INTRODUCTION

At present, surgery is an unparalleled choice of therapy for gastric carcinoma (1). In the 1960s, operative mortality rate resulting from gastric surgery was over 15%, but recent progress in both surgical and anaesthesiological techniques has noticeably reduced that percentage. In a recent review of the literature, the average mortality rate registered in the papers published up to 1990 was 7.8%, although very low values are reported in the Japanese series compared to those obtained in Western countries (2). Many studies have been carried out in order to identify risk factors that increase morbidity and mortality rates in gastric surgery. Advanced age has always been considered one of the highest risk factors (3-5).

Increased mean age among the populations of industrialized nations in the past few years is a significant finding, due to medical progress as well as improved social conditions. The group of subjects aged 80 years and over has been mostly affected by the rise in mean age. In 1970, individuals aged 80 and over made up 1.8% of the population in Italy. In 1990, this population rose to 2.9% and by 2020 it is likely to reach 5.6% (6). Recent studies have shown a considerable increase in patients with gastric cancer aged 80 and over (7). In this respect, surgeons are more frequently faced with the problem of choosing adequate therapy for aged patients.

The extended surgery (lymph node dissection and combined resection of adjacent organs) described by Japanese authors has been gradually introduced by some European groups (8,9). The routine use of these procedures in Japan resulted in high long-term survival and low morbidity and mortality rates (10). In Western countries two randomized prospective studies reported higher morbidity and mortality rates in regional lymph-node dissection (D2) compared with perigastric lymph-node dissection (D1). It has been speculated that these different results might be due to differences in mean age, physical characteristics and incidence of cardiopulmonary complications between Japanese and Western patients (11,12). As long-term results of randomized studies are still unknown, the problem of choosing limited or extended surgery is even more difficult in high risk patients such as the aged. In these patients, Japanese authors obtained low morbidity and mortality rates, analogous to those observed in younger patients, after employing less aggressive procedures (7,13-15). Screening programs have lead to a lower mean age in the Japanese series by 10 years, with respect to that of Western countries; as such, the number of gastric cancer patients aged 80 and over in Japan is relatively low if compared to the total observed cases (16). However, in Western countries this age group presently accounts for over 20% of cases (3,17), and recent operative mortality rates reported by Western authors are still quite high (18,19). The aim of the present study was to evaluate the incidence of postoperative morbidity and mortality in aged patients, and analyze risk factors for complications and their influence on long-term survival. The province of Siena has among the highest rates of incidence of gastric cancer in Europe, and includes a number of patients aged 80 years and over (20).

PATIENTS AND METHODS

Between January 1977 and December 1994, 1204 patients with gastric cancer were observed at the Second Department of Surgery, University of Siena. One hundred and ten patients aged 80 and over were selected for this study. Data regarding the clinicopathological and surgical aspects as well as those from follow-up were collected in a DBIV (Ashon-Tate) commercial data base installed on a PC. A preoperative evaluation of associated medical illnesses of each patient was always carried out. Patients with poor nutritional status underwent preoperative parenteral therapy. Preoperative staging was performed upon complete clinical-radiological examination. Factors that strongly determined whether or not to operate were an extremely advanced stage of disease, poor general conditions and patient consent. The surgical approachwas definedthrough a careful re-evaluation just after laparotomy, which allowed a complete staging of disease.

Clinicopathological evaluation as well as surgical procedure was carried out according to the criteria described by the Japanese Research Society for Gastric Cancer (JRSGC) (21). We performed subtotal gastrectomy for lesions located at the middle or lower third of the stomach, with a resection line located at least 3 cm away from the lesion. Tumors of the upper third of the stomach were treated by total gastrectomy. Reconstruction of the alimentary tract was carried out according to either the Billroth, Hoffman or Roux en Y technique. In cases of radical surgery, procedures included the removal of the greater omentum, the anterior leaf of the mesocolon and the pancreatic capsule with partial or total bursectomy. Extension of lymph node dissection and the removal of the spleen and pancreatic tail were decided upon during surgery. Lymphadenectomy was classified as: minimal, when the simple removal of perigastric lymph nodes was performed; standard, when node stations along the celiac axis (numbers 7, 8a and 9 of JRSGC classification) were removed; extended, including the total or partial removal of node stations 8p, 10, 11, 12, 13 and 14.

Oncological radicality was defined according to UICC standards (22).

Patients who underwent surgery received antibiotic prophylaxis. Following total gastrectomy, the patients received nutrition through a nasojejunal tube from the fourth postoperative day; a radiological check of the esophagojejunal anastomosis was carried out before resuming oral nutrition.

The postoperative events registered during hospitalization were used for calculating morbidity and mortality rates. Follow-up was carried out until December 31, 1996 and included six-monthly clinical and radiological examinations and tumor marker assays. Aged patients received quarterly check-ups for the first year following surgery. No patient was lost to follow-up. The median follow-up period of resected cases was 23 months (range 2-176).

For statistical analysis, we used the following: [chi]² test, to calculate the differences in morbidity and mortality rates, and the Biomedical Data Package (BMDP) Logistic Regression (LR) program for the elaboration of a multiple logistic regression model to evaluate independent risk factors for morbidity and mortality. For each variable, a significance level of P < 0.05 to enter the model was applied. The Hosmer's goodness of fit test was used to test the hypothesis that the model fits the data adequately (P > 0.05) (23). The Biomedical Data Package (BMDP) Life Table (1L) program was used for a univariate analysis of the survival rates according to the actuarial Kaplan-Meier model and the Mantel-Cox test for statistical significance. Patients who died during hospital stay were excluded from analysis.

RESULTS

The 110 cases we included in this study made up 9.1% of the total patients with gastric cancer we observed, with a considerable increase in recent years. Sixty of them were males and 50 were females (male:female ratio 1.2:1); the mean age was 83 years (range 80-92). Seventy-eight patients underwent surgery (operability 70.9%).

Table 1. Preexisting medical illnesses in 78 patients who underwent surgery

Illnesses	No. cases	%
Cardiovascular diseases	45	57.7
Respiratory diseases	16	20.5
Liver dysfunction (GOT or GDP [ge] 100 U/l)	2	2.6
Renal dysfunction (serum creatinine [ge] 1.5 mg/dl)	7	9.0
Anemia (Hb [le] 10.0 g/dl) and/or hypoproteinemia (total protein [le] 6.0 g/dl)	32	41.0
Diabetes	4	5.1
None of the above	11	14.1
Associated pathologies	33	42.3

Table 2. Surgical data of 52 cases treated by resective surgery

Surgical data	No. cases	%
Type of procedure
Subtotal gastrectomy	41	78.8
Total gastrectomy	11	21.2
Combined resection
None	47	90.4
Transverse colon	1	1.9
Transverse mesocolon	1	1.9
Left liver	1	1.9
Spleen	2	3.9
Oncological radicality of resective surgery
Curative (R0)	42	80.8
Non-curative (R1 or R2)	10	19.2
Lymphadenectomy
Minimal	20	38.4
Standard	29	55.8
Extended	3	5.8

Table 3. Histopathological characteristics of 52 resected cases

Characteristic	No. cases	%
Depth of invasion
T1	9	17.3
T2	17	32.7
T3-T4	26	50.0
Lymph nodal metastasis
N-positive	29	55.8
N-negative	23	44.2
Histological type
Tubular, well differentiated	6	11.5
Tubular, moderately differentiated	14	26.9
Poorly differentiated	15	28.9
Papillary	5	9.6
Signet ring cell	9	17.3
Mucinous	3	5.8
Site of tumor
Upper third	4	7.7
Middle third	8	15.4
Lower third	38	73.1
Gastric stump	2	3.8

Most operated patients were affected with other medical illnesses (Table 1). Among these, cardiovascular (57.7%) and pulmonary (20.5%) were the most frequent. Thirty-three patients (42.3%) had multiple associated illnesses.

Fifty-two patients underwent a resection, 10 underwent a bypass and in 16, surgery was restricted to simple laparotomy (resectability 47.3%). Table 2 reports the operative methods in 52 resected cases. Subtotal gastrectomy was the preferred procedure (78.8% of cases). In five cases (9.6%) we performed a combined resection of adjacent organs. Lymph node dissection was minimal in 38.4% of cases. Forty-two resections (32 subtotal gastrectomies and 10 total gastrectomies) were classified as curative (UICC R0).

Table 3 shows the histopathological features in the resected cases.

Postoperative complications according to the different surgical procedures are reported in Table 4. Twenty-five patients (32.1%) experienced postoperative complications. Cardiovascular complications were the most common. Two patients with a prolonged ileus required a further operation. One of these had an afferent loop syndrome and was surgically treated via conversion of anastomosis to Roux en Y; the patient died after 26 days due to anastomotic ulcer haemorrhage. In the other patient, adherences of the small intestine caused obstruction. Reoperation was necessary in a third patient to perform drainage of an abdominal abscess. Anastomotic leakage occurred in two patients who had undergone total gastrectomy (18.2%), whereas in one patient who underwent subtotal gastrectomy we observed a duodenal stump dehiscence. These three patients were completely healed through conservative treatment.

Average hospitalization period of all complicated cases was 19 ± 13 days versus an average period of 11 ± 3 days in cases which were uncomplicated. The total mortality rate was 12.8% (10 patients). Considering only resective procedures, morbidity and mortality rates were 26.9% and 3.8% respectively, with an average hospitalization period of 14 ± 9 days.

Table 4. Postoperative complications according to surgical procedure

Complication	Total no.	SG (41 cases)	TG (11 cases)	Bypass (10 cases)	Laparotomy (16 cases)
Morbidity
Cardiovascular	8	-	-	2	6
Haemorrhage	4	3	-	-	1
Ileus	4	3	-	1	-
Anastomotic leakage	3	1	2	-	-
Wound infection	3	1	2	-	-
Pulmonary	2	1	-	1	-
Abdominal abscess	1	1	-	-	-
Mortality
Cardiovascular	7	1	-	1	5
Haemorrhage	2	1	-	-	1
Septic shock	1	-	-	1	-

SG, subtotal gastrectomy; TG, total gastrectomy

Table 5. Morbidity and mortality rates according to different variables

Variable	No. cases	Morbidity (%)	P-value	Mortality (%)	P-value
Age
80-85	66	31.8	0.81	13.6	0.97
[ge]86	12	33.3		8.3
Sex
Male	41	39.0	0.25	19.5	0.12
Female	37	24.3		5.4
No. of preexisting medical illnesses
None	11	9.1	<0.01	0.0	<0.005
One	34	20.6		2.9
Two or more	33	51.5		27.3
Operative procedure
Subtotal gastrectomy	41	24.4	0.47	4.9	<0.005*
Total gastrectomy	11	36.4		0.0
Bypass	10	40.0		20.0
Laparotomy	16	43.7		37.5
Combined resection[dagger]
Yes	5	40.0	0.87	0.0	0.45
No	47	25.5		4.3
Extent of lymph node dissection[dagger]
Minimal	20	20.0	0.57	5.0	0.68
Standard-extended	32	31.3		3.1
Distant metastasis
Absent	62	30.6	0.82	6.5	<0.005
Present	16	37.5		37.5

^*Subtotal gastrectomy vs total gastrectomy, P = 0.41; bypass vs laparotomy, P = 0.61; ^[dagger]only resected cases are included

Table 6. Multivariate analysis of independent risk factors for morbidity and mortality

Factor	Odds ratio	P-value	95% CI
Morbidity*
No. of medical illnesses		<0.01
0-1	1
>1	4.91		1.73-13.9
Mortality[dagger]
No. of medical illnesses		<0.005
0-1	1
>1	3.41		1.71-6.75
Distant metastasis		<0.005
Absent	1
Present	2.82		1.57-5.05

^*Goodness of fit test, P = 0.12; ^[dagger]goodness of fit test, P = 0.21; CI, confidence interval

Morbidity and mortality rates according to different variables are given in Table 5. Statistical analysis of these variables identified the number of preexisting medical illnesses as a major risk factor for morbidity. Multivariate analysis confirmed such a risk factor as the only independent variable (P < 0.01) (Table 6). Multivariate analysis was performed separately for resected cases; the results confirmed the number of medical illnesses as the only independent predictor of morbidity. Univariate analysis applied to mortality identified the number of preexisting medical illnesses (P < 0.005), non-resective procedures (P < 0.005) and the presence of metastasis (P < 0.005) as significant risk factors. On the other hand, multivariate analysis identified the presence of metastasis (P < 0.005) and multiple medical illnesses (P < 0.005) as independent variables. Table 7 reports the morbidity and mortality rates obtained in resected and non resected patients according to the number of medical illnesses. When multiple medical illnesses were present, much higher morbidity rates in resected patients and morbidity and mortality rates in non resected patients were observed.

Table 7. Morbidity and mortality rates in resected and non resected patients according to the number of medical illnesses

No. of medical	Operative procedure
illnesses	Resected		Non resected
	Morbidity (%)	Mortality (%)	Morbidity (%)	Mortality (%)
0-1	18.2	3.0	16.7	0.0
>1	42.1	5.3	64.3	57.1

With regard to long-term survival, 16 patients were still alive at the end date of follow-up, while 77 had died because of cancer recurrence. In seven patients, death occurred due to causes other than neoplasia, with a median interval of 54 months. These seven patients were affected with preexisting medical illnesses that were multiple in two of the cases. Overall, the crude 5-year survival rate was 20%; following curative surgery, this value rose to 43%. Fig. 1 shows long-term survival rates, for those patients who had curative surgery, according to the presence of postoperative complications; no significant difference was found between these groups (P = 0.96). Patients without preexisting medical illnesses had a better survival rate than those with one illness or multiple illnesses, although the difference was not statistically significant (P = 0.14) (Fig. 2).

Figure 1. Long-term survival of curatively resected patients with regard to the presence of postoperative complications (- - - -, absent; -, present). Ticks represent censored cases.

Figure 2. Long-term survival of curatively resected patients with regard to the number of preexisting medical illnesses (- - - -, none; -, one; -, two or more). Ticks represent censored cases.

DISCUSSION

With few exceptions, surgeons in the past have always ruled out surgery for patients aged 80 and over. Recent progress, however, has offered such individuals new possibilities and, indeed, many aged patients undergo even major surgery (24).

Basic physiological faculties in the aged often change as the various organs fail to function (25). The literature gives numerous examples of how organ system functionality declines in subjects aged 80 and over (7,26,27). The most common malfunctions include hypertension, arrhythmia, lung pathologies and hypoproteinemia which are significantly more frequent than in 70-79-year-old patients (13).

Recent advance in several fields such as anaesthesiology, intensive care and surgical techniques, as well as an adequate treatment of concomitant illnesses and a thorough selection of patients, have made surgery more reliable for patients 80 and over (24), although operative mortality rates are still high in emergency operations (26). Our experience is of a significant increase, in recent years, of operability and resectability rates of aged patients (data not shown), which confirm that surgical therapy is becoming more aggressive in this age group. Although these rates are still lower compared to most Japanese authors (7,13), they are among the highest in Western reports (3,17).

Total gastrectomy is undoubtedly the most challenging operation for gastric cancer, as it involves higher morbidity and mortality rates (19). Most authors agree that this procedure should be performed in patients 80 and over only when necessary. Korenaga et al. carried out a multivariate analysis that identified total gastrectomy as the major risk factor for complications, due to excessive intraoperative blood loss and lengthy surgery (27). Other Japanese authors performed total gastrectomy and combined resections in very few aged patients (13,15). In elderly patients, second and third level lymphadenectomy involves higher morbidity and mortality rates (5,9,13), although this finding was not confirmed by other authors (27). Therefore, non-extended lymphadenectomy is the preferred procedure in patients aged 80 and over (13,15). We executed total gastrectomy only when necessary and in selected patients. Likewise, combined resections and extended lymphadenectomy were carried out in very few cases. In 29 patients, we performed a standard lymphadenectomy. This approach is linked to the antral location of tumors, frequent in these patients as previously reported by other authors (7,14,27). The resulting data emphasize the validity of our surgical approach; the mortality rate of resected patients reached 3.8%, which is a very low rate compared to other Western authors. In a multicenter study, Damhius and Tilanus reported an 11.2% mortality rate (3); in another study, Visteet al. reported 15% (4), and a population-based study in the United Kingdom reported a 23% mortality rate (28).

All these data refer to cases treated with resective procedures. Our results coincide with those obtained by Japanese authors who affirm mortality rates between 0-6% (7,13-15,27). The morbidity values we obtained were not significantly different, comparing the different surgical techniques. Former studies acknowledge the importance of coexisting disorders in postoperative complications rather than the age factor itself (25,29). Our results indicate that the most important predictor of morbidity is the number of preexisting medical illnesses. Multiple medical illnesses in resected patients involved a higher morbidity rate (42.1%) than patients with no illness or one illness (18.2%). No patient who underwent total gastrectomy or extended surgery died in the postoperative period. Following standard or extended lymphadenectomy a higher morbidity rate was observed, but this difference was not statistically significant in either the univariate or multivariate analysis; mortality rates did not differ. These results might be due to the selection of patients which influenced our surgical approach. Operative mortality rate including non-resective surgery was 12.8%. Besides medical illnesses, other factors such as the presence of metastasis raise this rate, which is higher in non-resective surgery than with resections. The presence of multiple medical illnesses in patients with locally advanced neoplasm or distant metastasis (not resected patients) was fatal in most cases (57.1% mortality rate vs 0% in cases with none or one illness). In these cases a careful preoperative staging of neoplasia is especially important.

Morbidity rate is higher in males than in females and mortality rate is four times higher in males. These data confirm what has been reported in the literature (3-5). Viste et al. have shown that the mortality rate in males increases almost exponentially with age compared with females, but they have not found what influences this pattern (4). Sex was not an independent variable in our study, but we found most cases with multiple general illnesses in males. This observation may shed more light on how aged males are more prone to complications.

Cardiovascular disorders were the most frequently observed complications in our study; they occurred above all in cases of highly advanced malignancy and were fatal in most cases. Pulmonary complications, reported in the literature as frequent in aged patients (7,13,27), were observed in only two of our cases. This might be due to the lower incidence of preexisting pulmonary illnesses in our patients. Anastomotic leakage was reported as the most frequent cause of mortality in elderly patients (30). This complication occurred in few cases: in two patients following total gastrectomy and in one following subtotal gastrectomy. All patients healed with conservative treatment by perianastomotic drainage. Our results show that major complications can be efficiently treated even in aged patients.

As for patients of other age groups, survival rates obtained by Japanese authors (7,14,27) are much higher than those reported by Western authors (18,26). In our findings, the 43% five-year survival rate following curative surgery is among the highest reported in Western literature. Postoperative complications did not influence long-term survival rates of curatively resected patients. Preexisting medical illnesses seem to play a more important role, although the low number of patients does not allow for statistical significance. All the seven patients who died of causes other than neoplasia had preoperative medical illnesses, but deaths occurred with a median interval of 54 months. This confirms that aged patients are naturally age-selected individuals, and most deaths within five years from surgery occur due to cancer recurrence.

Our results indicate that the age factor itself should not rule out surgery. In particular, special attention should be given to the preoperative evaluation of the patient's general condition and to an adequate treatment of any preexisting diseases prior to surgery. To avoid high risk operations, thorough preoperative staging of the neoplasia is mandatory in order to establish the possibility of resection. Preference should be given to subtotal gastrectomy with limited lymphadenectomy; total gastrectomy, combined resections and extended lymphadenectomy should be performed only when necessary, in patients with fewer than two medical illnesses. Surgery should be avoided in patients with highly advanced disease (distant metastasis or locally advanced cancer), if multiple medical illnesses are present. The results we obtained indicate that curative surgery provides good long-term survival even in aged patients; in fact, in Western countries patients aged 80 years and over have a 6-9-year life expectancy, as reported in demographic studies (31).

Acknowledgements

This work has been the subject of an oral presentation at the 2nd International Gastric Cancer Congress, Munich, April 27-30, 1997.

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Received August 1, 1997; accepted October 20, 1997
For reprints and all correspondence: Franco Roviello, Via Mentana 16, 53100 Siena, Italy
Abbreviations: JRSGC, Japanese Research Society for Gastric Cancer; UICC, Union Internationale contre le Cancer.

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