Surgical Management of Renal Tumors: A Historical Perspective

The modern era of renal surgery began on August 2, 1869 when the first planned nephrectomy on a living human being was performed. Eighteen years later in 1887, the first partial nephrectomy to remove a renal tumor was performed. Both total and partial nephrectomy have become the hallmark surgical procedures used today to treat renal tumors, and their conception and evolution represent two of the most important advances in medicine and surgery. Surgery for kidney cancer continues to evolve. This article traces the history of surgical management for renal tumors.

Foundations

The modern era of renal surgery began on August 2, 1869, just 139 years ago, when Gustav Simon (1824–1876), then Professor of Surgery at Heidelberg, performed the first planned nephrectomy on a living human being. His patient was a 46-year-old woman named Margaretha Kleb, who suffered from a pervious urinary fistula caused by an injury to the ureter sustained during a prior laparotomy to remove an ovarian cyst. She survived removal of her kidney and was permanently cured of her fistula. Eighteen years later in 1887, Vincenz Czerny (1842–1915), Simon’s successor at Heidelberg, performed the first partial nephrectomy to remove a renal tumor. Both total and partial nephrectomy have become the hallmark surgical procedures used today to treat renal tumors, and their conception and evolution represent two of the most important advances in medicine and surgery.

Simon ( Fig. 1 ) arrived at his decision to remove a healthy, functioning kidney, plagued with many questions for which he had no sure answers. Would the remaining kidney supply the needs of the body? Could the ligated renal artery withstand the blood pressure of the aorta following absorption of the ligature? Could the initial hemorrhage be controlled? Could wounds and infection of the peritoneum be avoided? Still, there was historical precedent for the operation.

For many years, physiologists had established the fact that animals could survive after removal of one kidney. In 1670, Zambecarri, along with Rounhuysen, extirpated sound kidneys without causing death; he was also the first to contemplate the operation of nephrectomy in man. Between 1690 and 1841, Blancard, Blundell, Claude Bernard and others repeated similar experiments, concluding that any adverse effects following nephrectomy were more a result of the operation itself than to the absence of one kidney. During the nineteenth century, abdominal surgery flourished, particularly to remove large ovarian cysts or tumors. In a few cases this had resulted in unintentional nephrectomies, as in those by Wolcott (1861), Spiegelberg (1867), and Peaslee (1868). Although the patients died eventually from infections, in each case the remaining kidney worked well. Many autopsies also showed that for an indefinite time before death, only one kidney had been functioning.

The animal experiments and surgical misadventures of the ovariotomists impressed Simon, but he was still not ready to remove a healthy kidney without witnessing the consequences himself. He nephrectomized 30 dogs and observed they lived in perfect health after ablation of one kidney. He noted compensatory hypertrophy and convinced himself that the physiologic function of the kidneys could be maintained by one kidney. He dissected cadavers to work out the anatomic details, steps of the operation, and the best access to the retroperitoneum. Only then was he ready to proceed with his landmark nephrectomy. In 1869, before a live audience, he removed Kleb’s left kidney through a lumbar incision. Simon completed the operation in 40 minutes and lost just 50 mL of blood. Renal surgery was born.

Early renal surgery

Simon had no imitators for nearly a year. In April 1870, Parker removed a kidney from a 12-year-old girl, for hydronephrosis, but the patient died from shock the following day. In December 1870, Gilmore, an American surgeon, removed a painful floating kidney in a woman, aged 39 years, who recovered without mishap. In 1875, Langenbuch performed the first nephrectomy for a malignant tumor, followed by Jessop in 1877, who removed a Wilms tumor. Both patients survived the operation. The first decade after Simon (1870–1879) saw 28 nephrectomies, but the mortality rate was a frightful 64%. With the wide acceptance of antisepsis in 1876, and later adopting Lister’s methods of asepsis in 1880, the next 5 years (from 1880 to 1884) saw the mortality rate fall to 24% after 219 nephrectomies. Most surgeons used the lumbar approach, believing that it was safer; however, in 1876 Kocher was forced to use the transperitoneal route to remove a bulky tumor and concluded that it afforded a fairly easy approach to the kidney. Some surgeons adopted this approach because they could ascertain the condition of the opposite kidney by palpation. However, the invention of the cystoscope by Nitze in 1877, and the practical applications of ureteral catheterization, soon gave adequate information on the opposite kidney; transperitoneal operations fell into disfavor, except for removal of large tumors.

Every decade up the dawn of the twentieth century, survival rates after nephrectomy improved. In 1901, von Schmieden reported on 1,118 nephrectomies, collecting the operations of the first three decades following the first deliberate nephrectomy by Simon. He showed that nephrectomy by the lumbar route was followed by a mortality of 44% in the first, by 27% in the second, and by 17% in the third decade. The abdominal method had a mortality of 55% in the first, 48% in the second, and 19% in the last decade. In 1902, Kuster collected the statistics of 1,521 nephrectomies performed by different surgeons around the world, giving mortality for all cases of 34% for the transperitoneal and 12% for the extraperitoneal removal of kidneys. By 1900 though, techniques of abdominal surgery had improved markedly so that both approaches were comparable. During the early twentieth century, mortality reported by specialists or skilled urologists was markedly less than nephrectomy done by general surgeons. In 1912, Gerster in New York reported mortality in 21% of 112 nephrectomies done by general surgeons in the last 16 years. During the same time, renal cases segregated, studied, and operated upon by urologists under the direction of Edwin Beer had a mortality rate of only 3.8% among 207 nephrectomies.

The usual indications for nephrectomy were stones, movable kidney, hydronephrosis, renal abscess, urinary fistulae, and tumors. Many of these diseases affected only a part of the kidney, and partial or heminephrectomy developed rapidly owing to the successes of total nephrectomy. In November 1887, Czerny ( Fig. 2 ) performed the first deliberate partial resection when he removed an angiosarcoma from the kidney of a 30-year-old gardener. The patient recovered. Fears of uncontrollable hemorrhage were dispelled by the work of Tuffier , who in 1889 showed that gentle pressure could control bleeding from the kidney, and animal experiments by Thiriar in 1888 and Bardenheuer in 1891 proved that incisions made into the kidney often healed primarily without fistula formation. They investigated renal repair mechanisms, compensatory hypertrophy, renal function, changes in body functions, and the amount of renal tissue necessary for life after partial resection.

Surgeons then began to perform partial nephrectomy in various types of cases, but the operation soon lost favor and it was more or less abandoned because of an unwarranted fear of extensive hemorrhage at operation, delayed bleeding following surgery, frequent and persistent urinary fistula, and poor results owing to the injudicious use of partial resection to treat tuberculosis and neoplasms of the kidney. Kummell (1890), Bardenheuer (1891), and Block (1895) attempted partial nephrectomy for tumors but their patients died of atrophy of the kidney, shock, and uremia. During this early period, lumbar nephrectomy became established as the only effective operation for malignant diseases of the kidney.

In spite of better surgical methods, nephrectomy for kidney tumors was followed by a high mortality, varying from 50% (Squier, 1909) to 11% (Braasch, 1913). As late as 1920, Hyman reported a mortality of 23% to 37%. The reasons for the unusually high mortality in nephrectomy for tumor were attributed to shock resulting from toxins released during the manipulation necessary to remove large tumors, and hemorrhage. Another frequent cause was fatal tumor emboli, owing to dislodged cancer cells entering the circulation during surgery. Block noted an extension of cancer cells into the renal vein in 13 of 86 cases studied. Enthusiasm for conservative surgery for renal tumors was especially discouraged by autopsy and nephrectomy specimens showing frequent tumor spread into fat around the kidney and involvement of renal veins, as well as that almost all patients during this time had palpable and symptomatic renal cancers.

In 1903, Gregoire reported removing kidney tumors en bloc with the fatty capsule, adrenal gland, and adjacent lymph nodes. This was the first description of the modern radical (perifascial) nephrectomy popularized later in the twentieth century. Its advantages were articulated by Chute , who in 1926 advocated anterior abdominal removal of kidney cancers because the pedicle is more easily reached and can be ligated immediately, minimizing the danger of forcing metastases into the renal veins, causing less trauma and affording palpation of the retroperitoneal glands. In large tumors, control of the renal pedicle posed problems. In 1902, Pasteau recommended ligating the renal artery and vein separately, whereas Legueu (1921) and others advised tying off the pedicle en masse. Early surgeons emphasized that dividing the upper ureter facilitated greater mobility of the kidney and easier ligation of the pedicle, and they did not hesitate to resect a rib to secure better exposure. Most surgeons continued to perform a lumbar or flank nephrectomy, however; and although they believed that total nephrectomy was the only effective treatment of malignant kidney tumors, despite such aggressive surgery for the times, 33% of patients died of disease within 1 year and 65% died in less than 5 years.

In 1921, Rosenstein performed a partial nephrectomy to palliate a kidney cancer and urged that this operation should be done in similar cases in which the contralateral kidney was incapable of satisfactory function following nephrectomy. In 1937 Goldstein and Abeshouse collected 296 cases of partial resection (1901–1935), of which 34 (11%) were done for renal tumors. They noted one death among 21 malignant tumors and no deaths for 13 benign tumors, and there were no cases of secondary hemorrhage or urinary fistula. They concluded that “small tumors and tumors of moderate size situated at one of the poles of the kidney, may be removed by partial resection out of necessity, but was contraindicated if the opposite kidney was healthy.” From 1937 to 1950 another 25 cases were added with similar results, although suspected renal tumors were primarily treated by total nephrectomy and only a few patients with poor renal function underwent local excision. Most surgeons regarded partial nephrectomy as technically more demanding than nephrectomy, associated with a higher complication rate, and simply unnecessary in most patients.

In 1950, Vermooten laid the foundation for modern nephron sparing surgery for renal neoplasms. “There are certain instances, when, for the patient’s well being, it is unwise to do a nephrectomy, even in the presence of a malignant growth involving the kidney. The question is, whether such a procedure is ever justifiable when the opposite kidney is normal. I am inclined to think that in certain circumstances it may be.” In 1948 he removed a 10-cm carcinoma from the left kidney of a 52-year-old woman with a normal right kidney. His decision was based on the pathologic studies by Cahill (1948), showing that clear cell carcinomas arose from the cortex, were localized, surrounded by a capsule, grew by expansile growth, rarely invaded surrounding structures, and generally spread by the bloodstream. He was also aware that the autopsy studies by Bell and others (1938–1944) had revealed few metastases from small renal tumors. Bell reported that only 7% of tumors less than 5 cm had metastasized, compared with 83% of tumors larger than 10 cm. In fact, small tumors rarely broke through the capsule and only one isolated metastasis was noted among 38 tumors 3 cm or smaller in size. Microscopic studies of tissue adjacent to tumors persuaded Vermooten that some tumors could be excised with only a 1-cm margin without fear of local recurrence, and local tumor excision should be attempted, especially in a solitary kidney or when there was markedly impaired function of the opposite kidney.

Few urologists paid much attention to Vermooten or to the observations of Bell except to argue that, because small tumors might metastasize, that warranted total nephrectomy for all renal tumors, especially in cases with two kidneys. During the next 40 years, partial nephrectomy was done mostly for tumors in a solitary kidney, poor renal function, or bilateral renal tumors. From 1950 to 1967, Zinman and Dowd collected only 18 essential cases of partial nephrectomy, adding 3 of their own. At the same time, other progressive surgeons reported individual cases of partial nephrectomy for unilateral renal tumors when the other kidney was considered satisfactory. Still, most urologists believed that partial nephrectomy was unwarranted unless there was a compelling reason to preserve renal function. Textbooks published between 1937 and 1970 do not mention partial nephrectomy.

Early renal surgery

Simon had no imitators for nearly a year. In April 1870, Parker removed a kidney from a 12-year-old girl, for hydronephrosis, but the patient died from shock the following day. In December 1870, Gilmore, an American surgeon, removed a painful floating kidney in a woman, aged 39 years, who recovered without mishap. In 1875, Langenbuch performed the first nephrectomy for a malignant tumor, followed by Jessop in 1877, who removed a Wilms tumor. Both patients survived the operation. The first decade after Simon (1870–1879) saw 28 nephrectomies, but the mortality rate was a frightful 64%. With the wide acceptance of antisepsis in 1876, and later adopting Lister’s methods of asepsis in 1880, the next 5 years (from 1880 to 1884) saw the mortality rate fall to 24% after 219 nephrectomies. Most surgeons used the lumbar approach, believing that it was safer; however, in 1876 Kocher was forced to use the transperitoneal route to remove a bulky tumor and concluded that it afforded a fairly easy approach to the kidney. Some surgeons adopted this approach because they could ascertain the condition of the opposite kidney by palpation. However, the invention of the cystoscope by Nitze in 1877, and the practical applications of ureteral catheterization, soon gave adequate information on the opposite kidney; transperitoneal operations fell into disfavor, except for removal of large tumors.

Every decade up the dawn of the twentieth century, survival rates after nephrectomy improved. In 1901, von Schmieden reported on 1,118 nephrectomies, collecting the operations of the first three decades following the first deliberate nephrectomy by Simon. He showed that nephrectomy by the lumbar route was followed by a mortality of 44% in the first, by 27% in the second, and by 17% in the third decade. The abdominal method had a mortality of 55% in the first, 48% in the second, and 19% in the last decade. In 1902, Kuster collected the statistics of 1,521 nephrectomies performed by different surgeons around the world, giving mortality for all cases of 34% for the transperitoneal and 12% for the extraperitoneal removal of kidneys. By 1900 though, techniques of abdominal surgery had improved markedly so that both approaches were comparable. During the early twentieth century, mortality reported by specialists or skilled urologists was markedly less than nephrectomy done by general surgeons. In 1912, Gerster in New York reported mortality in 21% of 112 nephrectomies done by general surgeons in the last 16 years. During the same time, renal cases segregated, studied, and operated upon by urologists under the direction of Edwin Beer had a mortality rate of only 3.8% among 207 nephrectomies.

The usual indications for nephrectomy were stones, movable kidney, hydronephrosis, renal abscess, urinary fistulae, and tumors. Many of these diseases affected only a part of the kidney, and partial or heminephrectomy developed rapidly owing to the successes of total nephrectomy. In November 1887, Czerny ( Fig. 2 ) performed the first deliberate partial resection when he removed an angiosarcoma from the kidney of a 30-year-old gardener. The patient recovered. Fears of uncontrollable hemorrhage were dispelled by the work of Tuffier , who in 1889 showed that gentle pressure could control bleeding from the kidney, and animal experiments by Thiriar in 1888 and Bardenheuer in 1891 proved that incisions made into the kidney often healed primarily without fistula formation. They investigated renal repair mechanisms, compensatory hypertrophy, renal function, changes in body functions, and the amount of renal tissue necessary for life after partial resection.