube grafts. AMA .Arch. Snrg., 73: 47, SHOEMAKER. W. C. AND Bmnrn, ll. · reconst{uction of ureter by a new S. Forum, 6: 615-GHJ, Hl55·. SaoEJ\IAKER, W. C. AND ]l,!L1.R1rccr, H. P : The experimental use of seromuscular grafts in bladder reconstruction . .J. Urn!., 73: :114 :321. HJ55. STRAUSS, A.: An artificial ureter nrnrle from the abd~minal wall. Surg., Gynec. & OhsL, 18: 78, 1914. SWENRON, 0., FISHER, J. H. AND CENDRON, Xew technique in the diagnosis and treatment of megalo-ureter. Surgery, 40: 22:3, 19.SG