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Ann Thorac Surg 2001;72:867-871
© 2001 The Society of Thoracic Surgeons

Original article: general thoracic

Three-field lymph node dissection for esophageal cancer in elderly patients over 70 years of age

Wentao Fang, MDa, Hiroyasu Igaki, MDa, Yuji Tachimori, MDa, Hiroshi Sato, MDa, Hiroyuki Daiko, MDa, Hoichi Kato, MDa

a Department of Surgery, National Cancer Center Hospital, Tokyo, Japan

Accepted for publication May 16, 2001.

Address reprint requests to Dr Kato, Department of Surgery, National Cancer Center Hospital, 1-1 Tsukiji 5-chome, Chuo-ku, Tokyo, 104-0045, Japan
e-mail: hckato{at}ncc.go.jp


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. The risk and benefit of esophagectomy with three-field lymph node dissection has not been well defined in elderly esophageal cancer patients.

Methods. A total of 441 patients underwent three-field lymph node dissection from 1986 to 1998. Patients were divided into two age groups: group 1 consisted of 79 patients aged 70 years or over, and group 2 consisted of 362 patients under 70 years of age. Patients’ characteristics and surgical outcomes were compared between groups. Risk factors for morbidity, mortality, and survival of patients in group 1 were further studied by multivariate analysis.

Results. Significantly more patients had multiorgan dysfunction preoperatively in group 1 (24; 30.4%) than in group 2 (34; 9.4%, p < 0.001). The overall (65.8% vs 61.6%, p = 0.483) and surgically related complication rates (41.8% vs 52.2%, p = 0.093) were similar, but significantly more organ failure (11.4% vs 5.0%, p = 0.031) and infection (22.8% vs 13.8%, p = 0.045), defined as medical complications, occurred in group 1. There was no significant difference in 30-day (3.8% vs 0.8%, p = 0.074) or in-hospital mortality (7.6% vs 3.3%, p = 0.082) between groups. The overall (40.9% vs 48.1%, p = 0.235) and cause-specific 5-year survivals (55.4% vs 59.1%, p = 0.688) were comparably good in both groups, but the risk of death due to causes other than esophageal cancer was much higher in the elderly (p = 0.028). Multiorgan dysfunction was an independent predictive factor in elderly patients for overall and medical morbidity, overall survival, and risk of death from causes other than esophageal cancer.

Conclusions. Esophagectomy with three-field lymph node dissection could be carried out safely in patients over 70 years of age with satisfactory long-term results. For elderly patients with multiorgan dysfunction, however, less invasive procedures might be more appropriate.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 References
 
Esophageal cancer is a disease that mainly involves elderly patients. Because of increased life expectancy of the population, it is not surprising that the number of esophageal cancers in septuagenarians or octogenarians keeps rising. Until now, esophagectomy, if applicable, offers the best palliation of dysphagia and chance for cure [1]. Since the introduction of extended lymphadenectomy, even better results have been obtained with decreased local-regional recurrence and prolonged survival [2–6]. However, the risk and benefit of extended lymphadenectomy with esophagectomy in elderly patients has not been addressed. We therefore conducted a retrospective study to determine whether transthoracic esophagectomy with three-field (cervico-mediastino-abdominal) lymph node dissection is also justified in patients aged 70 years or over.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
From 1986 to 1998, 1,085 patients were surgically treated for thoracic esophageal cancer at National Cancer Center Hospital, Tokyo, Japan. Among them, 845 were younger than 70 years of age and 240 were aged 70 years or older. Esopha-gectomy was offered to 441 patients with three-field lymph node dissection as a standard procedure by a group of surgeons. These patients were divided into two groups: group 1 consisted of 79 patients aged 70 years or over, and group 2 consisted of 362 patients under age 70 years (32.9% vs 42.8% of all patients, p = 0.007). The rest of the patients underwent less extensive lymphadenectomy.

All patients were assessed with past history, physical examination, routine blood and biochemical tests, chest roentgenogram, electrocardiogram, and pulmonary function tests (arterial blood gas and spirometry). Presence of organ dysfunction was defined only if it was moderate or severe (see below). Preoperative staging was based on the results of esophagogram, endoscopy, computed tomography, and endosonography.

Definition of preoperative organ dysfunction

Pulmonary: symptomatic chronic obstructive pulmonary diseases or obvious pulmonary function abnormal (FEV1 < 2 L or FEV1% < 60%, or PaO2 < 60 mm Hg or PaCO2 > 50 mm Hg).
Cardiovascular: past history or current symptoms and signs of myocardial infarction, angina pectoris, heart failure, alular disease, or high blood pressure needing medical intervention.
Hepatic: past history or current symptoms and signs of cirrhosis or hepatic function impairment.
Renal: past history or current symptoms and signs of renal function impairment.
Cerebrovascular: past history or current symptoms and signs of cerebrovascular events.
Diabetes mellitus: established diagnosis of diabetes mellitus needing medical intervention.

Esophagectomy with three-field lymph node dissection through cervico-thoraco-abdominal approach was carried out as described before [3]. All patients were extubated immediately after operation. Analgesia with morphine was provided through an epidural catheter. Bronchoscopic lavage was routinely performed for a couple of days postoperatively. Oral intake was restored on seventh postoperative day after barium swallow test to rule out anastomotic leakage. Patients who survived the operation were under careful follow-up at 1-month intervals.

The study was carried out in two steps. First, a comparison was made between the two age groups on demographic figures, tumor characteristics, and surgical outcomes. After that, the elderly patients, namely group 1, were isolated and multivariate risk factor analysis for the development of morbidity and mortality, as well as survival after operation, was performed within this group. Possible risk factors entered for morbidity and mortality analysis included duration of symptoms, location and length of tumor, preoperative multiorgan dysfunction, completeness of resection, coresection of other structures during operation, the method of reconstruction, and surgical-pathological tumor staging. The factors entered for survival analysis included patients’ gender, location of tumor, preoperative multiorgan dysfunction, completeness of resection, coresection of other structures during operation, presence of postoperative complication, and surgical-pathological tumor staging.

Contigency tables were analyzed using {chi}2 test or Fisher’s exact test when appropriate. Survival curves were calculated using the Kaplan-Meier method, and difference between groups was compared by log-rank test. Multivariate analysis of risk factors for morbidity and mortality was performed with logistic regression and survival analysis with Cox regression. All probabilities were two-tailed, with p values less than 0.05 regarded as statistically significant.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
Comparison between the two age groups
The characteristics of the two groups were otherwise quite similar, except that in group 1, there were significantly more patients who had multiorgan dysfunction before operation and there were fewer tumors located in the upper thoracic esophagus (Table 1). The operation time (488.0 vs 489.8 minutes, p = 0.859), blood loss (628.2 vs 580.7 ml, p = 0.289), and transfusion during operation (1.1 vs 0.9 units, p = 0.290) were also similar between the two groups. Resection was complete in 93.7% and 86.7% in groups 1 and 2 (p = 0.086), respectively, with 11 (13.9%) and 61 (16.9%) patients receiving coresection of other structures (p = 0.639). Mean numbers of lymph nodes dissected were 65.0 and 67.1, respectively (p = 0.456). In most cases (91.1% vs 93.4%, p = 0.456), a gastric tube was used for reconstruction of the upper digestive tract, and in the rest of the patients, this was fulfilled with either transverse or descending colon.


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  		Table 1. Demographic and Tumor Characteristics

 
Upon pathological examination, more than 90% of the tumors were of squamous cell origin, with adenocarcinoma, undifferentiated carcinoma, basaloid carcinoma, sarcoma, and melanoma occurring in only 7.6% and 6.9%, respectively, of each group (p = 0.799). The surgical-pathological staging of groups 1 and 2 was stage 0 or I in 12 (15.2%) and 51 (14.0%), stage II in 30 (38.0%) and 114 (31.5%), stage III in 28 (35.4%) and 132 (36.5%), and stage IV in 9 (11.4%) and 65 (18.9%) patients, respectively (p = 0.457).

Postoperative complications occurred in 275 (62.4%) patients, leading to 6 (1.4%) deaths within 30 days after operation and a total of 18 (4.1%) deaths during the entire hospital stay. The morbidity rates of the two groups were almost the same. However, organ failure and various kinds of infection, defined as medical complications, occurred significantly more frequently in group 1, while surgical complications more directly related to operative maneuver were similar between the two groups, as shown in Table 2. The 30-day and in-hospital mortality rates were higher in group 1 than those in group 2, but neither reached statistical significance.


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  		Table 2. Morbidity and Mortality

 
Overall 5-year survivals for group 1 and group 2 were 40.9% and 48.1% (p = 0.235) (Fig 1), and cause-specific survivals for esophageal cancer were 55.4% and 59.1%, respectively (p = 0.688). When death due to causes other than esophageal cancer was considered, the risk of death was almost two times (hazard ratio = 1.8319, p = 0.028) higher for patients in group 1 than those in group 2.



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  		Fig 1. Overall survival function of the two groups (log-rank test, p = 0.235).

 
Risk analysis for patients over 70 years of age (group 1)
Among the possible factors entered for multivariate analysis of postoperative complications, preoperative multiorgan dysfunction was identified as the sole independent risk factor for overall and medical morbidity. Among 24 elderly patients with multiorgan dysfunction and the other 55 who had only one or no organ dysfunction, postoperative complications developed in 22 (91.7%) and 30 (54.5%, p = 0.002), while medical complications occurred in 11 (45.8%) and 12 (21.8%, p = 0.031) patients, respectively. Location of tumor in the upper thoracic esophagus was found to be the only independent risk factor for surgical morbidity (see Table 3). None of the factors analyzed was related to increased risk of in-hospital death.


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  		Table 3. Multivariate Analysis of Postoperative Morbidity and Survival in Elderly Patients

 
In survival analysis, pathological T and N staging and gender appeared to be independent risk factors predicting overall and cause-specific survival for esophageal cancer. Multiorgan dysfunction was also identified as an independent risk factor for overall survival and the only predictive factor for death due to causes other than esophageal cancer (Table 3).


   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
References
 
Extended lymph node dissection has been shown to help increase the accuracy of tumor staging, improve long-term survival, decrease local-regional relapse, and therefore may lead to better quality of life after resection of esophageal cancer [2–6]. Although there remains the criticism of a lack of prospective randomized trial, a review of the literature showed that most reports of extended lymphadenectomy claimed long-term survivals around 40% to 50%, while slightly over 30% survival was experienced after lymph node sampling. A nationwide study carried out in Japan comparing two- and three-field lymph node dissection also demonstrated a significant survival advantage of extended lymphadenectomy [7]. However, one of the major reasons against its even wider application is the fear that high morbidity and mortality after extensive surgical maneuver might offset its benefit [4, 8]. This is particularly the case with elderly patients, who are often considered as having higher operative risk and shorter life expectancy. In fact, there was once a time when esophagectomy itself seemed formidable [9]. With the improvement in anesthesia, surgical techniques, and postoperative care, the morbidity and mortality rates after esophagectomy have been drastically reduced [10]. Quite similarly, elderly patients, usually defined as aged over 70 years, used to be denied surgical resection or offered less aggressive palliative procedures. The concept has been challenged recently by a series of reports documenting similar outcomes in elderly patients compared with their younger counterparts [11–16].

To our knowledge, this is the first series reported so far concerning three-field lymph node dissection in patients over 70 years of age. Our data showed that this radical procedure could be carried out in elderly patients with equal safety and satisfactory long-term survival results as in younger patients. The overall morbidity rates were similar between the two age groups. The mortality rate in the elderly patients was higher but did not reach statistical significance. The overall and cause-specific survivals were also quite comparable between the two age groups.

The morbidity rate in our series was within the same range as those reported by Naunheim and associates [11] or Thomas and associates [12], and was higher than those reported by others [13, 15, 16]. However, this kind of comparison was difficult to make because the definition of postoperative complication varies widely between institutions. The 30-day and in-hospital mortality rates of the elderly group were higher than those of the younger group, but both with borderline p values not reaching statistical significance. However, the 7.6% in-hospital mortality rate in our elderly patients compared favorably with the result of a 13% death rate in a collective review of 122 papers including 46,692 patients of all ages, which to some extent represented the level of practice around the world [10].

It is noteworthy that in other series reported during the same time period [11–16], most authors concluded that the safety and benefit of esophagectomy could be attained in selected groups of elderly patients. This kind of selection was reflected mainly in two aspects, ie, what percentage of patients could be selected for surgical treatment, and for those considered operable, what kind of procedure should be selected. Although we did not deny patients surgical therapy because of age, the percentage of elderly patients selected for three-field lymph node dissection was 10% less than that in the younger patients. The extent of resection and radical lymph node dissection, as well as the frequency of colon reconstruction, remained the same in the two age groups under study. Still, the overall morbidity and mortality rates in our patients were similar or lower compared with the above reports, indicating that three-field lymph node dissection could be safely carried out in elderly patients with an acceptable risk (Table 4). At the same time, the long-term result from our series appeared to be the best among all the above-mentioned literature. The 5-year overall and cause-specific survival was 40.9% and 55.4%, respectively, in patients over 70 years of age, which was similar to the results obtained in the younger patients. Therefore, it made us believe that if three-field lymph node dissection did render a better chance of cure for esophageal cancers, it should benefit elderly patients as well as younger ones. Age itself should not be the sole dependent factor in choosing patients for this procedure.


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  		Table 4. Comparison With Data From the Literature of the Same Time Period

 
Because selection is part of the process before offering a surgical option to patients over 70 years of age [17], it naturally leads to the question of what shall be the optimal method of selection. This remains unanswered by the previous literature. One recent study [18] elucidated that more important than age itself are the underlying chronic diseases that are more prevalent in elderly patients, which represent pathological alterations rather than normal physiological aging. This was also true even after selection, as the elderly groups in our series or in some of the other reports [12–14] still had more organ dysfunction than the younger patients. With such a low mortality rate, we were not able to detect any predictive factor for operative related death. But we did find that elderly patients with dysfunction of more than one organ had a much higher risk of developing postoperative complications, especially medically related complications, after three-field dissection. Morbidity rate for this special subgroup was over 90%, and half of these patients developed major organ failure or various kinds of infection. On the other hand, the overall and medical morbidity rates in elderly patients with one or no organ dysfunction were 54.5% and 21.8%, which were quite comparable with those under 70 years of age with (61.9% and 20.6%) or without multiorgan dysfunction (58.8% and 16.8%). Besides, this special subgroup also seemed less likely to benefit from extended lymphadenectomy, as multiorgan dysfunction appeared to be an independent risk factor in multivariate analysis for overall survival and death due to causes other than esophageal cancer. That is to say, even if their tumor could be cured, their chance of dying from preexisting chronic diseases was much higher, with a hazard ratio of 3.7, than those with only one or no obvious organ dysfunction. Therefore, nonsurgical therapy or less invasive procedures with limited lymphadenectomy, with the aim of palliation of dysphagia rather than an intent to cure, might be more appropriate for these special patients.

It is intriguing that gender should be one of the risk factors for survival in the elderly. In our series, the percentage of female patients in the elderly group was twice as that in the younger age group. Others [12, 14, 16] previously have reported similar results. The generally longer life expectancy in the female population alone could not provide a full explanation, as female gender was a favorable factor not only for overall survival but also for cause-specific survival for esophageal cancer. At present, it could only be said that this special phenomenon deserves further exploration.

Thus, we conclude that esophagectomy with three-field lymph node dissection could be carried out safely in patients over 70 years of age with satisfactory long-term results as in younger ones. For the elderly patients with multiorgan dysfunction, however, a balance of risk and benefit should be made upon more careful evaluation of their physical reserve and immune status. Either they should be selected for nonsurgical therapy or for less invasive procedures with the major aim of palliation.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. McLarty A.J., Deschamps C., Trastek V.F., Allen M.S., Pairoleo P.C., Harmsen W.S. Esophageal resection for cancer of the esophagus: long-term function and quality of life. Ann Thorac Surg 1997;63:1568-1572.[Abstract/Free Full Text]
  2. Kato H., Watanabe H., Tachimori Y., Iizuka T. Evaluation of neck lymph node dissection for thoracic esophageal carcinoma. Ann Thorac Surg 1991;51:931-935.[Abstract]
  3. Kato H., Tachimori Y., Watanabe H., Igaki H., Nakanishi Y., Ochiai A. Recurrent esophageal carcinoma after esophagectomy with three-field lymph node dissection. J Surg Oncol 1996;61:267-272.[Medline]
  4. Akiyama H., Tsurumaru M., Udagawa H., Kajiyama Y. Radical lymph node dissection for cancer of the thoracic esophagus. Ann Surg 1994;220:364-373.[Medline]
  5. Lerut T., De Leyn P., Coosemans W., van Raemdonck D., Scheys I., LeSaffre E. Surgical strategies in esophageal carcinoma with emphasis on radical lymphadenectomy. Ann Surg 1992;216:583-590.[Medline]
  6. Altorki N.K., Skinner D.B. Occult cervical nodal metastasis in esophageal cancer: preliminary results of three-field lymphadenectomy. J Thorac Cardiovasc Surg 1997;113:540-544.[Abstract/Free Full Text]
  7. Isono K., Sato H., Nakayama K. Results of a nationwide study on the three-field lymph node dissection of esophageal cancer. Oncology 1991;48:411-420.[Medline]
  8. Skinner D.B. Cervical lymph node dissection for thoracic esophageal cancer. Ann Thorac Surg 1991;51:884-885.[Medline]
  9. Earlam R., Cunha-Melo J.R. Oesophageal squamous cell carcinoma: I. A critical review of surgery. Br J Surg 1980;67:381-390.[Medline]
  10. Muller J.M., Erasmi H., Stelzner M., Zieren U., Pichlmaier H. Surgical therapy of oesophageal carcinoma. Br J Surg 1990;77:845-857.[Medline]
  11. Naunheim K.S., Honash J., Zwischenberger J., et al. Esophagectomy in the septuagenarian. Ann Thorac Surg 1993;56:880-884.[Abstract]
  12. Thomas P., Doddoli C., Neville P., et al. Esophageal cancer resection in the elderly. Eur J Cardiothorac Surg 1996;10:941-946.[Abstract]
  13. Jougon J.B., Ballester M., Duffy J., et al. Esophagectomy for cancer in the patient aged 70 years and older. Ann Thorac Surg 1997;63:1423-1427.[Abstract/Free Full Text]
  14. Poon R.T., Law S.Y.K., Chu K.M., Branicki F.J., Wong J. Esophagectomy for carcinoma of the esophagus in the elderly. Results of current surgical management. Ann Surg 1998;227:357-364.[Medline]
  15. Alexiou C., Beggs D., Salama F.D., Brackenbury E.T., Morgan W.E. Surgery for esophageal cancer in elderly patients: the view from Nottingham. J Thorac Cardiovasc Surg 1998;116:545-553.[Abstract/Free Full Text]
  16. Ellis F.H., Williamson W.A., Heatley G. Cancer of the esophagus and cardia: does age influence treatment selection and surgical outcomes?. J Am Coll Surg 1998;187:345-351.[Medline]
  17. Ginsberg R.J. Cancer treatment in the elderly. J Am Coll Surg 1998;227:427-428.
  18. Evers B.M., Townsend C.M., Jr, Thompson J.C. Organ physiology of age. Surg Clinic North Am 1994;74:23-39.



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