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(Chest. 2003;123:813-821.)
© 2003 American College of Chest Physicians

Logistic Regression Analysis of Potential Prognostic Factors for Pulmonary Thromboembolism*

Hugo Hyung Bok Yoo, MD; Sérgio Alberto Rupp de Paiva, MD; Liciana Vaz de Arruda Silveira, PhD and Thais Thomaz Queluz, MD

* From the Department of Internal Medicine (Drs. Yoo, de Paiva, and Queluz), Botucatu Medical School; and Department of Biostatistics (Dr. Silveira), Institute of Biosciences of Botucatu, Universidade Estadual Paulista–UNESP, Botucatu, State of São Paulo, Brazil.

Correspondence to: Thais Thomaz Queluz, MD, Department of Internal Medicine, Botucatu Medical School–UNESP, Botucatu, SP 18618–000 Brazil; e-mail: queluz{at}terra.com.br


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objective: To identify potential prognostic factors for pulmonary thromboembolism (PTE), establishing a mathematical model to predict the risk for fatal PTE and nonfatal PTE.

Method: The reports on 4,813 consecutive autopsies performed from 1979 to 1998 in a Brazilian tertiary referral medical school were reviewed for a retrospective study. From the medical records and autopsy reports of the 512 patients found with macroscopically and/or microscopically documented PTE, data on demographics, underlying diseases, and probable PTE site of origin were gathered and studied by multiple logistic regression. Thereafter, the "jackknife" method, a statistical cross-validation technique that uses the original study patients to validate a clinical prediction rule, was performed.

Results: The autopsy rate was 50.2%, and PTE prevalence was 10.6%. In 212 cases, PTE was the main cause of death (fatal PTE). The independent variables selected by the regression significance criteria that were more likely to be associated with fatal PTE were age (odds ratio [OR], 1.02; 95% confidence interval [CI], 1.00 to 1.03), trauma (OR, 8.5; 95% CI, 2.20 to 32.81), right-sided cardiac thrombi (OR, 1.96; 95% CI, 1.02 to 3.77), pelvic vein thrombi (OR, 3.46; 95% CI, 1.19 to 10.05); those most likely to be associated with nonfatal PTE were systemic arterial hypertension (OR, 0.51; 95% CI, 0.33 to 0.80), pneumonia (OR, 0.46; 95% CI, 0.30 to 0.71), and sepsis (OR, 0.16; 95% CI, 0.06 to 0.40). The results obtained from the application of the equation in the 512 cases studied using logistic regression analysis suggest the range in which logit p > 0.336 favors the occurrence of fatal PTE, logit p < - 1.142 favors nonfatal PTE, and logit P with intermediate values is not conclusive. The cross-validation prediction misclassification rate was 25.6%, meaning that the prediction equation correctly classified the majority of the cases (74.4%).

Conclusions: Although the usefulness of this method in everyday medical practice needs to be confirmed by a prospective study, for the time being our results suggest that concerning prevention, diagnosis, and treatment of PTE, strict attention should be given to those patients presenting the variables that are significant in the logistic regression model.

Key Words: autopsy • epidemiology • prognostic factors • pulmonary thromboembolism


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Although pulmonary thromboembolism (PTE) is associated with high morbidity and mortality rates all over the world, its epidemiology remains unclear. The acute and recurrent nature of the disease, its variable and nonspecific clinical picture, and the difficulty in establishing an accurate diagnosis, even when sophisticated laboratory techniques are used, keep its real incidence unknown and make it difficult to determine if it is the main cause of death or just a comorbidity or even an incidental finding.1 2 3 4

The most accurate information about incidence, origin of the thrombi, probable causes of thrombosis, and significance of PTE is provided by studies of unselected autopsies performed in general hospitals using rigid and systematic techniques.5 6 7 Even though PTE risk factors are widely known,4 5 8 9 the factors that influence the development of acute episodes of the disease remain unclear. Therefore, the purpose of the present work was to identify, in a series of autopsies carried out in a tertiary general medical school (São Paulo, Brazil), the potential PTE prognostic factors by developing a mathematical model to predict the risk for fatal and nonfatal PTE.


   Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Setting
This study was carried out in the Clinical Hospital, Botucatu Medical School, a tertiary referral medical school located in the state of São Paulo, southeastern Brazil, that provides care exclusively to the patients of the Single National Health System. The hospital is well equipped and currently has 500 beds. Autopsies are routinely requested and performed as long as consent of the families can be obtained. Forensic autopsies are referred to another department.

Outline
All the records of the consecutive autopsies performed in our hospital from 1979 to 1998 were reviewed. From the medical records and autopsy reports of all the patients with macroscopically and/or microscopically documented PTE, the following data were gathered: (1) demographic (sex, age, and race), (2) clinical (underlying diseases), and (3) localization of thrombosis (emboli located in the lungs and probable PTE site of origin). These data were collected by two experienced pulmonologists who considered as basic all the diseases confirmed by clinical, pathologic, and/or laboratory documentation. Cases of amniotic, septic, and fat emboli were excluded.

PTE was classified as fatal when no other causes of death were found at autopsy, emboli occluded at least two lobar arteries or several small-caliber arteries were occluded, and the extent of such occlusion corresponded to that of two lobar arteries. PTE was classified as nonfatal when death was caused by another disease and the extent of thrombotic occlusion did not exceed that of two lobar arteries.6 10 The study protocol was approved by the Committee of Ethics in Human Research of the Botucatu Medical School.

Autopsy Routine
Autopsies were jointly performed by medical professors and residents of the Department of Pathology, following a well-established, sequential, and systematic procedure. The autopsy routine includes analysis of the topography and in loco alterations followed by dissection, as well as macroscopic and microscopic analyses of the organs.

For examination of the thoracic organs (lungs, heart, and mediastinal structures), the heart is exposed through the pericardial sac and the base vessels are analyzed. The pulmonary artery trunk and both left and right pulmonary branches are dissected to the point where they enter the lungs. The lungs are detached from the heart while the lobes are kept united by the trachea. The lungs are then injected, via the trachea, with 10% formalin and embedded in formaldehyde for fixation. The heart is exposed and, after the cardiac chambers are examined, also embedded in formaldehyde. The initial segments of the jugular and subclavian veins are examined and, if an edema and/or an erythema is found in either or both upper limbs, these veins are further examined. Subsequently, the abdominal organs are dissected for examination of the pelvic veins (iliac, peri-uterine and periprostatic plexus). The upper and lower tendons are cut and the calf muscles (gastrocnemius and soleus) dissected out from the tibia and fibula. The whole muscle block is then transversally cut into 10-cm sections for analysis of the deep veins. Following examination of their external surface, the fixed lungs are transversally sectioned at the lateromedial plane at the level of the main bronchi of each lobe. Then, new sections are cut parallel to the previous ones, also at the level of the main bronchi. Thus, 10 cm apart from each other but united by the bronchi and trachea, the lungs with their anterior and posterior surfaces are kept for analysis. The anterior and posterior segments of each pulmonary lobe remain available for sectioning. The specimens are then analyzed. Every macroscopic diagnosis of pulmonary infarction is confirmed by microscopic examination of the lesions. Suitable fragments are removed, processed in paraffin, and histopathologically examined.

Statistical Analysis
Dependent variables (fatal PTE and nonfatal PTE) were compared by the {chi}2 method. Mean ages were compared by the Student t test, and the Mann-Whitney method was used to compare the logit medians of the groups studied (fatal PTE and nonfatal PTE). Statistical significance was set at p < 0.05.11

Independent variables (age, sex, race, underlying diseases, and PTE site of origin) and the dicotomic dependent variable (fatal PTE and nonfatal PTE) were compared by logistic regression analysis. Furthermore, multiple logistic regression analysis was used to create a model to predict the risk for fatal and nonfatal PTE utilizing the independent variable studied.11 The logistic regression analysis was performed with a commercial package (SigmaStat for Windows, v2.03; SPSS; Chicago, IL).

In order to validate the prediction rule, the "jackknife" method was performed and the results were presented as misclassification defined as the fraction of patients who were incorrectly classified. The jackknife method is a statistical cross-validation technique that can be employed when it is necessary to use the original study patients to validate a clinical prediction rule.12 In this method, sometimes called the "one-left-out" method, one patient is removed and the rule is rederived and used to classify the excluded patient. The patient's predicted state is compared with the true state. This process is repeated many times to determine the frequency with which the excluded patient is misclassified.12 Therefore, in this study, among 512 patients, 1 patient was selected to be excluded. A rule was derived from the remaining 511 patients and applied to the 512th patient. This process was repeated systematically for all 512 patients. The misclassification rate is the fraction of the 512 test patients who were incorrectly classified.


   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Prevalence and Demographics
Of the 9,591 patients who died at the Clinical Hospital-Botucatu Medical School between 1979 and 1998, autopsies were performed on 4,813 patients (50.2%). Total and relative PTE prevalence over the 20 years covered by this study as well as that observed at 5-year intervals (1979–1983, 1984–1988, 1989–1993, 1994–1998) are shown in Table 1 . The patients, 301 males (59%) and 211 females (41%), 417 whites (81.4%), 91 blacks (17.8%), and 4 Asians (0.8%), had a mean (± SD) age of 54.1 ± 18.9 years (range, 1 to 102 years). The ratio of white, black, and Asian patients reflects the general population demographics in the area served by the hospital.


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  		Table 1.. Number of Deaths, Autopsies Performed, PTEs, Fatal PTEs, and Nonfatal PTEs at 5-Year Intervals

 
Male patients had a mean age of 54.4 ± 18.5 years (range, 1 to 87 years), and female patients had a mean age of 53.5 ± 19.6 years (range, 1 to 102 years) [p = not significant]. Mean age of the patients with fatal PTE was 56.8 ± 17.7 years (range, 1 to 102 years) and 52.1 ± 19.6 years (range, 1 to 87 years) among the patients with nonfatal PTE (p = 0.006).

Clinical Data
Generally, the patients displayed more than one underlying disease. On average, they presented three underlying diseases, with a range of one to seven diseases. The frequency of the main underlying disease groups associated with PTE as well as the frequency of fatal and nonfatal PTE are shown in Table 2 .


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  		Table 2.. Frequency of the Main Underlying Disease Groups Associated With PTE

 
Localization of Thrombosis
The segmental and/or subsegmental pulmonary arteries were affected in 383 cases (74.8%), main pulmonary arteries in 70 cases (13.7%), the pulmonary artery trunk in 13 cases (2.5%), and "saddle" thrombi were found in 5 cases (1%). In 46 cases (9%), isolated pulmonary infarctions, ie, without the presence of thrombi in the corresponding vessels, were found. The probable PTE sites of origin were determined in 68% of the cases and are shown in Table 3 . No significant correlation was observed between the relative frequency rates of the disease groups studied and the probable PTE origin. PTE with pulmonary infarction areas occurred in 253 cases (49.4%) from which 101 cases (47.6%) and 152 cases (50.6%) were correlated with fatal and nonfatal PTE, respectively (p > 0.05).


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  		Table 3.. Probable Sites of Origin of the Thromboembolus

 
Multiple Logistic Regression Analysis
In order to determine the behavior of each variable in relation to PTE type, p value and a confidence interval (CI) of 95% of the odds ratio (OR) were used. As the variables age, sex, and race were stratified and adjusted to intrinsic individual variables, they could be present in all the analyses performed.

Logistic regression analysis revealed that the variables regarding age, diseases of the circulatory system, infectious diseases, trauma, right-sided cardiac thrombi, and pelvic vein thrombi were statistically significant (p < 0.05) and the 95% CI does not include 1 (Table 4 ). As these statistically significant variables were selected and analyzed together, the same significant behavior was observed (Table 5 ).


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  		Table 4.. Logistic Regression Analysis: Independent Variables (Demographics, Groups of Diseases, Thromboembolism Origin) x Dependent Variable

 

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  		Table 5.. Logistic Regression Analysis: Independent Variables Statistically Significant at the First Analysis x Dependent Variable

 
In order to be evaluated more closely, the variables regarding circulatory and infectious diseases were further detailed so that a new analysis of the association among diseases could be performed. The data in Table 6 show that systemic arterial hypertension, sepsis, pneumonia, and the other statistically significant variables shown in Tables 4 , 5 presented the same significant behavior.


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  		Table 6.. Logistic Regression Analysis: Independent Variables x Dependent Variables

 
Logistic Regression Model
Final regression analysis of the selected variables showed that they remained statistically significant (Fig 1 ), allowing the elaboration of a regression equation to predict the occurrence of fatal and nonfatal PTE. The equation may be applied using the variables selected according to the regression significance criteria:












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  		Figure 1.. Logistic regression analysis: independent variables x dependent variables; significance at p < 0.05. SAH = systemic arterial hypertension; Pelvic v = pelvic veins; R. Chambers = right-sided cardiac chambers.

 
The equation was employed in all the cases (n = 512), and the results are plotted in Figure 2 . Descriptive analysis revealed that the fatal PTE median was - 0.517; nonfatal PTE median, - 0.023 (p < 0.001); fatal PTE 75th percentile, 0.336; and nonfatal PTE 25th percentile, - 1.142.



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  		Figure 2.. Logistic regression analysis: independent variables x dependent variables. Plotting of the logit equation results for the 512 patients. *Comparison between fatal PTE and nonfatal PTE medians by the Mann-Whitney test (p < 0.001). The upper and lower lines of the box represent the 75th percentile and the 25th percentile values, respectively. The line inside represents the median; the upper and lower limits of the bars represent the 95th percentile and fifth percentile values, respectively.

 
Crossvalidation of the Prediction Rule
The jackknife method showed a misclassification rate of 25.6%. This result means that the prediction equation correctly classified 74.4% of the patients.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Our results show PTE was prevalent in 10.6% of the cases. In a similar study carried out in the same hospital between 1969 and 1976, PTE prevalence was 16.6%.13 As in other centers,6 7 10 14 15 16 PTE prevalence is declining in our hospital. Even though a decline in autopsy rates has also been observed, a worldwide phenomenon,17 the reduction in PTE prevalence seems to be related to improvements in prevention, development of diagnostic resources, and therapeutic advances rather than the decreasing number of autopsies.

It is noteworthy that over the 20-year period of study, there was a 10-fold increase of the population served by our hospital (data not shown), a fact that probably contributed to an increase in hospital deaths observed in our results. Despite this, our autopsy rate is declining, yet remains elevated when compared to those of the literature. Our overall autopsy rate was 50.2% and, even in the most recent 5-year interval (1994–1998), the autopsy rate (27.7%) was higher than those reported by others, 14.0 to 21.0%.18 19 20

As the results of autopsy studies depend on autopsy rates, the number of cases, type of hospital, interest and patience on the part of the pathologist while searching for thrombi, and preparing the material to be analyzed,5 6 we consider our data adequate for the present study because they are derived from a large series of unselected autopsies performed in a large general hospital and, most of all, because a technique that systematically searches for thrombi was used in all autopsies. Moreover, since the study setting is a medical school, medical records are reliable as they are collected by students and residents under the supervision of faculty members. Therefore, in our series, it was possible to determine comorbidities, classify PTE as fatal or nonfatal according to the criteria previously established and, in 68% of the cases, determine the probable origin of PTE.

The frequencies of fatal and nonfatal PTE were 4.4% and 6.2%, respectively, which are different from those reported by other authors who also differ from each other.7 10 16 20 21 Such a discrepancy seems to be due to the differences observed among the cases and autopsy techniques and, especially, to the different concepts of fatal and nonfatal PTE used. Fatal PTE has been defined as massive PTE in the absence of another disease that could cause death22 or as the occlusion of at least two lobar arteries in the absence of another death cause.23 In the present study, the definition of fatal PTE also included occlusions of small branches of the pulmonary artery as long as their extent corresponded to that of the occlusion of two lobar arteries. However, a shortcoming of our study and of other similar investigations is the possibility of small but fatal embolisms in patients with deteriorated cardiopulmonary conditions.24

In the present work, the finding of pulmonary hemorrhagic infarctions without thrombi was construed as evidence of PTE because the thrombi responsible for infarctions may undergo endogenous or therapy-derived lysis. Similarly, the 32% of cases in which the origin of PTE could not be determined might, at least partially, be the result of total disconnection of the thrombus from its origin, its physiologic disintegration, or a consequence of thrombolitic therapy or postmortem.16 25 This assumption is corroborated by the significantly higher frequency of these cases in nonfatal PTE (p < 0.001).

It is noteworthy that multiple logistic regression analysis identified a demographic parameter (age), a comorbidity (trauma), and two PTE sources (right-sided cardiac chambers and pelvic veins) as variables that favor the occurrence of fatal PTE. The discriminatory power of our results is especially reinforced by the fact that these variables have been extensively described in the literature as causes of death in PTE.

Both PTE morbidity and mortality exponentially rise with age, probably due to the concomitant increase in the number of risk factors.4 18 26 Among our cases, the mean age of patients with fatal PTE was significantly higher than that of the nonfatal PTE patients (p = 0.006). The incidence of PTE among trauma patients, which was elevated in the past, has been reported to be 2.3% and is frequently related with fatal events especially in patients > 55 years of age, with pelvic traumas and multiple traumas.27 These data may suggest the presence of thrombi in the pelvic veins, one of the major sources of fatal PTE because these thrombi are generally of a large size.26 Besides trauma and pelvic surgeries, thrombi in the pelvic veins may stem from untreated distal venous thrombosis.28 29

Similarly, cardiac thrombi are related to fatal PTE because they are generally large. They usually occur in patients with atrial and/or right-sided ventricular abnormalities, or may originate from peripheral veins or even adhere, transitorily or permanently, to the heart walls. They are generally elongated, thin, and mobile, which favors the occurrence of fatal PTE.9 30 31 32 When secondary to catheterization of the central vein, they are less mobile and therefore present a lesser probability of embolization.

As for the variables that favor nonfatal PTE (systemic arterial hypertension, pneumonia, and sepsis), systematic hypertension has not been described as a risk factor for venous thromboembolism; although the relationship between infection and PTE has not yet been well established, venous thromboembolism is a frequent complication of septicemia, especially when it is caused by Gram-negative bacteria and is associated with a hypercoagulable state and IV coagulation. PTE has been frequently observed in patients with sepsis who undergo central venous catheterization.33

The plotting and analysis of the mathematical model elaborated for the 512 patients of this study suggest a range that can be used to predict the risk of fatal and nonfatal PTE. Using the 75th percentile values (0.336) of the fatal PTE patients and the 25th percentile values (- 1.142) of the nonfatal PTE patients (Fig 2) , we established that when the result of the equation is > 0.336, the occurrence of fatal PTE is favored; when it is < - 1.142, it favors the occurrence of nonfatal PTE. The intermediate values are not conclusive.

The cross-validation of our results showed that the prediction equation correctly classified 74.4% of the patients, ie, it is able to predict fatal or nonfatal PTE in three fourths of the cases. Therefore, based on this equation, the majority of the cases are correctly classified and 25.6% are misclassified. Since the best way to test a prediction rule is to measure the misclassification rate in a new clinical setting,12 the usefulness of this method in everyday medical practice needs to be confirmed by a prospective study. For the time being, our results suggest that, concerning prevention, diagnosis, and treatment of PTE, strict attention should be given to patients presenting the variables that are significant in the logistic regression model.

Finally, our findings support those of other authors who have shown the importance of using Doppler echocardiography34 35 36 37 to investigate cardiac thrombi PTE and MRI to investigate thrombi in the pelvic veins.38 39 40


   Acknowledgements
 
The authors thank the medical professors and residents of the Department of Pathology, Botucatu Medical School, who performed the autopsies over the years of the study.


   Footnotes
 
Abbreviations: CI = confidence interval; OR = odds ratio; PTE = pulmonary thromboembolism

Received for publication April 2, 2002. Accepted for publication September 17, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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