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Ann Thorac Surg 2004;77:1740-1744
© 2004 The Society of Thoracic Surgeons

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Original article: general thoracic

Long-term results of operation for 420 patients with early squamous cell esophageal carcinoma discovered by screening

^a Department of Thoracic Surgical Oncology, Cancer Institute/Hospital, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing, China
^b Esophageal Cancer Hospital, Linzhou City, Henan Province, China,
^c Tai-Hang Hospital, Linzhou City, Henan Province China
^d Department of Pathology, Cancer Institute, Chinese Academy of Medical Sciences, Beijing, China,
^e Department of Epidemiology, Cancer Institute, Chinese Academy of Medical Sciences, Beijing, China

Accepted for publication October 28, 2003.

^* Address reprint requests to Dr Wang, PO Box 2258, Beijing 100021, People's Republic of China
e-mail: wgq2581{at}yahoo.com.cn

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
BACKGROUND: Cancer of the esophagus is one of the most commonly seen malignancies in China. From 1959 to 1981, mass screening of esophageal cancer disclosed that the age-adjusted incidence in the 40- to 69-year-old population in Lin County, Henan Province, was 470/10⁵ In its northern part, an even higher incidence of 760/10⁵was found. As they were discovered by mass screening, most of them were found to have early lesions. Surgical treatment was done in attempt to find out the feasibility of managing esophageal carcinoma by early diagnosis and early treatment. This paper is the result of the long-term follow-up.

METHODS: Since 1972, a total of 17 extensive mass screening has been conducted among more than 160,000 participants in the rural areas in Henan, Hebei, and northern Jiangsu provinces, sorting out more than 30,000 high-risk individuals. Among these individuals, 24,600 were examined by endoscopy, discovering 2,094 patients with carcinomas in the esophagus or gastric cardia; 757 of these 2,094 patients were found to have superficial esophageal cancer; 420 patients accepted surgical treatment. Esophagectomy with gastric replacement was performed through left thoracotomy in all patients. Cervical anastomosis 94 (22.4%), intrathoracic supraaortic anastomosis 307 (73.1%), and infra-aortic anastomosis 19 (4.5%) were done. Double thoracoabdominal lymphatic dissection was performed.

RESULTS: The resection rate was 100%. One-month operative mortality occurred in 5 (1.2%). Postoperative complications developed and were satisfactorily treated in 28 patients (6.7%). Pathology of the cancer specimens showed that there were carcinoma in situ in 76 (all without lymphatic metastasis), intramucosal (TI) carcinoma in 126 (2 [1.6%] with lymphatic metastasis), and submucous infiltrating (TI) cacinoma in 218 (34 [15.6%] with lymphatic metastasis). All these 420 patients have been followed up to 2001 with a follow-up rate of 94.1%. Those who were lost to follow-up were taken as censored cases. The survival rates were calculated by the life-table method. The 5-, 10-, 15-, 20-, and 25-year survival rates were 86.14%, 75.03%, 64.48%, 56.17%, and 49.93%, respectively.

CONCLUSIONS: Esophageal balloon cytology, endoscopy, mucosa 1.2% iodine stain, and multipoint biopsy may be the best approach for early diagnosis of esophageal carcinoma. Surgical resection of superficial esophageal cancer provides excellent long-term survival with acceptable quality of life. It was discovered that carcinoma in situ and intramucosal carcinoma gave far better results than the submucosal infiltrative carcinoma, as the latter tends to have a higher frequency of lymphatic metastasis.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
Carcinoma of the esophagus, one of the most common malignancies in China, is frequently found in the north and northwestern regions especially around the Tai-Hang Mountain. Mass screenings for esophageal cancer conducted from 1959 through 1981 showed that the age-adjusted annual mortality rate of this cancer in the 40- to 69-year-old population group was 470/10⁵. In a special area, the Lin County in Henan Province, it was as high as 760/10⁵ [1–3].

Esophageal carcinoma has a very poor prognosis when the disease presents symptomatically, but has a very good prognosis if detected when limited to the mucosa or submucosa. There is, therefore, a major benefit in detecting the tumors before they become manifest clinically. Currently, this can only be achieved by using screening programs. Since 1972, the authors have conducted studies of esophageal cancer in the high risk area, and got more experience of surgery for superficial (Tis, TI) esophageal cancer screened in the rural areas [4]. The purposes of this analysis are to review our 30-year experience with esophagectomy for superficial squamous cell carcinoma (Tis, TI) of esophagus and to address the long-term survival.

The studies were approved by Institutional Review Board of the Cancer Institute, Chinese Academy of Medical Sciences, and informed consent was obtained from each subject before the procedure.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
Patients from the screenings
Since 1972, a total of 17 large-scale mass screenings in a rural area with 160,000 asymptomatic participants aged more than 40 years have been conducted in Lin County, Henan Province, Ci County, Hebei Province, and the northern part of Jiangsu Province. Using esophageal balloon cytology and occult blood test as the primary method of screening, we found from the villages in those counties 30,000 high-risk subjects who were positive on the cytology and occult blood test [5, 6].

In all, 24,600 of these people accepted endoscopic examination, and 2,094 had been diagnosed as cancers of the esophagus and gastric cardia; 5,400 subjects (18%) refused the endoscopy. During endoscopic procedure, iodine (1.2%) staining to the esophageal mucous membrane was used in all subjects. From the unstained foci (the positive foci), multiple biopsies were taken; and upon negative endoscopic findings, according to the planned procedure, two blind biopsies were sampled from sites 25 cm and 35 cm from the incisors. The biopsy specimens were fixed in 10% buffered formalin, embedded in paraffin, cut in 5 µm sections, and stained with hematoxylin and eosin. The biopsy slides were read by two pathologists in Beijing, without knowledge of the visual endoscopic findings. The histologic criteria were based on previous descriptions [21].

In all, 2,094 cases with carcinoma of esophagus and cardia were found by endoscopy in screening. Among them, 757 cases were diagnosed by biopsy as superficial esophageal cancer. Of 757 cases, 420 patients underwent esophagectomy, and endoscopic mucosal resection has been performed in 124 cases. The remaining patients with no symptoms refused any management and had subsequent development of advanced squamous cell carcinoma of the esophagus. About 1,550 more patients with advanced esophageal and cardiac cancer underwent esophagectomy, radiotherapy, and chemotherapy in different periods. The treated outcome has been addressed in previous reports by us [7–11].

Patient selection for surgery
Among 420 patients who accepted esophagectomy as treatment, there were 213 males and 189 females with a sex ratio of 1.22:1. The age distributions were less than 39 years, 13 (3.1%); 40 to 49, 103 (24.5%); 50 to 59, 185 (44%); 60 to 69, 115 (27.4%); and 0.70, 4 (0.95%). Mean age was 53.5 years. Before admission, only 12.1% (51 of 420) patients had complained of transient discomfort or pain on deglutition. But upon being questioned by the doctor in the ward, 386 (91.9%) admitted that there had been symptoms related to the upper digestive tract. All the patients were in good health upon admission into the ward.

Site of lesion and method of resection
Of the 420 lesions, 71 (16.9%) were located in the upper thoracic segment, 307 (73.1%) in the midthoracic segment, and 42 (10%) in the lower thoracic segment. The resection of all cases with the esophageal carcinoma was done through a left posterolateral thoracotomy followed in the same stage by esophagogastrostomy, which was done in the neck in 94 (22.4%), in the thorax above the aortic arch in 307 (73.1%), and in the infra-aortic region in 19 (4.5%). The esophagogastrostomy covered by a tongue-like seromuscular flap of gastric wall as a manual anastomotic technique developed by the authors was used for the anastomotic procedure in all patients with esophageal carcinoma [7, 8]. The gastric replacement was used for all patients without pylorotomy or pyloroplasty [19]. A routine lymph node dissection was carried out in the mediastinum as well as in the abdomen. In the majority of the cases, the esophagus was found to be practically normal even on palpation during operation (Fig 1). The tumor was palpable as thickness of esophageal wall in only 12 cases. The resection rate was 100%.

View larger version (64K): [in this window] [in a new window]   Fig 1. Flat type of early esophageal cancer. The lesion is shown clearly after staining (right; pathology: carcinoma in situ) while not found on the surgical specimen (left).

	Results

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Postoperative complications and operative mortality rate
Twenty-eight patients (6.7%) with postoperative complications are shown in Table 1. All these episodes healed uneventfully, except for 5 cases that resulted in operative death. The operative mortality rate was 1.2% (5 of 420).

View larger version (14K): [in this window] [in a new window]   Fig 2. Postoperative survival of 420 patients with early esophageal carcinomas.

	Comment

Top Abstract Introduction Patients and methods Results Comment References

Since the 1960s, with the advent of exfoliative cytology, more and more superficial esophageal cancers have been found, giving a corresponding better result of surgical treatment [5, 12, 14]. From the 1980s, the improvement of endoscopy and staining methods have further help to discover greater mount of early esophageal cancers and precancerous lesions in the esophagus [17, 18]. Not only does it facilitate the invention and improvement of endoscopic minimal invasive surgery [11, 13], but it also provides great patient resources for traditional operative management. We believe that the combination of endoscopic examination, in vivo iodine stain, and multipoint biopsy is the best technical method available; and we also expect the outlook of surgery for esophageal cancer to be more and more optimistic in the future.

Early esophageal cancer, being in the subclinical stage, usually has no symptoms. Among our patients, only 12.1% had complained of discomfort or pain upon swallowing. Yet, this complaint rose to 91.9% after admission, presumably because of specific questioning by the doctors and the environmental mental pressure and power of suggestion in the hospital. The surgeons could not feel any abnormality of the esophagus during operation. So definitive diagnosis and exact location are very important before surgery; the necessity of endoscopy and in vivo iodine stain are absolutely needed for finding the lesion and locating the upper margin in order to properly resect the esophagus and do the anastomosis. Everything should be done perfectly beforehand to avoid the unfortunate situation of not being able to find the lesion and doubt the diagnosis with the patient on the operating table. Thus, the unwanted procedures of excising the esophagus to brush or taking frozen biopsies again to establish the diagnosis could be eliminated. In this series, the operative complications were relatively low. That was because of the relatively young age (mean age, 53.5 years) and good general condition of the patients. Finally, low complications rates were also related to surgical skill and patient care.

The criteria of diagnosing superficial (Tis, TI) esophageal carcinoma were based on the pathology findings of the resected specimens, not counting the incidence of lymphatic metastasis. As early esophageal cancer belongs to the subclinical disease, most of the screened subjects would not go to the doctor voluntarily because they had not had any subjective symptoms. Furthermore, we had aimed at finding the incidence of lymphatic spread of carcinoma in situ, intramucocal carcinoma, and submucous infiltrating carcinoma, and their respective outcome. The final results showed that the last type, having a higher incidence of lymphatic metastasis, is prognostically inferior to the former two types.

The total number of patients who died during the 25 years of follow-up is 89, among whom 44 (49.4%) succumbed to cancer recurrence or metastasis. Recurrence means an anastomotic relapse or a cancer in the residual esophagus. Metastasis means metastasis in the mediastinum, neck, or other organs that was not proved as a second primary or metastatic focus from a second primary. In this article, a second primary means a primary malignant tumor in other organs definitely proved such as liver cancer, lung cancer, or cancer of the intestine. However, those recurrences originated from the precancerous lesions on the mucosa of the residual esophagus. It is difficult to distinguish the recurrent and the second primaries beyond 5 years. In this analysis, we considered all cancer in the remaining esophagus as recurrent. Dawsey and associates [2] reported that the incidence of 3.5-year cancerous degeneration of severe and moderate dysplasia was 65% and 26%, respectively. This finding conforms well with the theory of esophageal squamous cell carcinoma arising from dysplasia. Therefore, before the surgical intervention, endoscopy with iodine stain must be done proximal to the cancer focus already discovered. If a positive lesion of moderate or severe dysplasia is found, the level of resection must be proximally shifted so as to ensure an adequate resection.

Most of the patients who died of causes unrelated to cancer did so from cardiovascular diseases or trauma. In these mountainous areas, falling is common. Thirty-three patients died of causes unknown or were lost to follow-up, comprising 37% of the total deaths. Those lost to follow-up had untraceable changes of address.

When there is extension of superficial esophageal cancer into the submucosa, the rate of lymphatic metastasis varies from 15% to 57% [15, 16]. These data from our series show that the incidence of lymphatic metastasis of submucous infiltrating carcinoma, being 15.6% (34 of 218), gave a total mortality rate of 30.7% (67 of 218), comprising 75.2% (67 of 89) of the total toll (Table 4). This demonstrates far poorer outcome (5-year survival, 64.5%) of this category, which has 5-year survival rates lower than that of carcinoma in situ (96.8%) and intramucosal infiltrating carcinoma (97.9%) [20]. The subtotal esophagectomy in patients was performed through the left thoracotomy approach with combined thoracoabdominal lymphatic dissection. However, no lower neck and right side dissection was done. That might be the reason for having a lower incidence of lymphatic metastasis than those reported in the literature. We suggest that radical esophagectomy should be performed for submucous infiltrating carcinoma because it has a relatively high incidence of lymph nodes. We do not recommend induction therapy, because the lymph nodes of metastasis may be left in the mediastina by that procedure [15].

	References

Top Abstract Introduction Patients and methods Results Comment References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Wang, G.-Q. Articles by Yang, L. Search for Related Content PubMed PubMed Citation Articles by Wang, G.-Q. Articles by Yang, L. Related Collections Esophagus - cancer