Br. J. Surg. Vol. 62 (1975) 226-230

Is ‘second look surgery’ justified in suspected recurrences of cancer of the H A R O L D ELLIS A N D G . JAYASEKARA*

SUMMARY A series of 23 patients with suspected recurrent disease following ‘curative’ resection .for gastric carcinoma was submitted to further laparoromy (24 operations). Three patients were found to have hopeless dissemination, 10 had palliative procedures performed which relieved their dysphagia, vomiting and jaundice, 4 had recur- rences resected and I had a secondprimary of the gastric stump excised, No less than 6 were found to have benign lesions.

Although the reward as far as prolonged survival is smnll, we believe that the relief of symptoms and the occasional long term excellent result justifies judicious use of a ‘second look’ laparotomy for suspected recurrent disease.

THE development of clinical features which suggest the recurrence of disease following what was believed to be a curative cancer resection is a depressing state of affairs which until recently was regarded by most sur- geons as an entirely hopeless situation. However, in the past few years it has become increasingly recog- nized that some cancers have a tendency to local re- currence which may be controlled by further radical surgery, or that the apparent recurrence is in fact the development of a second primary metachronous tumour, which itself may be entirely operable. In some instances the clinical features may indeed be produced by altogether benign and curable situations, for example, a granulomatous stricture at an anasto- mosis. It is particularly in cancers of the colon and rectum that such favourable situations are likely to be found, and this we have recently reviewed (Ellis, 1974). However, most surgeons regard recurrent disease following resection of a gastric or oesophageal cancer as carrying a particularly poor prognosis.

This paper presents the results of a policy, carried out over the past 10 years, of re-exploring the abdo- men for suspected recurrent cancer following ‘curative’ resections of gastric and oesophageal tumours in patients in whom the clinical features do not suggest that widespread hopeless dissemination of the disease had taken place. During this time 23 patients have been subjected to further laparotomy (24 operations). Of these, 20 had had their primary operation carrried out in the Surgical Unit, Westminster Hospital, and the remaining 3 were referred from other hospitals.

In carrying out this second exploration we had the following four possibilities in mind:

1. Could the clinical features be due to some altogether benign and remediable lesion?

2. If not, might a metachronous, resectable cancer have developed ?

stomach ?

3. If indeed the tumour had recurred, could this itself be resected 1

4. If the recurrence was unresectable, would a palliative short circuit or intubation to relieve obstruc- tion be worth while?

Findings at operation The findings in our 24 operations are shown in Table I .

Table I : FINDINGS AT ‘SECOND LOOK’ SURGERY Finding: Benign lesion

1 No. of cases: 6*

A second primary in the

Recurrence in the gastric 3

Resection of ovarian secondary I Palliative procedure l o t Laparotomy only 3

stomach

stump resected

* One patient was subsequently re-explored for recurrence. f One patient had undergone a previous laparotomy for a benign lesion.

Benign lesions mimicking recurrent disease (6 patients) Two patients developed a benign stricture which radio- logically mimicked recurrent cancer; both underwent re-resection. The first patient remains well 2 years following resection of his post-oesophagectomy stric- ture; the second died of disseminated cancer only 8 months after resection of his benign stricture following a total gastrectomy.

Two patients were re-explored for vomiting and pain which developed after partial gastrectomy. The first was found to have a benign stoma1 ulcer and was submitted to vagotomy; she remains well 4 years later. The second patient had a Roux conversion which relieved his symptoms but he developed disseminated recurrences and died 1 year following his second operation.

One patient presented with a mass in his abdominal scar, vomiting and loss of weight 5 months after total gastrectomy. The second laparotomy revealed that the mass was a sterile chronic abscess in the abdominal wall and his abdominal symptoms were produced by obstructing postoperative adhesions affecting the upper jejunum. These were divided and he remained well for 4 years. He then developed an anastomotic recurrence with dysphagia. This was treated by a Souttar’s tube intubation and he died I month following this.

One patient from Cyprus presented with vomiting and dysphagia 4 months after an upper partial gastrec- tomy for a carcinoma of the cardia performed at

* Surgical Unit, Westminster Hospital, London.

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another hospital. At laparotomy there was no evidence of recurrent disease. A pyloroplasty was per- formed and her symptoms disappeared. The patient returned to Cyprus and has been lost from our follow- UP.

In this group 3 patients achieved reasonably long term satisfactory results, 2 of whom are still living, 2 patients developed recurrences quite rapidly and 1 has been lost to follow-up.

A second primary in the stomach There was 1 example in this series of an undoubted metachronous primary in the stomach. This was a female patient who in 1943, at the age of 43, had a partial gastrectomy for a spheroidal cell carcinoma of the stomach. She returned in 1967 at the age of 67 with a tumour mass in the gastric stump and an abdominal total gastrectomy was performed. Histo- logical examination revealed a highly anaplastic carci- noma which did not resemble the appearance of the original tumour. The lymph nodes were extensively involved. Local recurrences rapidly developed and she died 6 months after her second operation.

Resection o j recurrences (4 patients) Three patients developed local recurrences which were resectable; 1 after partial gastrectomy and 2 after total gastrectomy. The partial gastrectomy was converted to total gastrectomy but recurrences developed and the patient died I 1 months later. One of the patients who had undergone total gastrectomy died only 4 months after resection of the anastomotic recurrence. The other patient remained well for 20 months fallowing this procedure; he then developed a further local recurrence which was treated by radiotherapy and he has remained clinically free from disease for 3 years.

The fourth patient developed an ovarian metastasis I year after her partial gastrectomy. This was resected but she died 14 months later with widespread meta- stases.

Only 1 of the 4 patients in this group has had reasonable long term benefit from surgery although 2 others were relieved of their dysphagia.

Palliative operations (10 patients) Four patients with dysphagia due to local recurrences following partial or total gastrectomy had the obstruc- tion intubated by means of a Porge’s or Souttar’s tube. Although dysphagia was relieved, these patients died 3 weeks, 3 weeks, 6 weeks and 2 months respec- tively following the procedure.

In 3 patients a gastro-enterostomy was performed to the gastric stump; obstructive symptoms were relieved but the patients died 3, 5 and 8 months re- spectively following surgery.

Three patients developed obstructive jaundice due to tumour masses in the porta hepatitis and it was possible to short-circuit the distended gallbladder to the jejunum. Jaundice was relieved but the patients died 6 weeks, 2 months and 7 months respectively after this second operation.

Laparotomy only (3 patients) In 3 patients laparotomy was performed with the dis- covery of widespread intra-abdominal dissemination. One patient died 4 days postoperatively. The others were treated with 5-fluorouracil but died 7 weeks and 7 months respectively following laparotomy.

Discussion Results of previous re-exploration programme5 An important stimulus to surgical thinking on the problem of recurrent abdominal cancer was the in- teresting and controversial work of Wangensteen, who introduced his ‘second look’ programme in 1948 (Wangensteen, 1949). In this experiment, patients who had undergone what was considered to have been curative resection of the stomach or large bowel, and in whom the regional lymph nodes were found to be involved on histological examination, were re- explored approximately 6 months later. At this ‘second look’ any recurrence of cancer, if found, was resected if this was technically possible. Subsequently, similar operations were performed on the patients in whom further tumour had been found and resected, and these were repeated at intervals of 6 months to 1 year until either no further tumour was discovered or the situation was obviously out of control. Once the patient had had an exploration which revealed no residual cancer, further laparotomy was not performed but careful follow-up was continued. Within a few years it was obvious that although results of re- exploration in colonic cancer were encouraging, rectal cancer recurrences tended to be diffuse and reoperation in gastric cancer was difficult and far less rewarding (Wangensteen et al., 1954).

An extensive survey of the results of this programme up to July 1967 was published by Griffen et al. in 1969. In the group of patients with carcinoma of the stomach 64 were submitted to re-exploration. Twenty- eight of these had a negative ‘second look’, of whom 10 subsequently developed recurrent cancer, 7 died of other causes and 11 remained alive and well. Of 37 patients with positive ‘second look’ operations, there were 3 operative deaths, 1 patient died of causes other than cancer and 31 developed further recurrent disease. Only 2 patients were alive and well and could therefore be considered to have been ‘converted’ to this state by the additional resection. In this study a further 37 patients were reported who presented with symptomatic recurrent disease and were re-explored ; none of these was converted to a cancer-free situation. These figures therefore gave no support to a con- tinued programme of elective re-explorations in gastric cancer.

In the past 20 years there have been other important studies of series of recurrent gastric carcinomas sub- jected to further laparotomy with re-resection, where this was possible. In addition to these reviews there has been a considerable number of individual case reports. These papers, on the whole, paint a gloomy picture of the prognosis following a further resection, but there are occasional brilliant results with survival of 5 or more years following the second operation.

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Bowden et al. (1954) described 37 patients ~ h o were re-explored for recurrent gastric carcinoma; in 15 a further resection was carried out. There were 2 post- operative deaths. Of the 13 recovering from surgery, 8 patients survived an average of 8 months, 2 were alive with metastases, 2 were alive and clinically clear of disease at 15 and 18 months and 1 patient was alive and well 5 years and 10 months following the second operation. Of the 22 patients in which further resection was impossible, 4 underwent palliative procedures. The average survival in these 22 patients was 6 months with a range of 1-20 months. Welch and Wilkins (1958) carried out 7 ‘second look‘ gastric cancer operations; in 4 it was possible to carry out further resection, and although 2 of the patients died postoperatively, the other 2 lived for 5 years after the second operation. It is interesting that neither of these had positive lymph nodes at either laparotomy. Funderburk (1962) collected reports on 53 patients undergoing reoperation for cancer of the stomach, including 2 of his own cases. Resection was possible in 24 of these patients, with survival of 4-70 months; 6 lived for more than 18 months. One of his own patients had a partial gastrec- tomy in 1946 which was converted in 1957 to total gastrectomy for recurrence. In 1961 she had a third operation in which a malignant node in the jejunal mesentery was resected and she was alive at the time of reporting. Ferguson and Nusbaum (1963) re- viewed 94 patients undergoing primary surgery for cancer of the stomach; 93 were explored and 48 underwent radical gastrectomy. Two of these were subsequently re-explored for recurrent disease; one recurrence was resected 7 years later and the patient was well 4 years after the second operation; another patient developed a metastatic lesion in the colon which was resected 8 years after the initial surgery, but the patient died 3 years later of recurrent disease. Lippert (1968) reported 5 cases of reoperation for gastric cancer; 3 underwent radical re-resection; 1 of these died 3 years after the second operation, but the other 2 were alive at 4 and 7 years. The fourth patient underwent a decompression operation for common bile duct obstruction and died 30 months later. The fifth patient underwent a total of 4 ‘second look‘ pro- cedures over the course of 21, years-resection of small bowel, removal of deposits first in the left and then in the right ovary and ftnally an ileotransverse colon bypass operation. The patient died 2 months after the short-circuit procedure.

Iwasa et al. (1972) have recently reported an exten- sive study of operations for recurrent gastric cancer in Tokyo, with overall discouraging findings; 109 patients were seen between 1956 and 1971 with re- current tumours. Of these, 58 were submitted to a second laparotomy. Four only were suitable for further resection and only 1 of these survived for 2 years. Fifteen patients were submitted to laparotomy only, and the rest had various palliative procedures, including bypass or feeding jejunostomy. Most of these were dead within 1 year.

An extraordinary case was reported by Aviles (1973); this woman underwent a right hemicolectomy

for carcinoma in 1942, a resection of a second tumour in the sigmoid colon in 1946, a partial gastrectomy for a carcinoma of the stomach in 1960 (at which time the lymph nodes were clear) and in 1967 a total gastrectomy for recurrence in the stump. The patient recovered from this procedure but no further inform- ation was given about her subsequent progress.

Tumour implantation It is well known that tumour cells may seed into the wound at the time of operation (Ryall, 1907). Such deposits may occur not only after surgical exploration but even at the site of paracentesis for malignant ascites (Bush, 1957). Such implantation may be wide- spread throughout the abdominal wound and peri- toneal cavity, but occasionally isolated deposits may develop which are suitable for excisional surgery. Ackerman and Wheat (1955) described a patient who was well 4 years after a resection of a tumour mass in the abdominal scar which developed 1 year following resection of a gastric carcinoma. Sonneland (1959) resected a scar deposit 2 years after gastrectomy for a carcinoma of the stomach. The patient was alive I year later but had liver deposits. Fortner and Lawrence (1 960) reviewed the extensive experience at the Memorial Hospital for Cancer, New York. ‘Curative’ gastric resections were carried out on 569 patients between 1931 and 1957. Eleven of these subsequently developed a lump in the laparotomy scar and it is interesting that 2 of these were benign, one being a desmoid, the other an inflammatory mass. Of the 9 secondary deposits, 3 were excised, 2 had radiotherapy and 4 had no local treatment. All these patients died with carcinomatosis 3-28 months after the recurrence.

In 1958, in a survey of 31 patients having laparo- tomies for suspected recurrent cancers, we reported a patient who had recurrences removed from the abdominal scar 7 and 17 months following resection for gastric carcinoma, Four months after the second recurrence had been removed she developed deposits in both axillae which were excised; she died some months following this from carcinomatosis (Cronin and Ellis, 1958).

A striking long term survival was reported by lnouye and Erb (1965); this was a patient who under- went a partial gastrectomy in 1945, developed a deposit in his abdominal incision 3 months later and then survived after its excision for 17 years until 1963, when he developed a recurrence in his gastric stump and died following further resection.

Metachronous cancer in the gastric stump A second carcinoma developing in the same organ is a well-recognized phenomenon, particularly in squa- mous and basal tumours of the skin, in carcinomas of the large bowel and, in a slightly different context, in the opposite breast following mastectomy. A second primary cancer may also undoubtedly develop in the gastric stump following partial gastrectomy for malig- nant disease. In this situation the development of a second primary tumour must be differentiated from recurrence of the original disease, and can be made

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on the grounds either that the two tumours are quite distinct in histological appearance or that the interval between the appearance of the two tumours is suffi- ciently long to make recurrence of the original cancer unlikely. Morgenstern (1960), in presenting 2 such patients, was able to review 1 I previously reported cases. Five of these had no follow-up, 5 died at intervals of up to 14 months following operation and 1 patient lived for 7 years after the second resection (Stoloff and Lattimore, 1955).

In a later paper Morgenstern et al. (1973) were able to add 2 more patients to Morgenstern’s original experience. They considered that a gap of no less than 20 years should elapse between the two tumours in differentiation between recurrence and a second primary cancer, although other authors accept a gap of 10 years. Of the 4 patients reported, 1 initially had a partial gastrectomy for a reticulum cell sarcoma and died 4 years after resection of an adenocarcinoma arising in the stump 25 years after the initial operation. The other 3 patients, all of whom had an initial carci- noma of the stomach and who subsequently developed a second tumour 22,25 and 30 years later respectively, underwent further resection. There was 1 postoperative death, I patient died 2 years after the second operation and 1 patient was still alive and well 5 years later.

Obviously, the development of a second cancer of the stomach following partial gastrectomy is an unusual occurrence, probably related, a t least in part, to the fact that prolonged survival following gastrec- tomy is unfortunately an infrequent phenomenon. In the patient we reported the interval between the two operations was 24 years and the histological appear- ance of the two tumours was entirely dissimilar so that undoubtedly this represented a metachronous primary cancer. Unfortunately rapid recurrence and death followed the second resection.

Conclusion Carcinoma of the stomach remains one of the most dangerous of the major cancers and is the third com- monest cause of death from malignant disease in the United Kingdom. In patients undergoing what is thought to be curative resection, large numbers pre- sent with obvious clinical recurrent disease within 5 years.

There is a general feeling among surgeons that when recurrence or metastases are diagnosed following gastric resection the situation is a hopeless surgical proposition. A review of previous publications and of our own experience confirms that the outlook is indeed gloomy, but by n o means hopeless. In the 23 patients we have operated upon over the past 10 years (24 operations) 3 had a laparotomy only, confirming a hopeless situation. Ten had palliative procedures for obstructive jaundice, gastric outlet obstruction or dysphagia, and all of these died within a few months, although useful palliation had been achieved from these unpleasant symptoms. Four patients with recurrent or metastatic disease were suitable for resection, but only 1 achieved 3 years of relief of his dysphagia, and this period included a

course of radiotherapy for further recurrent disease. One patient with an undoubted metachronous lesion in the gastric stump died 6 months after further re- section. However, it must be noted that from time to time encouraging long term survivals have been re- ported following re-resection of recurrent, metastatic and metachronous cancers after gastric resection.

Perhaps the brightest ray of encouragement is our finding that n o less than 6 of our patients who were considered clinically to have developed recurrent disease were found to have benign lesions at laparo- tomy. One has been lost t o follow-up, 2 are well 2 and 4 years after surgery respectively, but the remaining 3 developed frank recurrent disease and died 8 months, 1 year and 4 years respectively following the finding of a benign lesion at their ‘second look’ procedure (the last patient having intubation performed for his recurrent tumour).

In spite of this small reward we conclude that a laparotomy is still justifiable in a patient who develops clinical evidence of apparent recurrent disease follow- ing ‘curative’ resection for gastric cancer. Rarely an altogether benign lesion can be found and cured, and perhaps this alone is worth all the endeavour. Occasionally a recurrent or metachronous lesion can be resected with long term cure, although this was not our own experience in this small series. There is no doubt that in many cases unpleasant symptoms (dys- phagia, gastric outlet obstruction and jaundice) can be relieved up to the time of the patient’s death, even though this may be measured only in months or even weeks,

However, even if nothing at all can be done at the time of surgery, a t least the diagnosis can be con- firmed without any doubt, a decision made as to whether or not cytotoxic drugs should be employed and, perhaps most important of all, the patient’s family and the patient himself can realize that no stone has been left unturned before the final hopeless prognosis has been given.

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