- Open Access
The effectiveness of the sarcopenia index in predicting septic shock and death in elderly patients with community-acquired pneumonia
BMC Geriatrics volume 22, Article number: 341 (2022)
Community-acquired pneumonia (CAP) causes high morbidity and mortality in all age groups worldwide. Lower muscle radiodensity was associated with worse clinical outcomes (including shock) and higher in-hospital mortality. Prompt detection of sarcopenia in older adults with CAP is important. The measurement of muscle mass often involves specialized and expensive techniques. A relatively simple and inexpensive method such as the sarcopenia index (SI) to measure muscle mass would be helpful. Therefore, we performed a retrospective cohort study to assess the association between SI and septic shock risk and mortality in older patients with CAP.
In this retrospective cohort study, information on hospitalized CAP patients, including general information and septic shock, were obtained from the medical record database of the Southwest Medical University Zigong Affiliated Hospital, China. Data on patient survival and mortality (all-cause) were acquired from government authorities and telephonic follow-up. Serum creatinine (Cr) and cystatin-C (CysC) levels on admission were included in the database. The SI was determined as the serum Cr/CysC ratio × 100 and the participants were assigned to low and high SI groups. The association between SI and septic shock was evaluated by logistic regression, and that between SI and mortality by Cox regression analysis.
In total, 769 older adults (≥ 60 years) with CAP were included, of which 480(62.4%) were male and 289(37.6%)were female. We found that the total prevalence of septic shock in older adults with CAP was 16.0%. In the female group, septic shock was more prevalent in the low SI group than in the high SI group (low SI vs. high SI, 22.22% vs. 11.52%, p = 0.024). Following adjustment for confounders, there was a significant association between high SI and a lower risk of septic shock in female patients (OR = 0.38, 95%CI: 0.16–0.94; p < 0.05). The total death toll of older adults with CAP was 332(43.2%). Irrespective of sex, there was a higher risk of mortality in the low SI group (total group: low SI vs. high SI, 63.02% vs. 36.57%, p < 0.001; male group: low SI vs. high SI, 63.03% vs. 39.34%, p < 0.001; female group: low SI vs. high SI, 73.61% vs. 28.57%, p < 0.001) and, after adjustment for confounding factors and irrespective of sex, high SI was a protective factor for mortality in older adults with CAP (total group: HR = 0.64, 95%CI: 0.48–0.84; p < 0.05; male: HR = 0.69, 95%CI: 0.49–0.97; p < 0.05; female: HR = 0.39, 95%CI: 0.24–0.62; p < 0.05).
While the SI effectively predicts mortality in older adults with CAP, it was only found to be associated with septic shock in older females.
Community-acquired pneumonia (CAP) leads to high levels of morbidity and mortality among all ages throughout the world . It is most prevalent in older adults, with the highest rates in people over the age of 80 years . Mortality rates vary between 5 and 20% for patients hospitalized with CAP, reaching 50% in patients in intensive care . Studies have pointed out that lower muscle radio-density is associated with poor clinical results (including shock) . Sarcopenia is also associated with high in-hospital mortality in pneumonia patients . Therefore, the timely identification of sarcopenia in older adults with CAP is important.
Sarcopenia has been defined as “a geriatric syndrome characterized by low muscle mass and inadequate mass strength and/or physical performance” . The measurement of muscle mass usually involves specialized and expensive techniques, including dual-energy x-ray absorptiometry (DXA), bioelectrical impedance analysis (BIA), computer tomography (CT), and magnetic resonance imaging(MRI). It would thus be helpful to devise a relatively simple and inexpensive method for measuring muscle mass.
Recently, the use of the term “sarcopenia index” (SI) has been proposed in place of sarcopenia [7,8,9,10]. The SI is determined as the ratio between serum creatinine (Cr) and cystatin-C (CysC) and was defined by Kianoush et al.  as Cr/CysC × 100. The SI has been used effectively to measure both muscle mass and strength in different populations [8, 10,11,12]. Lower SI values indicate reduced muscle mass and were found to be effective in assessing the severity of malnutrition as well as predicting the need for intensive care treatment and mortality in critically ill patients .
Therefore, collecting the SI of older CAP patients at admission may provide insights into their prognosis that cannot be obtained by assessing the severity of pneumonia alone, making this assessment well-suited for improving patient-centred care settings 's recovery. Here, we conducted a retrospective cohort study to assess the association between SI and risk of septic shock and mortality in older CAP patients, assuming that low SI on admission is associated with higher septic shock and mortality in this patient population.
Research design and patients
This was a single-institution retrospective observational study done at the Southwest Medical University Zigong Affiliated Hospital, China, between January 2016 and March 2021. Hospitalized CAP patients aged 60 and over the age of 60 were included. The exclusion criteria were estimated glomerular filtration rates (eGFR) below 30 ml/min/1.73 m2, renal replacement therapy, acute kidney injury, septic shock was present on admission and patients who refused clinical follow-up. The study was approved by the Research Ethics Committee of Southwest Medical University Zigong Affiliated Hospital (No.2021-06-01).
The patients’ clinical information, including age, sex, history of drinking and smoking, height, weight, chronic diseases(including hypertension, diabetes, coronary heart disease [CHD], and chronic obstructive pulmonary disease [COPD]), septic shock, and all-cause mortality, as well as blood test results after admission, were collected. The diagnosis of septic shock refers to the diagnostic criteria described by Font et al. in 2020 .
Fasting venous blood (after overnight fasting) was drawn by experienced geriatric nurses. The SI was calculated as serum Cr/CysC × 100. The patients were then divided into two groups according to the lowest quartile SI value: patients with scores in the lowest quartile were placed in the “low SI” group and the remainder assigned to the “high SI” group.
SPSS 23.0 (IBM Corp. Armonk, NY, USA) was used for data analysis. Continuous data were expressed as means ± standard deviation (SD) or medians and interquartile ranges (IQR), based on the normality of distribution. Categorical data were represented as numbers (percentages). Patients’ baseline characteristics were compared using the Student's t test, Pearson’s χ2 test, and the logistic regression analysis was used to determine the associations between SI and septic shock and Cox regression analysis was used to determine the associations between SI and mortality. P < 0. 05 was considered to represent statistical significance.
We included 769 older adults with CAP, which of 480 (62.4%) were male and 289 (37.6%) were female. We divided the patients, including both male and female patients, into two groups according to their SI scores. In the low SI group: total < 51.08, male < 56.18, female < 44.92, and in the high SI group: total ≥ 51.08, male ≥ 56.18, female ≥ 44.92. In the total population, there were significant differences in age, serum albumin (ALB) level, eGFR, smoking history, drinking history, diabetes, and COPD between the low and high SI groups, while no differences were observed for BMI, hypertension, diabetes, and CHD. There were significant differences in male patients in the groups in terms of age, ALB level, eGFR, and smoking history, while females differed in age, ALB level, BMI, eGFR, drinking history, diabetes, and CHD between the low and high SI groups (Table 1).
We found that the total prevalence of septic shock in older adults with CAP was 16.0%, among which the prevalence of septic shock in older male patients with CAP was 17.1% and that in older female patients was 14.2%. Septic shock was more prevalent among female patients with low SI scores (low SI vs. high SI, 22.22% vs. 11.52%, p = 0.024), but this was not apparent in either male patients or the overall group (Table 2). In order to explore the relationship between SI and septic shock, we used the low SI group as the control group. Model 1 showed that SI was associated with septic shock in older female adults with CAP (OR = 0.46, 95%CI: 0.23-0.91; p < 0.05). Adjustment for age, sex, smoking history, drinking history, BMI, eGFR, ALB level, and chronic disease (hypertension, diabetes, CHD, and COPD) (Model 2) resulted in an association between high SI and a lower risk of septic shock in older female patients with CAP (OR = 0.38, 95%CI: 0.16-0.94; p < 0.05) (Table 3).
We followed up the death outcomes of all patients, starting from July 1, 2021, and ending on July 7, 2021, for a total of 1 week. The total death toll of the older adults with CAP was 332(43.2%), of which 217(45.2%) were among older male patients with CAP, and 115(39.8%) were among the older female group. A total of 297 patients died within one year after being discharged from the hospital, and 35 people died after one year. The mortality rate among patients with low SI was higher irrespective of group (total group, male, or female) (total group: low SI vs. high SI, 63.02% vs. 36.57%, p < 0.001; male group: low SI vs. high SI, 63.03% vs. 39.34%, p < 0.001; female group: low SI vs. high SI, 73.61% vs. 28.57%, p < 0.001) (Table 2). Similarly, to explore the relationship between SI and mortality, we used the low SI group as the control group. In the uncorrected model (Model 1), SI was associated with death in the overall population of older adults with CAP, the male population, and the female population (total group: HR = 0.44, 95%CI: 0.35-0.55; p < 0.05; male group: HR = 0.46, 95%CI: 0.34-0.6; p < 0.05; female group: HR = 0.26, 95%CI: 0.18-0.37; p < 0.05). After adjusting for age, sex, smoking history, drinking history, BMI, eGFR, ALB level, and chronic disease (hypertension, diabetes, CHD, and COPD) (Model 2), we found that, regardless of group, high SI is a protective factor for mortality in older adults with CAP (total group: HR = 0.64, 95%CI: 0.48–0.84; p < 0.05; male group: HR = 0.69, 95%CI: 0.49-0.97; p < 0.05; female group: HR = 0.39, 95%CI: 0.24-0.62; p < 0.05) (Table 4).
In this study, it was found that, regardless of group (total, male, or female), high SI was a protective factor for mortality in older adults with CAP. It is well known that acute diseases can cause inflammation and necrosis of tissues, leading to inflammatory reactions. This inflammatory response leads to the secretion of various factors, including cytokines and C-reactive protein, that, in turn, leads to reduced food consumption, weight loss, and diminished muscle function, promoting both malnutrition and sarcopenia in the elderly. This leads to a vicious circle of malnutrition and myocytopenia, resulting in further inflammation and repeated illnesses [14, 15].
We also observed an association between high SI and reduced risk of septic shock in older adults with CAP. It could be postulated that sarcopenia induces a prolonged catabolic state that reduces the body’s ability to respond adequately to inflammatory stimuli. Under these conditions, immune function may be reduced, leading to the development of septic shock in response to infection . However, our results cannot be generalized to male patients, and the specific reasons for this need to be further verified. Men and women differ in their protein and fat body composition and metabolism, and there are no studies that have examined the effects of sex differences on mortality in older CAP patients. Sex differences in the composition, functioning, and susceptibility to fatigue of skeletal muscles are well documented [17, 18]. Although male and female hormones clearly play a role in this dimorphism, the actual mechanism is not yet fully understood . Here, we found that the predictive value of SI for septic shock in older patients with CAP differed between males and females, suggesting that muscle exhaustion and muscle loss have different effects on disease progression and prognosis in male and female patients, and it may be necessary to develop prevention and treatment strategies for these pathological conditions based on an understanding these sex differences.
The availability of a reliable method for measuring CAP severity may assist the triage and management of patients by assisting clinical decision-making regarding conservative or more aggressive management. Thus, although there are many studies on the evaluation of CAP prognosis, each of these methods is insufficient [20,21,22,23]. This is the first time that the SI has been used to predict septic shock and mortality from CAP in older adults. These results indicate that the SI can be used as a surrogate marker for predicting septic shock in older females with CAP and mortality in older adults with CAP. A larger cohort investigation is, however, needed for confirmation.
There are several limitations to our study. First, at 769 patients, the sample size was relatively small, which, together with the retrospective observational study design, could have led to possible selection bias and affected the correction of possible confounding factors. A large cohort study may be needed to confirm our findings. Secondly, we did not use DXA or BIA to determine the actual muscle mass.
The SI is an effective predictor of mortality in older adults with CAP. However, an association between the SI and septic shock was only observed in older female patients.
Availability of data and materials
The datasets generated and analyzed during the current study are not publicly available due to this is a database which has a lot of important information and we are applying some important projects based on this. But this data sets will be available 2 years later and is also available now from the corresponding author on a reasonable request.
Dual-energy x-ray absorptiometry
Bioelectrical impedance analyses
Magnetic resonance imaging
Estimated glomerular filtration rates
Coronary heart disease
Chronic obstructive pulmonary disease
Medians and interquartile ranges
Mandell LA, Wunderink RG, Anzueto A, et al. Infectious Diseases Society of America; American Thoracic Society. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin Infect Dis. 2007;44(Suppl 2):S27-72.
Lim WS, Baudouin SV, George RC, et al. Pneumonia Guidelines Committee of the BTS Standards of Care Committee. BTS guidelines for the management of community acquired pneumonia in adults: update 2009. Thorax. 2009;64(Suppl 3):iii1-55.
Welte T, Köhnlein T. Global and local epidemiology of community-acquired pneumonia: the experience of the CAPNETZ Network. Semin Respir Crit Care Med. 2009;30(2):127–35.
Feng Z, Zhao H, Kang W, et al. Association of Paraspinal Muscle Measurements on Chest Computed Tomography With Clinical Outcomes in Patients With Severe Coronavirus Disease 2019. J Gerontol A Biol Sci Med Sci. 2021;76(3):e78–84.
Maeda K, Akagi J. Muscle Mass Loss Is a Potential Predictor of 90-Day Mortality in Older Adults with Aspiration Pneumonia. J Am Geriatr Soc. 2017;65(1):e18–22.
Cruz-Jentoft AJ, Landi F, Topinková E, et al. Understanding sarcopenia as a geriatric syndrome. Curr Opin Clin Nutr Metab Care. 2010;13(1):1–7.
Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. European Working Group on Sarcopenia in Older People. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing. 2010;39(4):412–23.
Kim SW, Jung HW, Kim CH, et al. A New Equation to Estimate Muscle Mass from Creatinine and Cystatin C. PLoS One. 2016;11(2):e0148495.
Kashani KB, Frazee EN, Kukrálová L, et al. Evaluating Muscle Mass by Using Markers of Kidney Function: Development of the Sarcopenia Index. Crit Care Med. 2017;45(1):e23–9.
Barreto EF, Kanderi T, DiCecco SR, et al. Sarcopenia Index Is a Simple Objective Screening Tool for Malnutrition in the Critically Ill. JPEN J Parenter Enteral Nutr. 2019;43(6):780–8.
Osaka T, Hamaguchi M, Hashimoto Y, et al. Decreased the creatinine to cystatin C ratio is a surrogate marker of sarcopenia in patients with type 2 diabetes. Diabetes Res Clin Pract. 2018;139:52–8.
Lin YL, Chen SY, Lai YH, et al. Serum creatinine to cystatin C ratio predicts skeletal muscle mass and strength in patients with non-dialysis chronic kidney disease. Clin Nutr. 2020;39(8):2435–41.
Font MD, Thyagarajan B, Khanna AK. Sepsis and Septic Shock - Basics of diagnosis, pathophysiology and clinical decision making. Med Clin North Am. 2020;104(4):573–85.
Gariballa S, Forster S. Effects of acute-phase response on nutritional status and clinical outcome of hospitalized patients. Nutrition. 2006;22(7–8):750–7.
Morley JE. Anorexia, sarcopenia, and aging. Nutrition. 2001;17(7–8):660–3.
Reisinger KW, van Vugt JL, Tegels JJ, et al. Functional compromise reflected by sarcopenia, frailty, and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery. Ann Surg. 2015;261(2):345–52.
Haizlip KM, Harrison BC, Leinwand LA. Sex-based differences in skeletal muscle kinetics and fiber-type composition. Physiology (Bethesda). 2015;30(1):30–9.
Bouffard J, Yang C, Begon M, et al. Sex differences in kinematic adaptations to muscle fatigue induced by repetitive upper limb movements. Biol Sex Differ. 2018;9(1):17.
Montalvo RN, Counts BR, Carson JA. Understanding sex differences in the regulation of cancer-induced muscle wasting. Curr Opin Support Palliat Care. 2018;12(4):394–403.
Loke YK, Kwok CS, Niruban A, et al. Value of severity scales in predicting mortality from community-acquired pneumonia: systematic review and meta-analysis. Thorax. 2010;65(10):884–90.
Jiang J, Yang J, Jin Y, et al. Role of qSOFA in predicting mortality of pneumonia: A systematic review and meta-analysis. Medicine (Baltimore). 2018;97(40):e12634.
Marti C, Garin N, Grosgurin O, et al. Prediction of severe community-acquired pneumonia: a systematic review and meta-analysis. Crit Care. 2012;16(4):R141.
Viasus D, Del Rio-Pertuz G, Simonetti AF, et al. Biomarkers for predicting short-term mortality in community-acquired pneumonia: A systematic review and meta-analysis. J Infect. 2016;72(3):273–82.
We thank all personnel for their contribution in the study.
This work was funded by the 2020 Zigong City Key Technology Support Plan (Project No. 2020YLSF19) and 2021 Key Science and Technology Plan of Zigong City (Project No. 2021YXY12). The sponsors did not participant in the design, methods, data collection, analysis, or in the preparation of this manuscript.
Ethics approval and consent to participate
This study was conducted in accordance with the Declaration of Helsinki and the ethical approval was obtained from the Research Ethics Committee of Southwest Medical University Zigong Affiliated Hospital (No.2021–06-01). The Research Ethics Committee of Southwest Medical University Zigong Affiliated Hospital waived informed consent for this study. All methods comply with relevant guidelines and regulations.
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Huang, S., Zhao, L., Liu, Z. et al. The effectiveness of the sarcopenia index in predicting septic shock and death in elderly patients with community-acquired pneumonia. BMC Geriatr 22, 341 (2022). https://doi.org/10.1186/s12877-022-03029-z
- Sarcopenia index
- Serum creatinine
- Serum cysteine C
- Septic shock
- Older adults