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Eur J Cardiothorac Surg 2006;29:824-828
© 2006 Elsevier Science NL

Lung cancer surgery: the first 60 days.

A population-based study

Hans Rostad a , * , Trond-Eirik Strand a , Anne Naalsund b , Olaug Talleraas a , Jarle Norstein a

a Cancer Registry of Norway, Montebello, Oslo, Norway
b Department of Respiratory Medicine, Rikshospitalet-Radiumhospitalet HF, Oslo, Norway

Received 6 October 2005; received in revised form 30 January 2006; accepted 31 January 2006.

* Corresponding author. Tel.: +47 22 45 13 04; fax: +47 22 45 13 70. (Email: hans.rostad{at}kreftregisteret.no).


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 
Objective: The postoperative mortality following lung cancer surgery is relatively high. The purpose of the present study was to identify preoperative risk factors as well as fatal complications in 27 Norwegian hospitals. Methods: In Norway, all clinical and pathologic departments submit reports on cancer patients to the Cancer Registry of Norway. The Registry also has a law-regulated authority to collect supplemental information regarding diagnosis, treatment, and outcome for all cancer patients from the hospitals in charge. This investigation included all patients who died within 30 and 60 days after resection of lung cancer in the period 1993–2002. Results: During the investigation lung cancer was diagnosed in 19,582 patients, 3224 (16.5%) were treated by surgery. The resection rate was almost similar in the two sexes, but postoperative mortality in women was less than half compared to men. Total mortality was 5% and 8% after 30 and 60 days, respectively. Bilobectomy and pneumonectomy were most risky with a mortality rate of about 10% within 60 days. In patients more than 70 years of age, there was a considerably higher frequency of pneumonectomy in men compared to women. Dominating causes of death were pneumonia with respiratory failure and cardiac events. Other identifiable causes were surgical hemorrhage and bronchopleural fistula. Conclusions: In this population-based, unselected series, the postoperative mortality was relatively high, and increased markedly in patients older than 70 years. Pneumonectomy in patients older than 70 years should only be performed when heart–lung function is found to be acceptable following full pulmonary function testing and thorough preoperative assessment of cardiovascular risk factors.

Key Words: Lung cancer surgery • Postoperative mortality


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 
In Norway, about 2000 new cases of lung cancer are diagnosed yearly and this tumor is also the most frequent cause of cancer deaths. Relative 5-year survival is 8–10%, 15–17% of the patients undergo resection. Surgery improves survival considerably [1–3].

However, several authors have reported morbidity and mortality after lung cancer surgery to be relatively high depending on the extent of the resection and the patients’ preoperative general health [4–6]. These reports, however, come from selected hospitals worldwide. Tobacco smoking leading to chronic obstructive pulmonary disease (COPD) causes reduced lung function, and this limits both the extent of surgery and in addition increases the risk of postoperative complications and death. Coronary heart disease also increases the risk of lung surgery [7].

This study was undertaken on a national basis to identify the preoperative risk factors as well as complications that caused postoperative death in all hospitals in Norway performing thoracic surgery.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 5. Conclusion
 References
 
The present investigation included all patients in Norway who died within 30 and 60 days after resection for lung cancer during 1993–2002. Notification of all forms of cancer in this country is mandatory without patient consent and regulated by law. All clinical and pathologic departments submit reports on cancer patients to the Cancer Registry. The Registry also has a law-regulated authority to collect supplemental information as needed regarding diagnosis, treatment, and outcome for all cancer patients from the hospitals in charge. Furthermore, the Registry receives death certificates from the Central Bureau of Statistics regarding all patients having cancer as the cause of death.

All clinical and pathological reports as well as supplemental information regarding patients who died postoperatively after resection of lung cancer were reviewed in order to identify preoperative risk factors, surgical procedures, and type of complications causing postoperative death.


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 5. Conclusion
 References
 
During the time period 1993–2002 lung cancer was diagnosed in 19,582 patients in Norway, 3224 (16.5%) underwent surgery with resection (Table 1 ). The rate was almost similar in the two sexes, but postoperative mortality rate in women was less than half compared to men both 31 and 61 days after surgery, the difference being highly significant (p < 0.001). Postoperative mortality was almost unchanged until 70 years, and then increased markedly after 70 years (Fig. 1 ).


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  		Table 1. Lung cancer in Norway 1993–2002
 

Figure 1
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  		Fig. 1. Age and postoperative mortality in patients operated on for lung cancer.

 
The highest postoperative mortality was registered in patients subjected to resection of the right lung in whom it was double that of the left, 6.4% versus 3.3%, respectively, a highly significant difference (Table 2 ).


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  		Table 2. Postoperative mortality related to tumor location in the lung and surgical procedure performed in 3224 resected patients
 
The 30-day mortality increased from 3.2% in patients whose tumors were classified as pathological stage Ia (pStage) to 10.3% in pStage IV. Of the latter seven patients, four had tumor in more than one lobe, two had solitary brain metastatic nodules and one was found to have metastases to the suprarenal gland.

The most frequent histologic tumor types were squamous cell carcinoma and adenocarcinoma. The latter occurred in 33% of men and 47% of women while the corresponding figures for squamous cell carcinoma were 44% and 23%, respectively.

Postoperative mortality after upper lobectomy was half that of lower lobectomy, 3.4% and 7.1%, respectively, within 60 days (p-value < 0.001). Bilobectomy and pneumonectomy were, not surprisingly, associated with a higher risk carrying a mortality rate of about 10%. In the older age groups there was a considerably higher frequency of pneumonectomies in men compared to women. In the age group 70–79 years pneumonectomy represented 25.0% of all procedures in men and 9.6% in women. This pneumonectomy ratio was even more pronounced in the age group 80–89 years, 15.0% in men and 4.3% in women. However, the numbers are small. Thus, the vast majority of postoperative deaths within 60 days after pneumonectomy were men. The high number of deaths after pneumonectomy in women less than 50 years is remarkable since none of them had preoperative risk factors influencing postoperative mortality (Fig. 2 ).


Figure 2
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  		Fig. 2. Postoperative mortality (<61 days) after pneumonectomy in men and women related to age.

 
The dominating cause of postoperative deaths was pneumonia complicated with respiratory failure (Table 3 ). Of the 84 patients who died within 60 days after surgery, 24 had preoperative risk factors for surgery. Cardiac events were the direct cause of 36 deaths, more than half of these had known coronary heart disease and/or valvular dysfunction. However, preoperatively, these patients were considered suitable for surgery, sometimes with limited resections.


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  		Table 3. Preoperative risk factors and causes of postoperative death after lung cancer surgery
 
Nine patients died from fatal intraoperative hemorrhage, the source of bleeding being the pulmonary artery in seven cases and the right atrium in two. In eight patients the hemorrhage could not be controlled, and death occurred on the table. One postoperative death was caused by the peroperative hemorrhage directly. Postoperative bleeding occurred in altogether 27 patients requiring reoperation in 23. In 13 cases the source of hemorrhage was the pulmonary artery or vein, in the remaining bleeding originated from intercostal arteries or smaller vessels. Autopsy in two patients who had not been reoperated revealed that the ligature of the main lung artery had slipped off. In eight more patients who died from other causes, the postoperative hemorrhage may have contributed to death.

Among 160 patients who died within 30 days of surgery, the tumor had not been resected completely in six of them and these patients died from their malignancy. In five patients this was confirmed by autopsy, demonstrating metastases, in one patient remaining tumor tissue was diagnosed clinically. Within 60 days after the operation, 15 more patients died of progressive cancer growth. Of the latter 15 patients, eight underwent autopsy, while seven were diagnosed clinically or with imaging, showing progressive disease like metastases or mediastinal infiltration.

Bronchopleural fistula (BPF) developed in 18 patients, 16 following right-sided pneumonectomy, and was the direct cause of death in all. All fistulas were preceded by infection days to weeks after the operation. In 14 cases the bronchus had been closed with staples. Fifteen had been reoperated.

Other causes of postoperative deaths were multi-organ failure, cerebral accident, pulmonary embolism, and cancer. Only 86 patients (39%) were autopsied. In this series all 3224 patients were operated in 27 hospitals. In 14 of these, less than 10 pulmonary resections were performed yearly. For hospitals with less than 10 procedures the 30-day mortality was 4.0% compared to 5.1% for hospitals with more procedures (p = 0.36). Of the 225 patients who died postoperatively, 135 were operated by a cardiothoracic surgeon, 90 by a general surgeon or a vascular surgeon, some being assisted by a specialist in cardiothoracic surgery.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
5. Conclusion
 References
 
The results of this demonstrate that lung cancer surgery is associated with a relatively high postoperative mortality rate. For Norway as a whole the mortality is somewhat higher than what has been quoted in other reports [4,8,9]. However, the difficult question may be posed: What risk should be accepted for surgery to be performed in order to cure a disease with near 100% mortality if left unresected? One potential cause of the high frequency of fatality is the fact that during the trial period thoracic surgery was performed in 27 different places in Norway. This has contributed to a decision of centralizing thoracic surgery to a smaller number of hospitals. It is our hope that this will also increase the resection rate of lung cancer in Norway.

During the investigation period the resection rate was comparable in the two sexes, while the postoperative mortality was less than half in women compared to men both 30 and 60 days after surgery. The main cause is probably the large number of pneumonectomies in elderly men while relatively few women in the same age group underwent such extensive resection. Women have more adenocarcinomas than men, 49% compared to 34% in the present series. These tumors are usually more peripherally located in the lung parenchyma than squamous cell carcinomas and can be removed by lobectomy, which is associated with less complications postoperatively. It may also be that women seem to develop COPD at an earlier age than men, rendering these patients medically inoperable due to reduced lung function. Finally, for some reason malignancy seems to be diagnosed earlier in women than men [10].

However, the high death rate in females <50 years is not quite clear. It may be reasonable to presume that females develop ischemic heart disease following a lower cumulative dosage of tobacco than what men do in the same manner as they develop lung cancer. One might suggest that coronary heart disease in females is underdiagnosed and untreated. For that reason they may not be adequately investigated preoperatively, as coronary heart disease is non-suspected in the clinical setting, resulting in an unsuspected high death rate postoperatively in this apparently low risk group of patients. In our series, as in others, the mortality after pneumonectomy in patients more than 80 years was very high [10–12]. Some authors therefore claim that such extensive surgery ought to be avoided in this age group [13,14], but in this matter opinion differs [8,15,16].

The reason why right-sided pneumonectomy is associated with a higher postoperative mortality than the same procedure performed on the left side is not clear [5]. Contributing factors may be the richer blood supply of the right lung, the larger volume which contributes more to the total bellow function and a shorter main bronchus. This implies more pronounced reduction in pulmonary function and a higher risk of bronchopleural fistula and postpneumonectomy pulmonary edema. In our series all fistulas after pneumonectomy causing death were on the right side. Finally, right pneumonectomy may lead to an increase in pulmonary artery pressure, and this could explain the higher rate of cardiac dysrhythmias [17]. Almost a similar argument may be used regarding the difference in mortality between upper and lower lobectomy: The lower lobe is larger than the upper one with richer blood supply and larger volume contributing more to the reduced bellow function.

The reason why a relatively high number of patients suffered cardio-respiratory deaths in our series is not clearly explicable. Certainly, many of them had recognized preoperative risk factors. The preoperative evaluation strategy, however, varied between the hospitals. Standardized exercise testing measuring maximal O2 uptake was only performed in a few places. Following lung function evaluation, patients with moderate COPD were considered operable, sometimes on the condition that only limited pulmonary resection was performed. Also, patients with coronary artery disease who had undergone surgical or percutaneous procedures, and had no cardiac complaint at the time of operation, were accepted for surgery without further investigation. May be more of these patients should have undergone preoperative coronary angiography.

The postoperative care and treatment may possibly have been inadequate because of limited capacity in the postoperative care units, which for many years has been a constant problem in Norwegian hospitals.

In principle, pulmonary physicians are responsible for diagnosis, investigation, classification, and preoperative evaluation of lung cancer patients. In Norway there has not been a common national strategy of this work. It is not known how each hospital selects patients for surgery, and in the actual period investigated TNM classification was inadequately performed [18].

Cardiac death is not uncommon after lung cancer surgery, especially following pneumonectomy [4,7,18,19]. In our series the exact number of cardiac fatalities is not clearly defined since some of the patients suspected to be within this category were not autopsied. A few were unexpectedly found dead in bed, and those known to have suffered from chronic heart disease preoperatively were coded as cardiac deaths. Due to limited capacity in the intensive care units they may have been transferred too early to the ward.

Fatal hemorrhages represented an important problem, both peri- and postoperatively. In many cases, this was caused by insufficient securing of large central arteries and veins. In some cases, hemorrhage was not considered to be the direct cause of death. It is, however, reasonable to believe that hypovolumia and hypotension during or after surgery may have been a contributing factor to death. The frequency of surgical hemorrhage was almost identical in the various hospitals although some had a relatively high number in few procedures.

Preceding postoperative infection seemed to be the main cause of developing BPF in a relatively high number of patients. Whether BPFs are a result of infection or whether an insufficient bronchial closure predisposes for infection of the thoracic cavity remains to be seen. Nevertheless, a low threshold for performing bronchoscopy in newly operated patients with signs and symptoms of infection is important. In accordance with previous reports on this matter, almost all occurred after right-sided pneumonectomy [5,19–21]. Reoperation and secondary closure of the bronchus are rarely successful unless being performed shortly after resection and before infection has developed.

It is notifiable that 21 of the 225 patients who died within 60 days after surgery, died due to rapidly progressive malignant disease, locally or by metastases. Postoperative complications were not identified as a cause of death in these patients. In hindsight, it may be argued that if advanced disease had been demonstrated preoperatively, the patients should have been spared the trauma of operation. However, given the aggressive nature of some lung tumors, even sophisticated preoperative imaging may have been unable to identify mediastinal infiltration or distant metastases. If preoperative investigation did not demonstrate spread beyond the lung, the patient should be offered an operation, since the alternative of no operation is associated with a poor prognosis.

In nearly half of the 27 hospitals less than 10 surgical procedures were performed yearly so that the competence regarding the preoperative evaluation, surgical skill, and postoperative handling of the patients may be questioned. In spite of that no significant difference in postoperative mortality between hospitals performing more or less than 10 procedures could be found. This may be a result of patients’ selection. Patients with risk factors before thoracic surgery may have been referred to larger hospitals with higher competence.

Cardiothoracic surgeons seem to achieve better results than general surgeons [22], and large patient volumes have been claimed to influence survival favorably [23,24].


   5. Conclusion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
References
 
Compared to the standard set by the British Thoracic Society and Society of Cardiothoracic Surgeons of Great Britain and Ireland Working Party in their consensus document of 2001, the postoperative mortality in the present series is too high within 30 days after surgery [25].

Most conspicuous were the high number of surgical hemorrhages. Fatal complications were otherwise dominated by pneumonia with respiratory failure and cardiac events.

Postoperative mortality rate increased markedly in patients more than 70 years. Pneumonectomy in patients more than 70 years should only be performed when heart–lung function is acceptable as judged from advanced exercise testing. Preoperative assessment of cardiovascular risk factors must be performed.

The effect on the mortality rates of a common investigational strategy and centralization of operations to a limited number of hospitals remains to be seen.


   Footnotes
 
{star} The result of this work was presented orally at the 11th World Conference on Lung Cancer in Barcelona, Spain, July 3–6, 2005.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
 References
 

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