Distribution of Nodal Metastases in Nonseminomatous Testis Cancer

0022-5347 /82/1282-0315$02.00/0

THE

Vol. 128, August Printed in U.S.A.

JOURNAL OF UROLOGY

Copyright© 1982 by The Williams & Wilkins Co.

DISTRIBUTION OF NODAL METASTASES IN NONSEMINOMATOUS TESTIS CANCER JOHN P. DONOHUE, JAMES M. ZACHARY

AND

BARNEY R. MAYNARD

From the Department of Urology, Indiana University School of Medicine, Indianapolis, Indiana

ABSTRACT

The distribution of 104 consecutive stage II (or B) nonseminomatous germinal cell testis tumor deposits in the retroperitoneal space has been analyzed and segregated into 11 anatomic zones of spread: 1) right para-caval, 2) right pre-caval, 3) inter aortocaval, 4) left pre-aortic, 5) left paraaortic, 6) right (renal) suprahilar, 7) left suprahilar, 8) right iliac, 9) left iliac, 10) inter iliac (prelumbosacral) and 11) gonadal vein. Each patient had no treatment after orchiectomy and before retroperitoneal lymph node dissection, that is no preoperative radiotherapy or chemotherapy, which may have influenced histologic analysis. Each patient had an extended bilateral retroperitoneal lymph node dissection, including both suprahilar zones. Tumor deposits in these 11 nodal zones were correlated with the side of the primary lesion (right versus left side) and the extent of metastatic disease (Bl, B2 or B3). The inter aortocaval zone, just below the left renal vein, is the most common site of tumor deposition (93 per cent) of right testis tumors (primary right side). The pre-aortic (88 per cent) and left para-aortic (86 per cent) areas are the most common sites of left testis tumor nodal spread (primary left side). The right and left suprahilar zones are involved rarely in low stage (Bl) disease. No suprahilar nodes were positive in stage Bl disease if the primary was on the right side and only 3 of 14 were positive with Bl disease on the left side. However, in stage B2 disease the suprahilar zones were involved more often with tumor (13 to 33 per cent if the primary was on the right side and 16 to 42 per cent if the primary was on the left side). There is a positive correlation between extent of disease and involvement of suprahilar nodes. A significant number of gonadal veins and their lymphatics are involved with tumor (14 to 17 per cent), even in low stage disease (8 to 14 per cent). The ipsilateral iliac areas rarely are involved with tumor in low stage disease (0 to 14 per cent), and contralateral iliac involvement is a rarity (1 of 40). Also, contralateral (right para-caval if the primary is on the left side or left para-aortic if the primary is on the right side) nodes were negative in low stage disease but commonly positive in B2 disease, especially when the primary was on the right side. The lymphatic drainage of the testis follows predictable and preferential pathways. This clinical study confirms earlier lymphangiographic studies here and abroad, suggesting abundant crossover and subsequent suprahilar drainage. However, suprahilar nodes are so rarely involved in low stage (Bl) disease that dissection in this area is unnecessary in routine staging retroperitoneal lymphadenectomy. Lymphatic drainage of the testicle has been a subject of interest to anatomists and surgeons for centuries. 1- 9 The first systematic experimental study in our language seems to be that of Jamieson and Dobson in 1910. 10 In the 1960s European and American investigators used lymphangiography to study details of testicular lymphatic drainage. In 1963 and 1965 Busch and associates reported their studies on the visualization of human testicular lymphatics. 11 • 12 These studies revealed primary zones of spread not shown on pedal lymphangiography. However, abundant intercommunication among the nodes from the primary testicular lymphatics quite promptly filled retroperitoneal nodes common to pedal and testis drainage. Chiappa, 13• 14 Tavel15 and W ahlqvist1 6 and their associates confinned and added to these observations. Because of these studies, which suggested suprahilar drainage and crossover (particularly right to left side), we became concerned about the clearance of the appropriate nodes, particularly if a right thoracoabdorninal approach is used since this did not afford easy exposure in the contralateral para-aortic suprahilar zones. Also, at this time 1 patient had a clinical relapse of a large retro-pancreatic mass above the renal hilus Accepted for publication August 14, 1981.

after dissection of negative nodes from the renal veins caudad. 17 Therefore, we were stimulated to develop a reliable technique for bilateral suprahilar clearance, as well as the standard infrahilar clearance previously described. 9 • 15• 18 Postmortem retroperitoneal dissections were done to determine what exposure techniques would be useful in perfonning such a procedure. The evolution of this procedure and the technique to obtain good pancreatic mobilization and high exposure in the suprahilar zone through the transabdominal approach have been described elsewhere. 19 MATERIAL AND METHODS

About 275 retroperitoneal lymphadenectomies have been performed by 1 ofus (J.P. D.) with this technique. The studies were segregated into 3 major groups: 1) those with negative nodes, 2) those with positive nodes and 3) those with extensive initial disease (stage C or B3) for which preoperative cytoreductive chemotherapy had been given. Groups 1 and 3 were excluded from this study. Group 2 cases, which were suitable for analysis, had not had treatment but had documented nodal disease. The influence of radiotherapy and chemotherapy in ablating micrometastatic deposits rendered group 3 cases unsuitable for this report but are the subject of another report. 20

315

316

DONOHUE, ZACHARY AND MAYNARD

The technique of retroperitoneal lymphadenectomy used is an extended bilateral dissection, including both suprahilar zones, both infrahilar zones with the lateral margins being either ureter and both iliac zones to the bifurcation of the hypogastric and external iliac arteries. The tissue then was subdivided into 11 segments after its removal for zonal analysis. These zones included 1) right para-caval, 2) pre-caval, 3) inter aortocaval, 4) pre-aortic, 5) left para-aortic, 6) right suprahilar (inter aortocaval above the right renal artery), 7) left suprahilar (left para-aortic above the left renal artery), 8) right iliac, 9) left iliac, 10) inter iliac and 11) gonadal vein (fig. 1). The method used by Ray and associates in describing nodal distribution has been used. 21 Our report differs from theirs only in that a full bilateral dissection was done in all cases and these were extended to include both suprarenal-hilar zones. This extended dissection was used in an attempt to report the entire retroperitoneal nodal distribution in testis cancer, providing for study of the suprahilar and contralateral zones, as well as those areas reported earlier. 21 The 11 zones then were analyzed for metastatic deposits in each of the 3 major subsets of nodal involvement: Bl disease<5 positive nodes and no gross disease >2 cm., B2 disease-i;;:5 positive nodes and/ or gross nodal disease >2 cm. and B3 disease-massive abdominal tumor, usually palpable abdominally. Each zone also was analyzed independently relative to whether the primary tumor was on the right or left side. Variables were controlled as far as possible. All dissections were done by the same surgeon or under his direct supervision, and the same pathologists did the gross and histologic reporting. Every effort was made to do each procedure in the standard manner reported earlier.

A

Right side, stage B-1

8

RESULTS

The distribution of positive lymph nodes has been analyzed relative to the side of the primary tumor and the retroperitoneal tumor stage (Bl, B2 or B3). These 2 parameters were then plotted against the 11 possible zones. Analysis of these data reveals several prevalent findings. I. Lymphatic drainage from the right side tends to be midline, with primary zones of involvement being inter aortocaval, pre-caval and pre-aortic in that order (fig. 2). In no case oflow

Rtght side, stage B-2

C

Right side.stage B-3

Fm. 2. Positive nodes in right testis tumors. A, stage Bl. B, stage B2. C, stage B3. Each circle represents patient with positive node(s) in zone. Space limitations require spreading circles, so they may not have been found precisely in spot noted. Patients with B2 and B3 disease had positive nodes in several zones. Also, if large node extended into several zones each was credited as positive.

Fm. 1. Retroperitoneum represented schematically. Aorta and inferior vena cava are separated to allow placement of markers and numerals. For nodal distribution study this area has been segregated arbitrarily into 11 zones: 1) right para-caval, 2) pre-caval, 3) inter aortocaval, 4) pre-aortic, 5) left para-aortic, 6) right suprahilar, 7) left suprahilar, 8) right iliac, 9) left iliac, 10) inter iliac and 11) gonadal vein.

stage disease, Bl with no gross tumor enlargement, was there any suprahilar nodal involvement. However, with more extensive B2 disease (gross enlargement and >5 nodes) suprahilar nodes were involved more often. In 33 per cent of the cases high posterior nodes were noted at and above the right renal artery and 13 per cent had even crossed over to involve the left

317

NODAL METASTASES IN NONSEMINOMATOUS TESTIS CANCER

A

Left side, stage B-1

8

Left side, stage B-2

C

the right side has a predilection for the midline. As one views right gonadal venous insertions the predominant pattern is mid caval below the renal veins and the flow of lymph is medial at this point rather than lateral. These clinical data confirm earlier reports_ 11-14, 16 II. Lymphatic drainage from the left side reveals a marked predilection for the left para-aortic and pre-aortic zones in cases of low stage disease and extension to the inter aortocaval zone as well in stage B2 disease (fig. 3). This finding is not surprising in view of the more lateral insertion into the left renal vein. Again, rare involvement of suprahilar nodes is noted in low stage Bl disease. In fact, only 1 case in the 100 analyzed had a solitary true suprahilar node involved in the presence of negative infrahilar nodes. There were 2 other Bl cases with suprahilar nodal involvement, for a total of 3 of 14, but these 2 cases also had positive nodes below the hilus as well as just above the renal artery low in the suprahilar zone. It could be argued that these are essentially hilar nodes in contiguity with the renal artery, which can be visualized by elevation of the renal vessels at the time of dissection. III. With advanced stage B2 disease, suprahilar nodes were involved much more frequently. Again, this is not surprising in view of the high insertion of the left gonadal vein. In 42 per cent of the cases (8 of 19) the left suprahilar zone was involved and 3 of 19 cases (16 per cent) had crossed over the aorta and involved the right suprahilar zone just above the right renal artery. Also, there is a clear trend for more advanced disease on the left side to cross to the midline, particularly to the deep or posterior set of nodes in the inter aortocaval zone in cases of more advanced disease. All 19 patients (100 per cent) with stage B2 disease had involvement in this area. However, it is of interest that there were no contralateral positive nodes in the face of negative ipsilateral nodes. IV. A significant number of gonadal veins were involved with tumor, particularly in cases of advanced disease. Over-all, 14 per cent of gonadal venous lymphatics were involved with either nodal or lymphatic disease on the right side and 17 per cent on the left side. It is noteworthy that even in low stage disease 2 of 14 on the right side and 2 of 26 on the left side still had elements of tumor associated with them. Hence, it appears imperative that the ipsilateral gonadal vein be removed generously, together with all of its investing lymphatics, in every case (table 1). V. The iliac areas were involved rarely in low stage disease and contralateral iliacs were not involved except for 1 case, TABLE

1. Incidence ofpositive nodes related to zone and stage Bl No. (%)

B2 No. (%)

B3 No. (%)

Totals (No. (%)

Primary tumor rt. side

Left side, stage B-3

Fm. 3. Positive nodes in left testis tumors. A, stage Bl. B, stage B2. C, stage B3. Each circle represents patient with positive node(s) in zone. Space limitations require spreading circles, so they may not have been found precisely in spot noted. Patients with B2 and B3 disease had positive nodes in several zones. Also, if large node extended into several zones each was credited as positive.

suprahilar zone. Also, there were no true contralateral nodes only, that is in no case with tumor on the right side was a contralateral left para-aortic zone found positive if the inter aortocaval nodes were negative. This finding also is true of iliac drainage, which rarely is involved in low stage disease (4 per cent) and never involved on a solitary contralateral basis when the ipsilateral nodes are negative. Therefore, lymphatic flow on

Rt. para-caval Pre-caval Inter aortocaval Pre-aortic Lt. para-aortic Rt. suprahilar Lt. suprahilar Rt. iliac Lt. iliac Inter iliac Gonadal

3/26 (12) 12/26 (46) 23/26 (88) 6/26 (23) 1/26 (4) 0/26 (0) 0/26 (0) 1/26 (4) 1/26 (4) 0/26 (0) 2/26 (8)

Rt. para-caval Pre-caval Inter aortocaval Pre-aortic Lt. para-aortic Rt. suprahilar Lt. suprahilar Rt.iliac Lt.iliac Inter iliac Gonadal

0/14 (0) 0/14 (0) 4/14 (29) 10/14 (71) 11/14 (79) 1/14 (7) 2/14 (14) 0/14 (0) 2/14 (14) 0/14 (0) 2/14 (14)

6/24 23/24 23/24 21/24 3/24 8/24 3/24 4/24 2/24 2/24 3/24

(25) (96) (96) (88) (13) (33) (13) (17) (8) (8) (13)

8/8 8/8 8/8 8/8 2/8 5/8 3/8 6/8 2/8 3/8 3/8

(100) (100) (100) (100) (25) (63) (38) (75) (25) (38) (38)

17/58 43/58 54/58 35/58 6/58 13/58 6/58 11/58 5/58 5/58 8/58

(29) (74) (93) (60) (10) (22) (10) (19) (9) (9) (14)

0/9 5/9 8/9 9/9 9/9 6/9 9/9 1/9 6/9 1/9 3/9

(0) (56) (89) (100) (100) (67) (100) (11) (67) (11) (33)

1/42 14/42 31/42 37/42 36/42 10/42 19/42 2/42 14/42 1/42 7/42

(2) (33) (74) (88) (86) (24) (45) (48) (33) (2) (17)

Primary tumor lt. side 1/19 9/19 19/19 18/19 16/19 3/19 8/19 1/19 6/19 0/19 2/19

(5)

(47) (100) (95) (84) (16) (42) (5)

(32) (0)

(11)

318

DONOHUE, ZACHARY AND MAYNARD

right to left side (1 of 26). VI. Because this report involves complete bilateral dissection in every case with the ureters as the lateral margins, we consider the contralateral side to be right para-caval in cases of tumors on the left side and left para-aortic in cases of tumors on the right side. We had no contralateral tumors involved in cases of low stage disease with the primary in the left testis and only 1 in left high stage disease. Conversely, if the tumor originated in the right testis contralateral (left para-aortic) involvement was rare but did occur once in low stage disease (1 of 26 in Bl disease) and more often in high stage disease on the right side (3 of 24 in B2 and 2 of 8 in B3 disease). This supports lymphangiography data, showing a strong trend on the left side in drainage from the right testis. Pre-aortic and post-aortic crossover is not uncommon in more extensive disease on the right side. However, there were no contralateral (left para-aortic) solitary positive nodes in the face of negative inter aortocaval TABLE

or pre-aortic nodes from primary testis tumors on the right side (table 2). VII. The histology of metastasis in the nodes generally parallels that of the primary tumor (table 3). However, the great potential for these tumors to express themselves in a variety of histologic forms is shown. For example 49 embryonal carcinomas were reported as having simply embryonal carcinoma in the testis. However, 4 cases were reported as revealing seminoma, 2 teratoma and 3 mixed with embryonal, choriocarcinoma and seminoma in the nodal metastases. Also, a variety of primary presentations involving mixed tumors (for example embryonal, teratocarcinoma and seminoma) represented themselves in a similar variety of tumor elements, usually one of the original elements being predominant. This simply confmns the earlier work of Ray and associates, indicating the potential for varied histology in the metastases of these nonseminomatous germinal cell tumors. 21

2. Positive nodes related to primary side, retroperitoneal

DISCUSSION

sides and stage B subsets Rt. side: Ipsilat. only (inter aortocaval, precaval, pre-aortic, rt. suprahilar, rt. iliac, inter iliac, gonadal vein) Ipsilat. and contralat. Contralat. only (para-aortic, It. iliac, It. suprahilar) Lt. side:• Ipsilat. only (para-aortic, pre-aortic, It. suprahilar, It. iliac, inter iliac, gonadal vein) Ipsilat. and contralat. Contralat. only (inter aortocaval, precaval, para-caval, rt. iliac) Lt. side:t Ipsilat. only (para-aortic, pre-aortic, inter aortocaval, It. suprahilar, It. iliac, inter iliac, gonadal vein) Ipsilat. and contralat. Contralat. only (pre-caval, para-caval, rt. iliac)

Bl

B2

B3

Totals

25/26

19/24

5/8

49/58

1/26 0/26

5/24 0/24

3/8 0/8

9/58 0/58

10/14

0/19

1/9

11/42

3/14 i/14

19/19 0/19

8/9 0/9

30/42 1/42

13/14

10/19

2/9

25/42

1/14 0/14

9/19 0/19

7/9 0/9

17/42 0/42

The purpose of this study was to determine if the suprahilar nodal zones were important in staging and/ or treating patients with testis tumors by retroperitoneal lymphadenectomy. It also was designed to study the importance of contralateral nodal involvement in the aortocaval and iliac areas. We believe the evidence is now at hand to make several observations. First, the patterns of metastatic spread are fairly predictable. Earlier spermatic cord dye injections nicely revealed the major zones of spread on either side. 1• 11• 14• 16 This clinicopathologic study confirms these earlier investigative lymphangiography reports. There is a remarkable absence of suprahilar nodal involvement in low stage disease, particularly if the primary is on the right side. It also is quite low on the left side and, in fact, only 1 in 100 cases had a solitary positive node on the crus above the hilus of the kidney when the infrahilar nodes were negative. The low incidence of suprahilar involvement from either the left or right side then indicates that routine lymphadenectomy in this area is simply not worthwhile in staging nonseminomatous testis cancer if the retroperitoneum has no grossly enlarged nodes when exposed surgically. On the other hand, if there appears to be gross involvement of nodes in the retroperitoneum

• Memorial Sloan-Kettering definition. t Indiana definition.

TABLE

3. Histology of primary tumor related to histology of metastatic nodes Metastasis

EmChoEmbryonal Ca Ca Primary Tumor CNo. S . Em- Tera- bryonal Embryonal Ca Embryonal Ca Embryonal Ca rioca. ± Yolk + Teratoca. + Fibrous + Teratoca. + Embryonal al ases erm- b Ca+ + Teratoca. ± + Chorioca. ± + Yolk Sac± noma Chorioca. ± toma SemiSemi- Sac Yolk Sac± Seminoma Seminoma Seminoma noma Seminoma Seminoma noma

rye:

Seminoma Embryonal Ca Teratoma Chorioca. Yolk sac Embryonal Ca +

2 49 9 2 1 6

2 4

37 1

2 5

3 1

1 2

1

1

1

1

1

1

1 2

1

1

seminoma

Embryonal Ca + teratoca. ±

14

5

2

1

5

1

seminoma

Embryonal Ca + chorioca. ± seminoma Embryonal Ca + teratoca. + chorioca. ± seminoma Embryonal Ca + yolk sac Teratoca. + yolk sac Teratoca. + seminoma Embryonal Ca + teratoca. + yolk sac

2

6

2

3

1

1

1

2

3 3

2

2 1

1 1

2

319 an incn,ased incidence suggests that extension of the node dissection to include this area may be of some therapeutic benefit. The specialized exposure techniques required for good exposure in the suprahilar zones have been described. 19 Aortic retraction and elevation after lumbar arterial division, gentle anterior elevation of the renal arteries and, rarely, crural muscle incision in bulky disease will expedite dissection of suprahilar nodes. It should be emphasized that most positive suprahilar nodes are retrocrural. Progression of disease into the chest is through the aortic hiatus formed by the crura of the diaphragm. One advantage of the midline extended technique in all cases to this point has been the provision of standard surgical treatment and identical pathologic mapping of all 11 zones in every case. Marginal or peripheral zone metastases have been detected, especially in advanced disease, which might have been missed otherwise. The real value of this technique has been to provide definite information on the entire retroperitoneal space for all tumors at every stage (Bl, B2 and B3). Also, in grossly low stage disease the need for a full contralateral dissection is doubtful. The absence of positive contralateral nodes only, if ipsilateral nodes are negative, has been confirmed again. Ray and associates showed this in their study. 21 A difference in definition of contralateral between that report and this refers to the inter aortocaval zone. This zone was considered contralateral relative to the left side when Ray and associates reported drainage from the left side. It was considered ipsilateral when reporting the right side by that group and we would agree that it is ipsilateral when referring to drainage from the right side. Because we report bilateral dissections we consider the inter aortocaval zone central when viewing the retroperitoneum. In the left pre-aortic zone lymphangiogram data show almost immediate drainage to this area after initial left para-aortic infrarenal filling. 11 ' 13• 16 We would suggest that the inter aortocaval zone be considered a common zone to the right and left sides, and, therefore, ipsilateral when referring to tumors on the right or left side. Our pathologic data and earlier lymphangiographic reports clearly suggest that this is a commonly shared central zone for both sides. It would be more accurate, in our opinion, to consider only the pre-caval and right para-caval zones as contralateral when referring to drainage f:rom the left side. If the central inter aortocaval zone were to be called contralateral, all B2 cases with tumors on the left side would have been contralateral. This prevalence suggests that the term contralateral is inappropriate for this basically central zone in either case. It appears that a routine staging retroperitoneal lymphadenectomy in clinical stage A cases can be limited to the zones as described by Ray and associates. 21 In cases with tumor on the left side this would involve full dissection in and around the renal vessels on the left side, extending to the mid pre-caval zone, omitting the right para-caval, right iliac and suprahilar zones. Conversely, the left para-aortic, left iliac and, in low stage disease, suprahilar zones can be omitted when dissecting a lesion on the right side. As our philosophy embraces the concept that in addition to pathologic staging retrope:ritoneal lymphadenectomy is therapeutic when nodes are positive a full extended bilateral dissection, including bilateral sup:rarenal hilar dissections, would be appropriate only in cases of gross nodal involvement. However, if we can discern truly bulky, massive nodal involvement with preoperative staging (such as computerized tomography scan or palpation) we would recommend preoperative treatment with combination chemotherapy. 22 Also, if the surgeon is confronted at the time of exploration with much more extensive disease than anticipated it is reasonable to abandon the procedure at that point in view of the excellent combination chemotherapy now available for extensive disease. Secondary cytoreductive surgery is far more effective when the extensive disease is cytoreduced chemically to smaller gross dimensions. On the other hand, if the disease appears easily resectable there is no

reaSOTI

Why

O"Pt·w,nP1'e1".,,nPPil

completed and the assigned an active chen,otherapy program. Our experience indicates that relapses are high when dealing with extensive disease and adjuvant chemotherapy would be reasonable in such cases. However, we have pointed out that even if adjuvant chemotherapy is withheld salvage of subsequent relapse is highly effective if combination chemotherapy programs are used at that point. 23 Abdominal relapse is uncommon after a thorough retroperitoneal lymphadenectomy. These data would support the principle that a more limited dissection is reasonable if retroperitoneal lymphadenectomy is done for staging only in low level disease. However, it is possible that if the dissections are limited the future may be greeted by an increased incidence of abdominal relapse. The retroperitoneal space is difficult to monitor and relapses in this area may achieve extensive proportions before discovery. Our computerized tomography scans combined with markers currently are inaccurate in detection of nodal disease at the 30 per cent level (30 per cent false negatives).24 Therefore, if these more limited dissections are to be used, it would seem prudent to link them with effective adjuvant chemotherapy programs in every positive case. The last decade has revealed improved results in centers where there was also therapeutic intent to retroperitoneal lymphadenectomy. While this may be contributory to improved results it is clear that the major impetus to these better survival figures is more effective combinations of drugs. Therefore, at relapse most of our patients have been salvaged. Again, if more limited dissections are to be done (for example modified bilateral and infrahilar) effective adjuvant prog--.rams should be linked to these when the nodes are found positive. 25 Conversely, in full dissections adjuvant chemotherapy has been withheld without survival disadvantage in 1 report. 23 However, this approach is controversial. The ideal is to have 100 per cent survival and the best quality of life possible. Our current randomized study regarding adjuvant chemotherapy in stage B disease may provide the answer regarding survival, relapse rate and quality of life after retroperitoneal lymphadenectomy resection of stage B disease. 23 REFERENCES

1. Stinson, J. C.: A new operation for malignant disease of the testicle-the necessity of a more extensive operation than castration for carcinoma, sarcoma, etc. of the testicle. Med. Record, 52: 623, 1897. 2. Roberts, J. B.: Excision of the lumbar lymphatic nodes and sper-

matic vein in malignant diseases of the testicle. Amer. J. Surg., 36: 539, 1902. 3. Bland-Sutton, J .: An improved method of removing the testicle and spermatic cord for malignant disease. Lancet, 2: 1406, 1909. 4. Howard, R.: Malignant disease of the testis. A clinical study of 57 cases. Practitioner, 79: 794, 1907. 5. Chevassu, IvI.: Deux cas d'epithe!iome du testicle traite par la castration et l'ablation des ganglions lombo-aortiques. Bull. e. mem. Soc. de Chir., Paris, 36: 236, 1910. 6. Hinman, F.: The operative treatment of tumors of the testicle. Vvith the report of thirty cases treated by orchidectomy. J.A.M.A., 63: 2009, 1914. 7. Lewis, E. L., Johnston, R. E., Rowe, R. B. and Kimbrough, J. C.: Retroperitoneal lymph node resection: intercosto-inguinal approach. J. Urol., 67: 338, 1952. 8. Cooper, J. F., Leadbetter, W. F. and Chute, R.: Thoracoabdominal approach for retroperitoneal gland dissection: its application to testis tumors. Surg., Gynec. & Obst., 90: 486, 1950. 9. Mallis, N. and Patton, J. F.: Transperitoneal bilateral lymphadenectomy in testis tumor. J. Urol., 80: 501, 1958. 10. Jamieson, J. K. and Dobson, J. F.: The lymphatics of the testicle. Lancet, 1: 493, 1910. 11. Busch, F. M. and Sayegh, E. S.: Roentgenographic visualization of human testicular lymphatics: a preliminary report. J. Urol., 89: 106, 1963. 12. Busch, F. M., Sayegh, E. S. and Chenault, 0. W., Jr.: Some uses of lymphangiography in the management of testicular tumors. J.

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Urol., 93: 490, 1965. 13. Chiappa, S., Uslenghi, C., Bonnadonna, G., Marano, P. and Ravasi, G.: Combined testicular and foot lymphangiography in testicular carcinomas. Surg., Gynec. & Obst., 123: 10, 1966. 14. Chiappa, S., Uslenghi, C., Galli, G., Ravasi, G. and Bonadonna, G.: Lymphangiography and endolymphatic radiotherapy in testicular tumors. Brit. J. Rad., 39: 498, 1966. 15. Tavel, F. R., Osius, T. G., Parker, J. W., Goodfriend, R. B., McGonigle, D. J., Jassie, M. P., Simmons, E. L., Tobenkin, M. I. and Schulte, J. W.: Retroperitoneal lymph node dissection. J. Urol., 89: 241, 1963. 16. Wahlqvist, L., Hulten, L. and Rosencrantz, M.: Normal lymphatic drainage of the testis studied by funicular lymphography. Acta Chir. Scand., 132: 454, 1966. 17. Skinner, D. G.: Non-seminomatous testis tumors: a plan of management based on 96 patients to improve survival in all stages by combined therapeutic modalities. J. Urol., 115: 65, 1976. 18. VanBuskirk, K. E. and Young, J. G.: The evolution of the bilateral antegrade retroperitoneal lymph node dissection in the treatment of testicular tumors. Mil. Med., 133: 575, 1968. 19. Donohue, J. P.: Retroperitoneal lymphadenectomy: the anterior approach including bilateral suprarenal-hilar dissection. Urol. Clin. N. Amer., 4: 509, 1977. 20. Donohue, J. P., Roth, L. M., Zachary, J. M., Rowland, R. G., Einhorn, L. H. and Williams, S. D.: Cytoreductive surgery for metastatic testis cancer: tissue analysis ofretroperitoneal masses after chemotherapy. J. Urol., 127: llll, 1982. 21. Ray, B., Hadju, S. I. and Whitmore, W. F., Jr.: Proceedings: distribution of retroperitoneal lymph node metastases in testicular germinal tumors. Cancer, 33: 340, 1974. 22. Donohue, J. P., Einhorn, L. H. and Williams, S. D.: Cytoreductive surgery for metastatic testis cancer: considerations of timing and extent. J. Urol., 123: 876, 1980. 23. Donohue, J. P., Einhorn, L. H. and Williams, S. D.: Is adjuvant chemotherapy following retroperitoneal lymph node dissection

for nonserninomatous testis cancer necessary? Urol. Clin. N. Amer., 7: 747, 1980. 24. Rowland, R. G., Weisman, D., Williams, S. D., Einhorn, L. H., Klatte, E. C. and Donohue, J. P.: Accuracy of preoperative staging in stages A and B nonseminomatous germ cell testis tumors. J. Urol., 127: 718, 1982. 25. Scardino, P. T.: Adjuvant chemotherapy is of value following retroperitoneal lymph node dissection for nonseminomatous testicular tumors. Urol. Clin. N. Amer., 7: 735, 1980. EDITORIAL COMMENT This objective and detailed analysis of a large and unique experience with retroperitoneal lymph node dissection for germ cell tumors provides novel and definitive information on lymph node distribution in this disease, which may be amplified in the future but which is not likely ever to be superseded. Ambiguities in definitions of lymph node distribution have been addressed, the absence of contralateral lymph node metastases in the face of negative ipsilateral nodes has been confirmed, the higher incidence of hilar and suprahilar adenopathy with tumors on the left rather than the right side has been demonstrated and explained, the incidence of hilar and suprahilar node metastasis in association with the different stages of retroperitoneal disease has been defined, the frequency of inter aortocaval node involvement with tumors on the right and left sides has been shown, and the not uncommon involvement of the retroperitoneal spermatic cord by tumor has been indicated. Finally, an analysis of the relationship of the pathologic findings in the testis tumor to those in the retroperitoneal metastases further documents the potentials for differentiation of embryonal carcinoma. Willet F. Whitmore, Jr. Urologic Service Memorial Sloan-Kettering Cancer Center New York, New York