Extended Pelvic Lymphadenectomy for Prostatic Cancer

0022-534 7/79/1215-0617$02. 00/0 Vol. 121, Ma)

THE JOURNAL OF UROLOGY

Printed in U.S.A.

Copyright © 1979 by The Williams & Wilkins Co.

EXTENDED PELVIC LYMPHADENECTOMY FOR PROSTATIC CANCER MIRCEA GOLIMBU, PABLO MORALES, SALAH AL-ASKARI

AND

JORDAN BROWN

From the Department of Urology, New York University Medical Center, New York, New York

ABSTRACT

Thirty patients with clinically localized prostatic carcinoma underwent extended pelvic lymphadenectomy, including the presacral and presciatic (lateral sacral) areas. The first echelon of pelvic nodes to be involved by metastases was the external iliac, obturator, presacral and presciatic. The deep presacral-presciatic nodes were involved almost as often as the more superficial external iliac-obturator group. Metastases limited only to the deep pelvic nodes were found in 14 per cent of the cases. Pelvic lymphadenectomy has become an accepted method to stage and treat localized prostatic carcinoma. 1- 14 The incidence and most common sites of nodal metastases have been discussed previously 1- 11 but controversy still exists as to the appropriate extent of lymphadenectomy. Most workers limit the dissection to the external iliac, main trunk of hypogastric and obturator areas. 3• 7• 8 • 14 Some include a part of or the entire common iliac1. 2• 4 • 5 and a few others clean the presacral and presciatic (lateral sacral) areas. 10• 15 The external iliac, hypogastric and obturator nodes, alone or in combination, have been reported as the most common sites of nodal metastases.1. 3• 4• 7 • 10 However, the incidence of nodal involvement in the presacral or presciatic areas is not known. According to anatomy textbooks the presacral area, in the concavity of the sacrum, contains 2 to 6 lymph nodes that form a promontorial and a middle hemorrhoidal group. 16 • 17 The presciatic area contains 2 to 4 nodes grouped around the lateral sacral artery, opposite the 2nd and 3rd sacral foramina (see figure). 16 In view of this we extended the usual lymphadenectomy to include the presacral and presciatic areas and, in addition, included the areas around the entire common iliac and branches of the hypogastric vessels. MATERIALS AND METHODS

Extended pelvic lymphadenectomy was done on 30 consecutive patients with histologically proved adenocarcinoma of the prostate. The patients ranged in age from 47 to 75 years, with a mean of 62 years. All patients had undergone preoperative evaluation of serum and bone marrow acid phosphatase, bone scan and skeletal survey; none had a pedal lymphangiogram. Clinical staging was done according to criteria established by Whitmore and Jewett. 11 There was 1 case of clinical stage Al, 9 stage A2, 6 stage Bl, 9 stage B2 and 5 stage C disease. The lymphadenectomy was performed through a midline extraperitoneal approach in 28 patients and transperitoneally in 2. The lymph nodes were collected separately from the common iliac, external iliac, hypogastric and its branches, obturator, presacral and presciatic areas. The tissue removed was examined histologically for the number of lymph nodes and the presence of metastases in each group. SURGICAL TECHNIQUE

A suprapubic midline incision was used. In the extraperitoneal approach the peritoneum was freed from its iliopsoas attachments and reflected upward, exposing the iliac vessels up to the bifurcation of the aorta. In the transperitoneal approach the posterior peritoneum on the right side was incised along the iliac vessels from the aorta to Poupart's

ligament. On the left side the sigmoid colon was mobilized from its lateral aspect and pushed medially to expose the left common iliac vessels and the anterior surface of sacrum from the promontorium to the coccyx. Care was taken not to injure the middle hemorrhoidal vessels that approach the sigmoid colon at this level. Dissection began at the bifurcation of the aorta and followed the common iliac artery and vein, removing all lymph-bearing tissue around both vessels, including the adipose tissue located laterally and posteriorly between the vein and iliopsoas muscle. The dissection continued along the external iliac vessels down to the circumflex vein and included Cloquet's inguinal node. The genitofemoral nerves marked the lateral limit of the dissection on both sides. The hypogastric vessels were approached next and, although the yield was minimal, all areolar tissue surrounding its superior and inferior vesical, gluteal and internal pudendal branches was removed. Obturator nodes were then removed by cleaning the areolar tissue around the obturator nerve from Cooper's ligament to underneath the hypogastric vein. The nerve was preserved carefully but the obturator artery and vein were removed with the specimen. Exposure of the presciatic nerve and the lateral margin of the sacrum, on either side, was accomplished by retracting the bladder medially. All adipose tissue overlying the sciatic nerve and its roots of origin were then removed from the sacral foramina medially to the pelvic wall laterally. Dissection of the upper 2 sacral roots was facilitated by retracting the common iliac vessels medially. Finally, by lifting the sigmoid colon upwards and to the left, the concavity of the sacrum was cleansed of all fibroadipose tissue from the promontorium superiorly, the sacral foramina laterally and the coccyx inferiorly. The middle sacral artery and vein were exposed and clipped occasionally. RESULTS

The number of lymph nodes removed from each patient ranged from 22 to 89, with an average of 43. Fifteen patients (50 per cent) had metastases in 1 or more nodal groups. The number of nodes per group and the metastases were distributed as indicated in table 1. Common iliac area. The number of nodes identified ranged from Oto 14, with an average of 4. In 3 patients there were no nodes found on one side. Metastases were demonstrated unilaterally in 4 cases (27 per cent) in conjunction with metastases in other groups: presciatic in all cases, obturator and external iliac in 3 cases and presacral in 2 cases (tables 1 and 2).

External iliac area. The number of nodes removed ranged between 1 and 24, with an average of 7. Positive nodes were found in 9 cases (60 per cent): unilaterally in 5 and bilaterally in 4. All were associated with metastases to other nodal groups: presacral in 6 patients, presciatic in 5 (unilateral 3

Accepted for publication July 21, 1978. Read at annual meeting of American Urological Association, Washington, D.C., May 21-25, 1978. 617

618

GOLIMBU AND ASSOCIATES

and bilateral 2), obturator in 4 and common iliac and hypogastric in 2. Obturator area. The number of nodes removed ranged between O and 20, with an average of 5.2 per side. The area contained no nodes on one side in 2 patients. Metastases were found in 8 cases (53 per cent). The obturator area was the only site of nodal involvement in 3 patients; in the remaining 5 patients metastases also were present in the presciatic and external iliac group in 4 cases, common iliac in 3, presacral in 2 and hypogastric group in 1 (tables 1 and 3). Internal iliac area. The number of nodes removed ranged

!.

from Oto 7, with an average of2.5. In 2 patients there were no nodes on both sides and in 12 patients there was none on one side. Nodes were not encountered twice as often from the left side (8) as from the right (4). Metastases were identified unilaterally in 2 cases (14 per cent), both in association with involvement of the presacral, presciatic, obturator and external iliac groups. Presciatic area. The number of nodes removed ranged from 1 to 17, with an average of3.5. No lymph nodes were found on both sides in 1 case and on one side in 5 cases. The nodes contained metastases in 7 cases (47 per cent): unilaterally in 4 and bilaterally in 3. Six patients had concomitant involvement of other groups: external iliac in 5 cases, obturator in 4 and presacral in 2. The presciatic nodes were the only site of metastases in 1 case. Presacral area. The number of nodes removed ranged from 0 to 10, with an average of 5. Lymph nodes were not found in 3 patients (10 per cent). Metastases were discovered in 8 cases (53 per cent). The presacral area was the only site of nodal metastasis in 1 case. In the remaining 7 cases most commonly associated metastatic groups were the external iliac, followed by the obturator, common iliac and presciatic. TABLE

2. Incidence of nodal metastases in 15 patients Cases No.(%)

External iliac Obturator Presaeral Presciatic Common iliac Hypogastric External iliac obturator Presacral-presciatic

TABLE

9 (60) 8 (53)

8 (53) 7 (47) 4 (27) 2 (14) 13 (86) 12 (80)

3. Single group metastases in 15 patients Cases No.(%)

· 1) C
2):Elttetnal Ilia~ '3) Internal 4} Obhµ:ator 5) Prescuffic . O) Presactal , '1t,~o~oQ'to,'l'iitl' &} Prostate ~yBladder-

l!tlic ,

Drawing modified from Cuneo and Marcille 16 TABLE

Pt.

No. Nodes

Clinical Stage

MD ER PW DA BF KA

55 44 50 52 45 47 43 44 22 52 46 41 89 55 35 29 25 30 31 59 23 27 32 32 36 22 36 57 80 45

A2 A2 A2 A2 Bl B2 B2 C Bl A2 B2 Bl Bl Al B2 Bl A2 B2 B2 C B2 B2 C C A2 A2 B2 C Bl A2

cw

TS GT WP ST MJ OD

RJ LS FR CL DA DD RS GW KH MI HH PG WW SR KF HC RS

* Positive nodes.

Rt. Common Iliac 7 1 6 5 2 6 3 4 1 4 3 4 7 5 4 1 2 4 2/3* 2 0 3 3* 1 3 0 5 2/4* 2 12

3 (20) 1 (7) 1 (7)

Obturator Presciatic Presacral

1. Number of lymph nodes removed from individual areas

Rt. Exter. Iliac

Rt. Inter. Iliac

7 8 6 4 11 10 7 9 3 5 7 8 20 11 2/5* 2 1/5* 5 3/5* 10 2 3/4* 4 4 5 4 6 8/15* 2/7* 7

2 3 4 3 2 1 0 5* 2 2 3 1 1 3 0 3 0 1 0 2 2 0 1 6 2 0 2 3 2/5* 1

Rt. Obturator 10 4 5 6 4 3 7 6 2 2/7* 3 1 15 7 5 5 2/3* 2 3 5 5/7* 2 4* 1 3 3 4 4/11* 4/8* 4

Rt. Later. Sacral

Presacral

8 0 2 6 5 4 3 4 1 5/7* 6 4 2/17* 5 2 2 0 2 2/4* 3 4 0 2/3* 6 6 1 2 2 3/4* 1

3 2 3 3/4* 1 3 2 1/3* 3 2* 4/6* 0 4 3 2 3 3/4* 5 3* 10 0 3* 0 4 3 3 3 1 6 1

Lt. Common Iliac 4 5 7 6 5 4 5 2 2 2* 4 5 4 3 3 4 5 5 4 4 1 1 4 4 2 2 4 0 14 2

Lt. Exter. Iliac

Lt. Inter. Iliac

Lt. Obturator

4 3 4 5/12* 3 9 4 6* 3 4/12* 2 9 9 5 6 2 2/4* 4 3/4* 5 3 6 6 1 2 5 4 6/7* 1/24*

0 1 3 2 4 2 2 0 2 1 3 0 5 4 2 0 0 0 1 3 1 2 0 0 3 0 1 1 7 0

9 6 7 4 3 5 4 3 0 5 5 6 20 5 3 4 1/2* 2 2 1/11* 1/3* 5 4* 1/3* 4 1 3 4/11* 18 0

16

Lt. Later. Sacral 1 11

3 0 5 1 6 2 3 2/5* 4 3 2 4 2/3* 3 0 0 2*. 4 0 1 3* 2 3 3 2 2* 5 1

EXTENDED PELVIC LYMPHADENECTOMY FOR PROSTATIC CANCER DISCUSSION

Pedal lymphangiogram, 15 ' 18 ' 19 67 gallium scan, 20 pelvic node biopsy 2 ' 13 and lymphadenectomy1-1 2 , 15 have been used to detect regional metastases in clinically localized prostatic carcinoma, The limitations of pedal lymphangiogram and 67 gallium scan include an unacceptable number of falsely negative and falsely positive results, inadequate visualization of hypogastric and obturator nodes and inability to detect microscopic metastatic foci, 10 , 15 , rn, 20 Pelvic lymphadenectomy has remained the only accurate way to assess the pelvic nodes for staging, Its therapeutic role has not been established, However, several reports suggest an increase in the cure rate when micrometastatic lymph nodes are removed, 7 ' 12 Although postmortem studies 21 of advanced stages of prostatic carcinoma showed the highest incidence of metastases in the periaortic nodes, numerous dinicalL '3' 4 , 7 , ,o, 12 and pathologicaF2 observations demonstrate the nodes to be the first involved, observers have the hypogastric or external iliac groups, alone or in combination, to be the most common sites of metastases,'l, 4 , 10 Catalona and Scott refer to the obturator, hypogastric, external iliac and presacral as the primary echelon for nodal metastasis, and the common iliac and para-aortic groups as the second echelon, 14 There is no agreement as to the appropriate extent of lymphadenectomy and suggested areas of dissection range from the entire pelvic retroperitoneum up to the renal pedicle 2 " to limited biopsy of ipsilateral pelvic nodes, 2 ' 4 Whitmore and Mackenzie,3 Donohue and associates/ and Catalona and Scott 14 remove the nodes surrounding the external iliac, main trunk of the hypogastric and obturator vessels, Others include part of or the entire common iliac area L 2' 4 ' 5 and only a few workers have removed the presacral nodes, rn, 15 Cerny and associates have suggested another group of nodes, the lateral sacral, as an important intermediary station for the posterior lymphatic pathways draining into the common iliac groups, 1'' Although amply described in anatomy textbooksw, 17 or research works,2 4 little attention has been given to presacral and presciatic nodes during lymphadenectomy, Consequently, the incidence of their involvement by prostatic carcinoma in comparison with other groups is not known, Our study demonstrated nodal metastases in half of 30 patients with stages A to C prostatic carcinoma, an incidence in agreement with other reported series. Among the 15 patients with nodal metastases the external iliac (60 per cent), obturator (53 per cent), presacral (53 per cent) and presciatic (47 per cent) were the most commonly involved lymph node groups (table 2), The obturator or obturator-hypogastric groups have been regarded as the most commonly involved by other workers using less extended dissection, A comparison of nodal involvement between the superficial and deep pelvic groups shows an almost equal distribution, There were 13 patients (86 per cent) with superficial nodal metastases to either external iliac, obturator or both groups and there were 12 patients (80 per cent) with nodal metastases to either presciatic, presacral or both areas (tables 1 and 2), Single group metastases were found in the obturator nodes in 3 cases (20 per cent) and in presciatic and presacral nodes each in 1 case (7 per cent) (table 3), It is significant that 14 per cent of the cases with metastases had spread only to the deep nodes in the presacral and presciatic areas and none to the superficial nodes. Therefore, staging would have been inaccurate if dissection had not been extended to include the presacral and presciatic areas, It also follows that, if positive, these deep nodes may act as second primaries, producing distant metastases after curative radical prostatectomy, Our study suggests that the first echelon of pelvic nodes to be involved by metastatic prostatic carcinoma is the external iliac, obturator, presacral and presciatic groups, The deeper presacral-presciatic nodes are :involved almost as often as the 1r1ore external iliac-obtu.rator group. f./[etastases

were limited only to the deep pelvic nodes in 14 per cent of the cases, Thus, removal of presacral and presciatic nodes should be included in lymphadenectomy for staging or treatment of prostatic carcinoma, REFERENCES

L Flocks, R, H,, Culp, D, and Porto, R: Lymphatic spread from prostatic cancer, J, UroL, 81: 194, 1959, 2, Arduino, L. J" and Glucksman, M, A: Lymph node metastases in early carcinoma of the prostate, J, UroL, 88: 91, 1962, 3, Whitmore, W, F,, Jr, and Mackenzie, A, R,: Experiences with various operative procedures for the total excision of prostatic cancer. Cancer, 12: 396, 1959, 4, Wilson, C, S,, Dahl, D, S, and Middleton, R G,: Pelvic lymphadenectomy for the staging of apparently localized prostatic cancer, J, UroL, 117: 197, 1977, 5, McCullough, D, L,, Prout, G, R, Jr, and Daly, J, J,: Carcinoma of the prostate and lymphatic metastases, J. UroL, Hl: 65,

1974, 6. 'Varkarakis, M. J., G. P., Nelson, C. lVL K., Chehval, IV.L, Moore, RH, and R, H,: Lymph node involvement in prostatic carcinoma, UroL Clin, N, Amer., 2: 197, 1975, 7, Barzell, W,, Bean, M, A,, Hilaris, B, S, and Whitmore, W, F,, Jr,: Prostatic adenocarcinoma: relationship of grade and local extent to the pattern of metastases, J, Urol., 118: 278, 1977, 8. Donohue, R. E., Pfister, R.R., Weigel, J. W. and Stonington, 0. G,: Pelvic lymphadenectomy in stage A prostatic cancer, Urology, 9: 273, 1977, 9. rvrcCullough, D. L.j McLaughlin, A. P. and Gittes, R. F.: Morbidity of pelvic lymphadenectomy and radical prostatectomy for prostatic cancer, J, Urol., 117: 206, 1977, 10, McLaughlin, A, P,, Saltzstein, S. L,, McCullough, D, L, and Gittes, R, F,: Prostatic carcinoma: incidence and location of unsuspected lymphatic metastases, J, UroL, 115: 89, 1976, 11, Golimbu, M,, Schinella, R, Morales, P, and Kurusu, S.: Differences in pathological characteristics and prognosis of clinical A2 prostatic cancer from Al and B disease, J, UroL, 119: 618, 1978, 12, Hilaris, B, S,, Whitmore, W, F,, Jr., Batata, M, A, and Grabstald, H,: Radiation therapy and pelvic node dissection in the management of cancer of the prostate, Amer, J, Roentgen,, 121: 832, 1974, 13, Ray, G, R, Pistenma, D, A,, Castellino, RA,, Kempson, R. L,, Meares, E, and Bagshaw, M. A,: Operative staging of apparently localized adenocarcinoma of the prostate: results in fifty unselected patients, l, Experimental design and preliminary results, Cancer, 38: 73, 1976, 14, Catalona, W, J, and Scott, W, W,: Carcinoma of the prostate. UroL Dig,, p, 15, October 1977, 15. Loening, S, A, Schmidt, J, D., Brown, R. C,, Hawtrey, C, K, Fallon, B. and Culp, D. A: A comparison between lymphangiography and pelvic node dissection in the staging ofprostatic cancer. cL UroL, 117: 752, 1977, 16, Gray, H,: Anatomy of the Human Body, 27th ed, Philadelphia: Lea & Febiger, Publishers, 1959. 17, Rouviere, H,: Anatomy of the Human Lymphatic System, Translated by M. J. Tobias, Ann Arbor: Edwards Brothers, Inc., 1938, 18, Castellino, RA,, Ray, G,, Blank, N,, Govan, D, and Bagshaw, M.: Lymphangiography in prostatic carcinoma: preliminary observation, J,AM.A,, 223: 877, 1973, 19, Cerny, J, C,, Farah, R, Rian, R and Weckstein, M. L,: An evaluation of lymphangiography in staging carcinoma of the prostate, J, Urol., 113: 367, 1975, 20, Golimbu, M,: "1 Gallium scan for staging of prostatic carcinoma. Presented at annual Valentine Fellowship Award, New York Academy of Medicine, 1975, 21. Arnheim, F, K,: Carcinoma of the prostate: a study of the postmortem finding in one hundred seventy-six cases. J. UroL, 60: 599, 1948, 22, Elkin, IVL and Mueller, H, P,: Metastases from cancer of the prostate; autopsy and roentgenological findings, Cancer, 7: 1246, 1954, 23, Gill, W, R, Marks, J, E,, Straus, F, H,, Sylora, H, 0, and ~u""'V"'-', H, NL: Radical

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sion of stage C to stage B carcinoma of the prostate. J. Urol., 111: 656, 1974. 24. Smith, M. J. V.: The lymphatics of the prostate. Invest. Urol., 3: 439, 1966. EDITORIAL COMMENT The authors have made an important contribution by documenting the high incidence of metastatic disease to the presacral and presciatic lymph nodes. However, the clinical implications of these findings are somewhat unclear. Because 80 per cent of the patients with positive nodes had involvement of either the presacral or presciatic lymph nodes, these lymph nodes must be resected if the lymph node dissection is to be of therapeutic value. However, because anatomical factors may preclude their complete removal, it seems most likely that the major role of lymphadenectomy will be for staging purposes only. Conversely, because the presacral or presciatic nodes were the sole site of metastatic disease in only 14 per cent of the patients, one must seriously consider whether it is wise to perform a more extended operation in an effort to increase the diagnostic ability of a staging procedure that is already 86 per cent accurate. P.C.W.

REPLY BY AUTHORS We agree with the reviewer that a staging procedure that is 86 per cent accurate is, perhaps, acceptable. However, since there is increasing evidence that lymphadenectomy prolongs survival in prostatic cancer, 1- 3 we should strive to make the nodal extirpation as complete as possible. Extended lymphadenectomy adds approximately 30 minutes to the usual operating time and the rate of complications is no different from that of a conventional lymphadenectomy. 1. Bagshaw, M. A.: Radiation therapy for cancer of the prostate.

In: Genitourinary Cancer. Edited by D. G. Skinner and J.B. deKernion. Philadelphia: W. B. Saunders Co., p. 360, 1978. 2. Carlton, C. E., Jr.: Radioactive isotope implantation for cancer of the prostate. In: Genitourinary Cancer. Edited by D. G. Skinner and J. B. deKernion. Philadelphia: W. B. Saunders Co., p. 385, 1978. 3. Barzell, W., Bean, M.A., Hilaris, B. S. and Whitmore, W. F., Jr.: Prostatic adenocarcinoma: relationship of grade and local extent to the pattern of metastases. J. Urol., 118: 278, 1977.