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This study aimed to investigate whether the dorsal skeletal muscle area at 12th thoracic level (T12SMA) could be used as a predictor of in-hospital mortality and long-term survival among patients with community-acquired pneumonia (CAP).
Materials and Methods
A retrospective study was conducted on 1701 CAP patients who underwent chest computed tomography (CT) examinations at the First Hospital of Qinhuangdao. The primary outcome was in-hospital mortality. The T12SMA was analyzed. Multivariate regression logistic models were constructed to identify the prognostic markers of hospital mortality. Cox regression logistic models were constructed to identify the risk factors of long-term survival.
The multiple logistic regression analysis showed that T12SMA [odds ratio (OR) = 0.946; p = 0.007], CURB-65 (OR = 1.521; p = 0.008), creatinine (OR = 1.003; p = 0.001), albumin (OR = 0.908; p = 0.001) and intensive care unit (ICU) (OR = 2.715; p = 0.007) were independent risk factors for predicting the in-hospital mortality. The cox regression logistic analysis showed that T12SMA (OR = 0.968; p = 0.000), age (OR= 1.036; p = 0.000), sex (OR= 1.435; p = 0.002), CURB-65 (OR = 1.311; p = 0.000), albumin (OR = 0.952; p = 0.000), creatinine (OR = 1.002; p = 0.000) and ICU (OR = 1.606; p = 0.001) were prognostic markers of long-term survival.
T12SMA, CURB-65, creatinine, albumin and ICU were independent risk factors for in-hospital mortality among patients with CAP. And low T12SMA affected the in-hospital mortality and long-term survival of patients with CAP.
). CAP patients may have different outcomes varying from rapid recovery to death. Therefore, it is crucial to evaluate the severity of CAP before starting treatment. Commonly, CURB-65 is used to evaluate the severity of CAP, which has been recommended by several CAP guidelines (
). The EWGSOP recommends the area measurement on a single cross-section computed tomography (CT) image at the level of the third lumbar (L3) vertebra as an alternative tool, since this area accurately represents the whole-body muscle. Thus, this method may serve as an alternative tool for assessing muscle quantity. A study showed that sarcopenia, which was defined by L3 skeletal muscle area (SMA) using a single transverse CT slice, was highly prevalent among patients with respiratory failure requiring mechanical ventilation (
). However, abdominal CT is not a routine examination for patients with CAP. Chest CT scanning is a conventional assessment for patients with CAP. The examination of the twelfth thoracic (T12) vertebra on CT images may serve as an alternative strategy when L3 is unavailable (
). Moreover, the decline in paravertebral muscle size and attenuation at T12 on CT images had been reported to be associated with in-hospital mortality and long-term survival in elderly patients undergoing chronic obstructive pulmonary disease (COPD) (
). The relationship between the dorsal skeletal muscle area at T12 vertebral level (T12SMA) and the mortality of CAP remains unclear.
This study retrospectively investigated clinical parameters, including T12SMA, dorsal skeletal muscle density at T12 vertebral level (T12SMD), and other risk factors, to evaluate whether these parameters might serve as prognostic markers for in-hospital mortality with CAP. It also explored whether the level of T12SMA at admission might be a predictor of long-term survival among patients with CAP.
METHOD AND MATERIALS
This study was approved by the ethics committee of the First Hospital of Qinhuangdao.
Population Cohort and Design
This retrospective study included patients hospitalized due to CAP at the First Hospital of Qinhuangdao between January 2015 and December 2018. The inclusion criteria were the following: 1) all patients were diagnosed with CAP, 2) patients over 18 years of age. The exclusion criteria were: 1) no adequate imaging within 7days after admission; 2) clinical data about CURB-65 missing; 3) clinical data about albumin, glucose, creatinine and body mass index(BMI) missing. They were divided into two groups based on their survival when discharged from the hospital. All enrolled patients were followed up until October 31, 2020.
Definition of CAP
The definition of CAP was done according to the 2016 CAP clinical practice guidelines by the Chinese Thoracic Society (
Initial data after admission were extracted from the Hospital Information System. Demographic variables included age and sex. Physical examination included mental status, respiratory rate, blood pressure, temperature, pulse, height and weight. Laboratory data included urea, glucose, albumin, creatinine and C-reactive protein (CRP). The scores of CURB-65 [confusion, urea>7mmol/L, respiratory rate≥30/min, blood pressure (systolic blood pressure<90mmHg or diastolic blood pressure≤60 mmHg) and age ≥65 years] was calculated (
Patients underwent plain CT using a 64-row multidetector CT (GE Healthcare, Milwaukee, WI, USA) with 1-mm slice thickness in the supine position at admission or within 7days after admission. The electronically stored CT images were collected from Picture Archiving and Communication Systems (PACS, IMPAX220.127.116.1195, AGFA HealthCare NV, Belgium). T12SMA was defined as any muscle within the region posterior to the T12 spine and ribs and no more lateral than the lateral-most edges of the erector spinal muscles (Fig 1). The skeletal muscle boundaries were segmented manually. The cross-sectional muscle area and radiodensity were semi-automated thresholding using Slice-O-matic software, version 4.3 (Tomovision, Montreal, QC, Canada). Skeletal muscle was identified and quantified by use of Hounsfield unit (HU) thresholds (–29 to +150) (
). All imaging analyses were conducted in the cross-sectional area at the level of T12 vertebral. T12SMA was recorded as the sum of bilateral dorsal SMA, while T12SMD was recorded as the mean of bilateral dorsal muscle group radiodensity (Fig 1). Muscle segmentations were performed by an experienced operator, with an audit of all images and segmentations by a musculoskeletal radiologist.
Statistical analyses were performed using SPSS 23.0 (IBM, NY, USA). All demographic and clinical characteristics were described between the two groups based on the status at discharge (surviving or deceased) and compared using chi-square test or Student's t-test. Multivariate regression logistic models were constructed to identify the prognostic markers of hospital mortality. The selected variables were subjected to forward conditional stepwise regression. p<0.05 was considered to be statistically significant.
To emphasize the prognostic role of T12SMA in hospital mortality, the receiver operating characteristic (ROC) curve was used to analyze the accuracy, sensitivity, specificity, and area under the ROC. The Youden index was obtained by the ROC analysis, and the maximum tangent point was selected to establish the cutoff value. Cox regression logistic models were constructed to identify the prognostic markers of long-term survival. p<0.05 was considered to be statistically significant.
A total of 2808 CAP patients were analyzed. One thousand one hundred and seven patients were additionally excluded due to missing clinical data. Eventually, this study enrolled 1701(61%) patients (995 males and 706 females), aged 65.39±17.17 years (Table 1). Of the 1701 patients, 70 died at discharge. The demographic and clinical characteristics and details of patient samples in the two groups are shown in (Table 1). In the univariate analyses, the variables, such as age (65.39±17.17, p = 0.000), BMI (23.47±4.25, p = 0.000), CURB-65(1.11±0.99, p = 0.000), glucose (7.54±3.96, p = 0.000), albumin (35.47±5.55, p = 0.000), creatinine (86.42±92.53) and CRP (53.23±64.24, p = 0.003) had significant differences between the groups. T12SMA was lower in the deceased group (26.65±8.96) than in the surviving group (34.67±10.51, p = 0.005). Further, 246 patients (14.5%) were admitted to the intensive care unit (ICU) during hospitalization, and the frequency of ICU had significant differences between the groups (p = 0.000).
Table 1Clinical Characteristics of Patients in the Two Groups
All Patients (n = 1701)
Surviving (n = 1631)
Deceased (n = 70)
t or χ2
Abbreviations: BMI, body mass index; SBP, systolic blood pressure; DBP, diastolic blood pressure; T12SMA, dorsal skeletal muscle area at the T12 vertebral level; T12SMD, dorsal skeletal muscle density at the T12 vertebral level; ICU, intensive care unit; CRP, C-reactive protein. p <0.05 was considered statistically significant.
Multivariate analyses were performed using the significant risk factors determined in the univariate analysis. As shown in (Table 2, multiple logistic regression analysis showed that T12SMA [odds ratio (OR) = 0.946; 95% confidence interval (CI), 0.909 – 0.985, p = 0.007], CURB-65 (OR = 1.521; 95% CI, 1.115 – 2.076, p = 0.008), creatinine (OR = 1.003; 95% CI, 1.001 – 1.005, p = 0.001), albumin (OR = 0.908; 95% CI, 0.857 – 0.964, p = 0.001) and ICU (OR=2.715; 95% CI, 1.314 – 5.608, p = 0.007) were independent risk predictors for the in-hospital mortality.
Table 2Logistic Regression Analysis of the Risk Factors for in-Hospital Mortality
Multiple logistic regression analysis, in-hospital mortality was considered as the dependent variables in a multiple logistic regression analysis with sex, age, BMI, CURB-65, T12SMA, T12SMD, creatinine, albumin, glucose, ICU and CRP as independent variables. Abbreviations: T12SMA, dorsal skeletal muscle area at the T12 vertebral level; ICU, intensive care unit.
The area under the ROC curve (AUC) for the prognostic role of T12SMA in hospital mortality was 0.728 (p = 0.000). The optimal cutoff value of T12SMA to predict survival was 30.67 cm2 (Fig 2).
As shown in (Table 3), the variables in the cox regression logistic models were T12SMA (OR = 0.968; 95% CI, 0.955 – 0.982, p = 0.000), age(OR = 1.036; 95% CI, 1.025 – 1.046, p = 0.000), sex(OR = 1.435; 95% CI, 1.137 – 1.810, p = 0.002), CURB-65 (OR = 1.311; 95% CI, 1.154 – 1.489, p = 0.000), albumin (OR = 0.952; 95% CI, 0.933 – 0.972, p = 0.000), creatinine (OR = 1.002; 95% CI, 1.001 – 1.002, p = 0.000) and ICU(OR = 1.606; 95% CI, 1.223 – 2.108, p = 0.001). They were independent risk factors for predicting the long-term survival.
Table 3Cox Regression Analysis of the Risk Factors for Long-Term Survival
Cox regression analysis, long-term survival was considered as the dependent variables in a cox regression analysis with age, sex, BMI, CURB-65, T12SMA, T12SMD, creatinine, albumin, glucose and ICU as independent variables. Abbreviations: T12SMA, dorsal skeletal muscle area at the T12 vertebral level; ICU, intensive care unit.
GBD 2017 Disease and Injury Incidence and Prevalence Collaborators Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017.
). In this study, we showed that T12SMA, CURB-65, creatinine, albumin and ICU were independent risk factors for in-hospital mortality among patients with CAP. Low T12SMA affected the in-hospital mortality and long-term survival of patients with CAP. As a surrogate of L3 SMA, T12SMA was used to measure the skeletal muscle mass of patients with CAP in this study. As reported, the low skeletal muscle mass prognosticated high mortality in the acute episode and long-term survival chronic rehabilitation stage with different lung diseases that included COPD, cancer and COVID-19 pneumonia (
). Muscle mass may affect the occurrence of pneumonia through different mechanisms. Weakened muscle strengths and low body muscle mass were risk factors for the onset of pneumonia, which suggested malnutrition (
). Similar to the above study, we found that T12SMA was associated with the inflammation biomarker CRP (supplementary Table). Therefore, the level of skeletal muscle mass reflected the degree of inflammatory response. In addition, inflammation caused the production of pro-inflammatory cytokines and induced muscle weakness (
). Pro-inflammatory cytokines induced muscle proteolysis by a twostep process, consisting of myofibrillar protein cleavage by calpains and/or caspase-3, followed by further degradation by the ubiquitin-proteasome system (
). What's more, paravertebral muscle is a major muscle of respiration along with the diaphragm and intercostal muscles. Low T12SMA suggested a loss of respiratory muscle mass, which was a risk factor for the onset of pneumonia (
). Our findings suggest that the quantitative assessment of the paravertebral muscle on CT may aid risk assessment in patients with CAP.
Sarcopenia was defined as the progressive decline of skeletal muscle area, strength and function. Generally bioelectrical impedance analysis (BIA) and dual-energy X-ray absorption (DXA) have been used to measure the muscle mass and grip strength devices and a gait speed test have been used to measure function (
). This suggests that skeletal muscle size may be more sensitive than BMI as a measure of wasting and weakness. Also, tests such as stair-climbing or the 6-min walk test require additional patient effort and cooperation (
) while muscle quantification relies on already available objective data, given that CT scans of the thorax are commonly obtained in patients with CAP.
Further, CURB-65 is a classical tool for evaluating the severity of CAP. A previous meta-analysis showed that the AUC area under the curve (AUC) of CURB-65 was about 0.8 for predicting 30-day mortality in hospitalized CAP patients (
). Similarly, our study showed that CURB-65 was significantly elevated in the deceased group and was an independent risk factor for predicting the in-hospital mortality. Albumin is a protein made by the liver that plays many important roles. Numerous studies confirmed that serum albumin correlated with short-term and long-term mortality of CAP (
). In line with previous studies, albumin level was also an independent predictor of in-hospital mortality and long-term survival of CAP in our study.
This study had several limitations. First, this was a single-center retrospective study. A certain number of patients were eliminated due to unavailable imaging or clinical data elements, resulted in a 39% exclusion rate. Especially very critically ill patients who could not undergo CT often had a bad outcome rapidly. Thus, larger studies with data from other hospitals or regions are required to assess the role of the paravertebral muscle mass in CAP risk prediction. Second, confounding factors, such as arterial blood gas analysis, pathogens of infection were not evaluated in our study. Finally, muscle is just one body composition metric that can be derived from CT examinations. Future studies could explore the role of fat, edema and bone density in this context. Prospective data collection would also allow the inclusion of important factors such as respiratory function measurement and exercise testing.
The T12SMA was an independent predictive factor for in-hospital mortality and long-term survival in adult patients with CAP. Skeletal muscle mass loss was a crucial problem in CAP and hence should not be neglected. This study presented an alternative method for measuring the skeletal muscle mass when the CT scans were available, especially for critically ill patients whose body composition like BMI could not be acquired. Finally, these findings allow us to evaluate CT-derived muscle measurement in the prediction of CAP or other infections.
GBD 2017 Disease and Injury Incidence and Prevalence Collaborators
Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017.