Br. J. Surg. 1992, Vol. 79, September, 935-937
K. Moghissi Humberside Cardiothoracic Surgical Centre, Castle Hill Hospital, Cottingham, Hull, North Humberside HU16 5J0, UK Correspondence to: Mr K. Moghissi
Surgical resection for stage I cancer of the oesophagus and cardia A study was carried out to establish the long-term survival ofpatients with stage I carcinoma of the oesophagus and cardia, and to assess the influence of various factors on the 5-year survival rate. The study, which was partly prospective and partly retrospective, involved 60 patients with early (stage I ) carcinoma of the oesophagus or cardia f r o m a total o f 8 1 1 consecutive patients with such carcinomas who were referred to one regional centre over a 1.5-year period, 42.5 of whom underwent resection. Survival at 5 years was taken as the main measure of outcome. Forty-two patients (70 per cent) were alive at 5 years. None of the factors studied (sex, age, site or histological type of tumour) had a signijicant eflect on outcome.
According to the classification of the American Joint Committee on Cancer', stage I oesophageal cancers are those that involve up to 5 c m of the length of the oesophagus ( T I ) with no extraoesophageal spread, no lymph node involvement (No), and no known distant metastases (Mo). The author has been unable to find any report in Europe devoted specifically t o the treatment and prognosis of stage I carcinoma of the oesophagus and cardia. This paper presents the results of a partly prospective, partly retrospective study of all patients with stage I disease treated in one regional referral centre over a 15-year period.
Patients and methods Between September 1970 and September 1985,811 consecutive patients with carcinoma of the oesophagus were referred to the author. Treatment policy was always to offer resection provided there was no evidence of distant metastasis and the patient was fit for operation. Advanced age alone was not regarded as a reason for withholding surgery. Of the 811 patients, 425 (52 per cent) underwent resection of the tumour and reconstruction of the upper alimentary tract. Only 60 patients with stage I lesions were identified after clinical and pathological analysis of the resected specimens. Apart from routine biochemical and haematological investigations, every patient underwent a radiographic contrast examination, oesophagoscopy and biopsy, bronchoscopy, and abdominal ultrasonography. Computed tomography was used once it had become available. From the results of these investigations the type and extent of resection was planned. Operation The operation performed was a Lewis oesophagectomy with oesophagogastric anastomosis in the right chest2 in 21 patients with a mid-thoracic tumour, and a left thorac~phrenotomy~ in 39 patients with carcinoma of the lower oesophagus and cardia. These were reconstructed by oesophagogastre~tomy~in 36 cases, but in two patients who had undergone previous gastric surgery, and in one with suspicion of gastric invasion, total gastrectomy with Roux-en-Y oesophagojejunostomy was performed. In all 60 stage I patients, the tumour was resected together with at least 5 cm of macroscopically normal tissue on either side. Mediastinal and coeliac lymph nodes were included in the resection. All oesophageal anastomoses were made in two layers using interrupted silk sutures, and resected specimens sent for detailed histological examination for tumour staging. Postoperative follow-up After discharge from hospital patients were followed up at intervals of 1 month, 3 months and thereafter every 6 months for 5 years or until death. Those who survived for more than 5 years were seen annually. Patients with symptoms suggestive of recurrent tumour were admitted for investigation and palliation.
0007-1323/92/09093543
0 1992 Butterworth-Heinemann
Ltd
Survival was calculated by the life-table method5. Differences between mortality related to variables studied were analysed by Armitage's standardized normal deviate. Confidence interval ( c i ) calculations used the CIA microcomputer program (Version 1.1;British Medical Association, London, UK).
Results Of the 60 patients with stage I disease, there were 31 men and 29 women; the mean age was 64 (range 38-83) years. The sites and histological types of tumours are shown in Table I . The mode of presentation and symptoms on admission are shown in Table2. The mean duration of symptoms before referral was 10 (range 6-16) weeks. There were no postoperative anastomotic leaks or other serious complications. One patient died 3 days after operation from myocardial infarction, and a second died a t home 3 months after operation of bleeding from ulceration at the site of the anastomosis. The
Table 1 Site and histological type of 60 stage I tumours of the oesophagus and cardia
Histological type Site
Squamous
Adenocarcinoma
Undifferentiated
Mid-thoracic oesophagus Lower thoracic oesophagus and cardia
18 (30)
3 (5)
0 (0)
7 (12)
31 (52)
1(2)
Total
25 (42)
34 (57)
1(2)
Values in parentheses are percentages
Table 2 Symptoms and mode of presentation in 60 patienrs with stage I carcinoma of the oesophagus and cardia
Symptom
No. of patients with main presenting symptom
No. of patients with symptom on admission
Dysphagia Retrosternal pain or heartburn Haematemesis Nausea and vomiting
52 5 2 1
55 29 4 4
935
Early cancer of the oesophagus and cardia: K. Moghissi
m
Y
2
80
50
"
.-r
-
'
0
n v
I 2
I
1
I
I
3
4
G
I 5
Time a f t e r o p e r a t i o n [ y e a r s )
Figure 1 Survival curve for 60 patients undergoing operation for stage I carcinoma of the oesophagus and cardia. 0 , Deathsfrom cancer: 0, censored deaths (those known to be unrelated to cancer)
Table 3 Fioe-year survival rate ofpatients with cancer of the oesophagus and cardia: association with sex, age, site ofturnour and histological type Associated variables
Total
Sex (n)* 31 M 29 F Mean (range) age 64 (38-83) (years) Site of tumour ( n ) * 21 Mid-thoracic Lower thoracic 39 Histological type (n)* Adenocarcinoma 34 Squamous 25 Undifferentiated 1
Survival at 5 years
Death within 5 years
Death in hospital
21 (68) 21 (72) 63 (38-83)
10 (32) 7 (24) 67 (50-81)
0 (0) 1(3) 78
11 (52) 31 (79) 27 (79) 14 (56) 1(1@))
*Values in parentheses are percentages
actuarial survival curve is shown in Figure I ; 42 patients (70 per cent) were alive 5 years after operation. The cause of death was known in 14 of the further 16 patients who died: metastatic carcinoma ( n = 7 ) and debility, old age and conditions unrelated to the oesophageal cancer ( n = 7). The influence on mortality of age, sex, site of tumour and its histological type is shown in Table 3. Age and sex had no influace on survival. More patients with tumours in the lower oesophagus survived than with tumours in the mid-oesophagus ( U = 1.89, P = 0.059; difference 27 (95 per cent c.i. 2-52) per cent). Those with adenocarcinomas (including one patient with an undifferentiated carcinoma) also had a survival advantage over those with squamous carcinoma (difference 24 (95 per cent c.i. 1-48 ) per cent), although the difference was not significant.
of the oesophagus continues to be regarded as solely palliative by many who refer patients to specialist centres. There is, however, a subgroup of patients in whom the long-term survival rate after resection is considerably This subgroup, those with stage I cancers, merits detailed study to attempt to determine those characteristics which make the outcome in these patients so much more favourable. All 60 patients reported here were symptomatic before diagnosis and in 52 (87 per cent) the presenting symptom was dysphagia. Endo et al." found that most (72 per cent) of the 69 patients they described with early disease had symptoms, commonly dysphagia. These were all submucosal tumours as defined by the Japanese Society for Diseases of the Oesophagus' . The remainder were detected by screening or during routine follow-up for other conditions of the upper gastrointestinal tract. Therefore, most patients with stage I cancer present with dysphagia; this suggests that early oesophageal cancer can be detected without a complicated and expensive screening programme, provided those concerned in primary care are aware of it. The incidence of early, or stage I, tumours in any surgical series of carcinoma of the oesophagus depends on the criteria the method of detection and the used to define pattern of referral to that particular surgeon. There are difficulties of interpretation of results, however, because not all authors present their data clearly7. Patients with stage 1 cancer comprised 14 per cent of those undergoing resection in the present series, and 7 per cent of the total number referred. Using similar criteria Gatzinsky et reported 14 early cancers in a total of 185 patients (8 per cent), and Hennessy and Keeling'4 found 5 per cent in a series of 239. Using the Japanese classification (in which the criteria are somewhat stricter) HuangI5 and Endo et al." found a frequency of 3 per cent, but whatever the incidence there is no doubt that the survival rate after resection is considerably higher in patients with early cancer than in the more advanced cases. Both the hospital mortality rate ( 2 per cent) and 5-year survival rate (70 per cent) in the present series compare favourably with data reported by other authors, mostly from Japan and China9.10~17~'8, who used more stringent classification criteria. Neither age nor sex seems to have influenced long-term survival; some authors have reported better results in women, but they were concerned with overall outcome rather than just with stage I tumours' 3 * 1 9 - 2 1 . The site and histological type of the tumour did not have any significant influence on long-term survival, although patients with tumours in the lower oesophagus and those with adenocarcinomas tended to do better than the others. This is contrary to results expressed by some authors'.'' but consistent with the findings of Giuli and Gignoux". In conclusion, the general pessimism towards patients with carcinoma of the oesophagus or cardia should be tempered by the knowledge that some can be cured by timely and adequate resection.
'
Discussion During the past 10- 15 years there has been not only a reduction in postoperative morbidity and mortality rates among patients undergoing oesophagectomy and gastro-oesophageal reconstruction, but also improvement in the short-term survival rate637.This improvement has not, however, been matched by a corresponding overall improvement in the 5-year survival rate after resection, which remains7 about 10 per cent. One of the difficulties in assessing published reports is that there is little or no agreement regarding definition, amount of data reported, or method of analysis, so that even the quoted 5-year survival rate of 10 per cent loses credence. These problems include failure to indicate operability and resectability rates and exclusion of hospital mortality from discussion of long-term survival. As a result, the role of surgery in the treatment of carcinoma
936
Acknowledgements The author thanks Miss Mary Evans for help with statistical analysis.
References Beahrs OH, Myers M H , eds. American Joint Committee on Cancer. Manual for Staging of Cancer. 2nd ed. Philadelphia: JB Lippincott, 1983. Lewis I. The surgical treatment of carcinoma of the oesophagus with special reference to a new operation for growths of the middle third. Br J Surg 1946; 34: 18-31. Thompson VC. Carcinoma of the oesophagus, resection and oesophagogastrectomy. Br J Surg 1945; 32: 377-80. Moghissi K. Resection and reconstruction of the oesophagus. In: Moghissi K, ed. The Essentials of Thoracic and Cardiac Surgery. London: Heinemann, 1986: 297-9.
Br. J. Surg., Vol. 79, No. 9. September 1992
Early cancer of the oesophagus and cardia: K. Moghissi Pet0 R, Pike MC, Armitage P et al. Design and analysis of randomized clinical trials requiring prolonged observation of each patient. 11: Analysis and examples. Er J Cancer 1977; 35: 1-39. 6. Earlam R, Cunha-Melo JR. Oesophageal squamous cell carcinoma: a critical review of surgery. Br J Surg 1980; 67: 381-90. 7. Muller JM, Erasmi H, Stelzner M, Zieren U, Pickzmaier H. Surgical therapy of oesophageal carcinoma. Br J Surg 1990; 77: 845- 57. 8. Lund 0,Hasenkam JM, Agaard MT, Kimose HH. Time-related changes in characteristics of prognostic significance in carcinomas of the oesophagus and cardia. Er J Surg 1989; 76: 1301-7. 9. Lu Yun Kan, Li Yeuh Min, Gu Yue Zhi. Cancer of esophagus and esophagogastric junction: analysis of results of 1025 resectionsafter 5 to20years. Ann ThoracSurg 1987;43: 176-81. 10. Endo M, Ide H, Yoshino K, Yoshida M. Diagnosis and treatment of early esophageal cancer. In: Siewert JR, Holscher AH, eds. Diseases of the Esophagus. Berlin: Springer-Verlag, 1988:375-80. 11. Japanese Society for Diseases of the Oesophagus. Guidelines for clinical and pathological studies of carcinoma of the oesophagus. Jpn J Surg 1976; 6 : 69-86. 12. Harmer MH, ed. TNM Classijication of Malignant Turnours. 3rd ed. Geneva: Union Internacional Contra la Cancrum, 1982. 13. Gatzinsky P, Berglin E, Dernevik L, Larson I, William Olsson G. Resectional operations and long-term results in carcinoma of the esophagus. J Thorac Cardiovasc Surg 1985; 89: 71-6. 5.
Br. J. Surg., Vol. 79, No. 9, September 1992
14. 15. 16.
17. 18.
19. 20. 21. 22.
Hennessy TPJ, Keeling P. Adenocarcinoma of the esophagus and cardia. J Thorac Cardiovasc Surg 1987; 94: 64-8. Huang GJ. The management of early cancer of the oesophagus. In: Jamieson CG, ed. Surgery of the Oesophagus. Edinburgh: Churchill Livingstone, 1988: 629-34. Endo M, Yamada A, Ide H, Yoshida M, Yayashi T, Nakayama K. Early cancer of the esophagus: diagnosis and clinical evaluation. In: Murphy G , ed. International Advances in Surgical Oncology. Vol. 3. New York: Alan R Liss, 1980:49-71. Mitomi T, Makuuchi H, Ogoshi K et al. Treatment of so-called early esophageal carcinoma. In: Siewert JR, Holscher AH, eds. Diseases of the Esophagus. Berlin: Springer-Verlag, 1988:381-4. Yamada A, Hanyu F , Ide H et a/. Superficial esophageal carcinoma with special reference to X-ray diagnosis. In: Siewert JR, Holscher AH, eds. Diseases of the Esophagus. Berlin: Springer-Verlag, 1988: 126-31. Akiyama H, Tsurumaru M, Watanabe G, Ono Y, Udagawa H, Suzuki M. Development of surgery for carcinoma of the esophagus. Am J Surg 1984; 147: 9-16. Salama FD, Leong YP. Resection for carcinoma of the oesophagus. J R Coll Surg Edinb 1989; 34: 97-100. Matthews HR, Walker SJ. Oesophageal carcinoma; the view from East Birmingham. J R Coll Surg Edinb 1990; 35: 279-83. Giuli R,Gignoux M. Treatment ofcarcinoma of the oesophagus. Ann Surg 1980; 192: 144-52.
Paper accepted 29 February 1992
937
K. Moghissi Humberside Cardiothoracic Surgical Centre, Castle Hill Hospital, Cottingham, Hull, North Humberside HU16 5J0, UK Correspondence to: Mr K. Moghissi
Surgical resection for stage I cancer of the oesophagus and cardia A study was carried out to establish the long-term survival ofpatients with stage I carcinoma of the oesophagus and cardia, and to assess the influence of various factors on the 5-year survival rate. The study, which was partly prospective and partly retrospective, involved 60 patients with early (stage I ) carcinoma of the oesophagus or cardia f r o m a total o f 8 1 1 consecutive patients with such carcinomas who were referred to one regional centre over a 1.5-year period, 42.5 of whom underwent resection. Survival at 5 years was taken as the main measure of outcome. Forty-two patients (70 per cent) were alive at 5 years. None of the factors studied (sex, age, site or histological type of tumour) had a signijicant eflect on outcome.
According to the classification of the American Joint Committee on Cancer', stage I oesophageal cancers are those that involve up to 5 c m of the length of the oesophagus ( T I ) with no extraoesophageal spread, no lymph node involvement (No), and no known distant metastases (Mo). The author has been unable to find any report in Europe devoted specifically t o the treatment and prognosis of stage I carcinoma of the oesophagus and cardia. This paper presents the results of a partly prospective, partly retrospective study of all patients with stage I disease treated in one regional referral centre over a 15-year period.
Patients and methods Between September 1970 and September 1985,811 consecutive patients with carcinoma of the oesophagus were referred to the author. Treatment policy was always to offer resection provided there was no evidence of distant metastasis and the patient was fit for operation. Advanced age alone was not regarded as a reason for withholding surgery. Of the 811 patients, 425 (52 per cent) underwent resection of the tumour and reconstruction of the upper alimentary tract. Only 60 patients with stage I lesions were identified after clinical and pathological analysis of the resected specimens. Apart from routine biochemical and haematological investigations, every patient underwent a radiographic contrast examination, oesophagoscopy and biopsy, bronchoscopy, and abdominal ultrasonography. Computed tomography was used once it had become available. From the results of these investigations the type and extent of resection was planned. Operation The operation performed was a Lewis oesophagectomy with oesophagogastric anastomosis in the right chest2 in 21 patients with a mid-thoracic tumour, and a left thorac~phrenotomy~ in 39 patients with carcinoma of the lower oesophagus and cardia. These were reconstructed by oesophagogastre~tomy~in 36 cases, but in two patients who had undergone previous gastric surgery, and in one with suspicion of gastric invasion, total gastrectomy with Roux-en-Y oesophagojejunostomy was performed. In all 60 stage I patients, the tumour was resected together with at least 5 cm of macroscopically normal tissue on either side. Mediastinal and coeliac lymph nodes were included in the resection. All oesophageal anastomoses were made in two layers using interrupted silk sutures, and resected specimens sent for detailed histological examination for tumour staging. Postoperative follow-up After discharge from hospital patients were followed up at intervals of 1 month, 3 months and thereafter every 6 months for 5 years or until death. Those who survived for more than 5 years were seen annually. Patients with symptoms suggestive of recurrent tumour were admitted for investigation and palliation.
0007-1323/92/09093543
0 1992 Butterworth-Heinemann
Ltd
Survival was calculated by the life-table method5. Differences between mortality related to variables studied were analysed by Armitage's standardized normal deviate. Confidence interval ( c i ) calculations used the CIA microcomputer program (Version 1.1;British Medical Association, London, UK).
Results Of the 60 patients with stage I disease, there were 31 men and 29 women; the mean age was 64 (range 38-83) years. The sites and histological types of tumours are shown in Table I . The mode of presentation and symptoms on admission are shown in Table2. The mean duration of symptoms before referral was 10 (range 6-16) weeks. There were no postoperative anastomotic leaks or other serious complications. One patient died 3 days after operation from myocardial infarction, and a second died a t home 3 months after operation of bleeding from ulceration at the site of the anastomosis. The
Table 1 Site and histological type of 60 stage I tumours of the oesophagus and cardia
Histological type Site
Squamous
Adenocarcinoma
Undifferentiated
Mid-thoracic oesophagus Lower thoracic oesophagus and cardia
18 (30)
3 (5)
0 (0)
7 (12)
31 (52)
1(2)
Total
25 (42)
34 (57)
1(2)
Values in parentheses are percentages
Table 2 Symptoms and mode of presentation in 60 patienrs with stage I carcinoma of the oesophagus and cardia
Symptom
No. of patients with main presenting symptom
No. of patients with symptom on admission
Dysphagia Retrosternal pain or heartburn Haematemesis Nausea and vomiting
52 5 2 1
55 29 4 4
935
Early cancer of the oesophagus and cardia: K. Moghissi
m
Y
2
80
50
"
.-r
-
'
0
n v
I 2
I
1
I
I
3
4
G
I 5
Time a f t e r o p e r a t i o n [ y e a r s )
Figure 1 Survival curve for 60 patients undergoing operation for stage I carcinoma of the oesophagus and cardia. 0 , Deathsfrom cancer: 0, censored deaths (those known to be unrelated to cancer)
Table 3 Fioe-year survival rate ofpatients with cancer of the oesophagus and cardia: association with sex, age, site ofturnour and histological type Associated variables
Total
Sex (n)* 31 M 29 F Mean (range) age 64 (38-83) (years) Site of tumour ( n ) * 21 Mid-thoracic Lower thoracic 39 Histological type (n)* Adenocarcinoma 34 Squamous 25 Undifferentiated 1
Survival at 5 years
Death within 5 years
Death in hospital
21 (68) 21 (72) 63 (38-83)
10 (32) 7 (24) 67 (50-81)
0 (0) 1(3) 78
11 (52) 31 (79) 27 (79) 14 (56) 1(1@))
*Values in parentheses are percentages
actuarial survival curve is shown in Figure I ; 42 patients (70 per cent) were alive 5 years after operation. The cause of death was known in 14 of the further 16 patients who died: metastatic carcinoma ( n = 7 ) and debility, old age and conditions unrelated to the oesophageal cancer ( n = 7). The influence on mortality of age, sex, site of tumour and its histological type is shown in Table 3. Age and sex had no influace on survival. More patients with tumours in the lower oesophagus survived than with tumours in the mid-oesophagus ( U = 1.89, P = 0.059; difference 27 (95 per cent c.i. 2-52) per cent). Those with adenocarcinomas (including one patient with an undifferentiated carcinoma) also had a survival advantage over those with squamous carcinoma (difference 24 (95 per cent c.i. 1-48 ) per cent), although the difference was not significant.
of the oesophagus continues to be regarded as solely palliative by many who refer patients to specialist centres. There is, however, a subgroup of patients in whom the long-term survival rate after resection is considerably This subgroup, those with stage I cancers, merits detailed study to attempt to determine those characteristics which make the outcome in these patients so much more favourable. All 60 patients reported here were symptomatic before diagnosis and in 52 (87 per cent) the presenting symptom was dysphagia. Endo et al." found that most (72 per cent) of the 69 patients they described with early disease had symptoms, commonly dysphagia. These were all submucosal tumours as defined by the Japanese Society for Diseases of the Oesophagus' . The remainder were detected by screening or during routine follow-up for other conditions of the upper gastrointestinal tract. Therefore, most patients with stage I cancer present with dysphagia; this suggests that early oesophageal cancer can be detected without a complicated and expensive screening programme, provided those concerned in primary care are aware of it. The incidence of early, or stage I, tumours in any surgical series of carcinoma of the oesophagus depends on the criteria the method of detection and the used to define pattern of referral to that particular surgeon. There are difficulties of interpretation of results, however, because not all authors present their data clearly7. Patients with stage 1 cancer comprised 14 per cent of those undergoing resection in the present series, and 7 per cent of the total number referred. Using similar criteria Gatzinsky et reported 14 early cancers in a total of 185 patients (8 per cent), and Hennessy and Keeling'4 found 5 per cent in a series of 239. Using the Japanese classification (in which the criteria are somewhat stricter) HuangI5 and Endo et al." found a frequency of 3 per cent, but whatever the incidence there is no doubt that the survival rate after resection is considerably higher in patients with early cancer than in the more advanced cases. Both the hospital mortality rate ( 2 per cent) and 5-year survival rate (70 per cent) in the present series compare favourably with data reported by other authors, mostly from Japan and China9.10~17~'8, who used more stringent classification criteria. Neither age nor sex seems to have influenced long-term survival; some authors have reported better results in women, but they were concerned with overall outcome rather than just with stage I tumours' 3 * 1 9 - 2 1 . The site and histological type of the tumour did not have any significant influence on long-term survival, although patients with tumours in the lower oesophagus and those with adenocarcinomas tended to do better than the others. This is contrary to results expressed by some authors'.'' but consistent with the findings of Giuli and Gignoux". In conclusion, the general pessimism towards patients with carcinoma of the oesophagus or cardia should be tempered by the knowledge that some can be cured by timely and adequate resection.
'
Discussion During the past 10- 15 years there has been not only a reduction in postoperative morbidity and mortality rates among patients undergoing oesophagectomy and gastro-oesophageal reconstruction, but also improvement in the short-term survival rate637.This improvement has not, however, been matched by a corresponding overall improvement in the 5-year survival rate after resection, which remains7 about 10 per cent. One of the difficulties in assessing published reports is that there is little or no agreement regarding definition, amount of data reported, or method of analysis, so that even the quoted 5-year survival rate of 10 per cent loses credence. These problems include failure to indicate operability and resectability rates and exclusion of hospital mortality from discussion of long-term survival. As a result, the role of surgery in the treatment of carcinoma
936
Acknowledgements The author thanks Miss Mary Evans for help with statistical analysis.
References Beahrs OH, Myers M H , eds. American Joint Committee on Cancer. Manual for Staging of Cancer. 2nd ed. Philadelphia: JB Lippincott, 1983. Lewis I. The surgical treatment of carcinoma of the oesophagus with special reference to a new operation for growths of the middle third. Br J Surg 1946; 34: 18-31. Thompson VC. Carcinoma of the oesophagus, resection and oesophagogastrectomy. Br J Surg 1945; 32: 377-80. Moghissi K. Resection and reconstruction of the oesophagus. In: Moghissi K, ed. The Essentials of Thoracic and Cardiac Surgery. London: Heinemann, 1986: 297-9.
Br. J. Surg., Vol. 79, No. 9. September 1992
Early cancer of the oesophagus and cardia: K. Moghissi Pet0 R, Pike MC, Armitage P et al. Design and analysis of randomized clinical trials requiring prolonged observation of each patient. 11: Analysis and examples. Er J Cancer 1977; 35: 1-39. 6. Earlam R, Cunha-Melo JR. Oesophageal squamous cell carcinoma: a critical review of surgery. Br J Surg 1980; 67: 381-90. 7. Muller JM, Erasmi H, Stelzner M, Zieren U, Pickzmaier H. Surgical therapy of oesophageal carcinoma. Br J Surg 1990; 77: 845- 57. 8. Lund 0,Hasenkam JM, Agaard MT, Kimose HH. Time-related changes in characteristics of prognostic significance in carcinomas of the oesophagus and cardia. Er J Surg 1989; 76: 1301-7. 9. Lu Yun Kan, Li Yeuh Min, Gu Yue Zhi. Cancer of esophagus and esophagogastric junction: analysis of results of 1025 resectionsafter 5 to20years. Ann ThoracSurg 1987;43: 176-81. 10. Endo M, Ide H, Yoshino K, Yoshida M. Diagnosis and treatment of early esophageal cancer. In: Siewert JR, Holscher AH, eds. Diseases of the Esophagus. Berlin: Springer-Verlag, 1988:375-80. 11. Japanese Society for Diseases of the Oesophagus. Guidelines for clinical and pathological studies of carcinoma of the oesophagus. Jpn J Surg 1976; 6 : 69-86. 12. Harmer MH, ed. TNM Classijication of Malignant Turnours. 3rd ed. Geneva: Union Internacional Contra la Cancrum, 1982. 13. Gatzinsky P, Berglin E, Dernevik L, Larson I, William Olsson G. Resectional operations and long-term results in carcinoma of the esophagus. J Thorac Cardiovasc Surg 1985; 89: 71-6. 5.
Br. J. Surg., Vol. 79, No. 9, September 1992
14. 15. 16.
17. 18.
19. 20. 21. 22.
Hennessy TPJ, Keeling P. Adenocarcinoma of the esophagus and cardia. J Thorac Cardiovasc Surg 1987; 94: 64-8. Huang GJ. The management of early cancer of the oesophagus. In: Jamieson CG, ed. Surgery of the Oesophagus. Edinburgh: Churchill Livingstone, 1988: 629-34. Endo M, Yamada A, Ide H, Yoshida M, Yayashi T, Nakayama K. Early cancer of the esophagus: diagnosis and clinical evaluation. In: Murphy G , ed. International Advances in Surgical Oncology. Vol. 3. New York: Alan R Liss, 1980:49-71. Mitomi T, Makuuchi H, Ogoshi K et al. Treatment of so-called early esophageal carcinoma. In: Siewert JR, Holscher AH, eds. Diseases of the Esophagus. Berlin: Springer-Verlag, 1988:381-4. Yamada A, Hanyu F , Ide H et a/. Superficial esophageal carcinoma with special reference to X-ray diagnosis. In: Siewert JR, Holscher AH, eds. Diseases of the Esophagus. Berlin: Springer-Verlag, 1988: 126-31. Akiyama H, Tsurumaru M, Watanabe G, Ono Y, Udagawa H, Suzuki M. Development of surgery for carcinoma of the esophagus. Am J Surg 1984; 147: 9-16. Salama FD, Leong YP. Resection for carcinoma of the oesophagus. J R Coll Surg Edinb 1989; 34: 97-100. Matthews HR, Walker SJ. Oesophageal carcinoma; the view from East Birmingham. J R Coll Surg Edinb 1990; 35: 279-83. Giuli R,Gignoux M. Treatment ofcarcinoma of the oesophagus. Ann Surg 1980; 192: 144-52.
Paper accepted 29 February 1992
937
