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. Author manuscript; available in PMC: 2022 Feb 14.
Published in final edited form as: Arch Gerontol Geriatr. 2019 Jan 29;82:100–105. doi: 10.1016/j.archger.2019.01.008

Risk of community-acquired pneumonia in older adults with sarcopenia of a hospital from Callao, Peru 2010–2015

Sofia Altuna-Venegas a,*, Raul Aliaga-Vega a, Jorge L Maguiña a, Jose F Parodi b,d, Fernando M Runzer-Colmenares b,c
PMCID: PMC8842506  NIHMSID: NIHMS1011369  PMID: 30739000

Abstract

Introduction:

Sarcopenia is a geriatric syndrome characterized by loss of muscle mass and strength. The prevalence in people between 60–70 years is about 5–13% and in adults over 80 years, between 11–50% in the USA. Sarcopenia increases the risk of mortality and nosocomial infections.

Community-acquired pneumonia is the first infectious-related cause of death in elderly people. However, there is lack of evidence about the association between sarcopenia and pneumonia. The aim of our study was to determine the incidence and risk factors of community-acquired pneumonia in older adults with sarcopenia in a Peruvian hospital.

Methods:

A retrospective cohort study was conducted in the geriatrics service of Centro Medico Naval “Cirujano Mayor Santiago Tavara”. Sarcopenia was defined by “European Consensus of Sarcopenia” criteria. MultivariatePoisson regression model was conducted to estimate the effect of the independent association between sarcopenia and pneumonia.

Results:

A total of 1598 subjects were enrolled, 59.0% were male; with a mean age of 78.3 ± 8.6 years. The prevalence of sarcopenia was 15.1% (95% CI: 13.3–16.8) and the incidence of community-acquired pneumonia was 15.14% (95%CI 13.4–16.9). In the multivariate model, we found a higher incidence of pneumonia in sarcopenic compared to non-sarcopenic, RR(a) 3.88 (95% CI: 2.82–5.33).

Discussion:

Our study showed a higher incidence of community-acquired pneumonia in sarcopenic subject. Results provide information on the importance of detecting this syndrome because it gives us scientific evidence of the interest of a correct comprehensive geriatric assessment in older patients with a high risk of pneumonia.

Keywords: Community-acquired pneumonia, Hospitals, Sarcopenia, Elderly

1. Introduction

There are aging-related changes that increase the risk of some health conditions or problems, such as sarcopenia, which is defined as the gradual and generalized loss of muscle mass and strength with the risk of generating frailty (Cruz-Jentoft et al., 2010). Sarcopenia is associated with an increased risk of mortality regardless of age, medical comorbidities such as chronic obstructive pulmonary disease, cardiovascular disease and/or cerebrovascular disease, disability, cognitive impairment and education (Arango-Lopera, Arroyo, Gutiérrez-Robledo, Pérez-Zepeda, & Cesari, 2013; Landi et al., 2013). It is considered that sarcopenia is a conditioning factor to acquire nosocomial infections (Cosquéric et al., 2006).

In the United States, between 5–13% of people between 60 and 70 years have sarcopenia and in adults over 80 years, the prevalence ranges between 11–50% (Morley, 2008). In Latin American cities such as Bogotá, the percentage of sarcopenia was 11.5% (Samper-Ternent, Reyes-Ortiz, Ottenbacher, & Cano, 2016) and with respect to Peru, a study by Tramontano A et al. showed a prevalence of 17.6% (Tramontano et al., 2017).

Sheean et al. showed a high prevalence of sarcopenia (60%) in patients with respiratory insufficiency who entered the ICU due to the need for mechanical ventilation (Sheean et al., 2014). Criteria for sarcopenia, as a decreased grip strength, has been linked to the risk of pneumonia, because it is an indicator of generalized muscle strength loss, including respiratory and oropharyngeal muscles (Yardimci et al., 2016). In addition, this syndrome is a risk factor for dysphagia(Maeda & Akagi, 2016), which has been associated with hospital readmission for aspiration and non-aspiration pneumonia (Cabré et al., 2014). Also, some studies have found a positive association between sarcopenia and having a respiratory complication in postoperative esophagectomy and liver transplant patients (Krell et al., 2013; Nishigori et al., 2016). However, there is lack of scientific evidence to establish the relationship between sarcopenia and community-acquired pneumonia, considered as the first cause of mortality of infectious origin in the geriatric population.

The objective of our study was to evaluate the relationship between sarcopenia and community-acquired pneumonia and other risk factors. In Latin America and Peru there is an increase in the geriatric population, so we need to focus the resources of public health in the main diseases. For example, our National Institute of Statistics (INEI) reported in 2015 the main cause of mortality in elderly population was the lower respiratory infection (INEI, 2017). Additionally, health services burden and health-related costs are increasing, on behalf of the elderly population become higher (Valdez et al., 2017). Sarcopenia, a very important (but poorly explored) geriatric syndrome, as we describe in our introduction section, is highly associated with frailty and abnormal responses to infections, therefore, we aimed our research to explore its association.

2. Methodology

2.1. Sample

A retrospective cohort study which analyzes a database where participants from Geriatric Service of Centro Medico Naval “Cirujano Mayor Santiago Tavara” which is one of the most well-equipped centers in Peru with excellent healthcare and research facilities. They have a research team, that they do geriatric evaluations on patients to improve quality of life or quality of care of older adults with sarcopenia and others geriatric diseases. The primary study conducted by the research team, entitled “Prevalence and factors associated with frailty among Peruvian older adults” has allowed the publication of different sub-studies in the topic (Díaz Villegas & Runzer Colmenares, 2015; Parodi et al., 2018; Runzer-Colmenares et al., 2014, 2017; Sandival Ampuero et al., 2017).

The participants were followed-up annual time since 2010, entering a new group every year until 2015; chosen by non-probabilistic sampling. All participants were 60 years older or more and resided in Lima or Callao. A total of 1891 subjects were recruited, 293 were excluded from this study: 89 have a Mini-Mental State Examination (MMSE) less than 17, because it reflects severe cognitive impairment (Nguyen, Black, Ray, Espino, & Markides, 2002), and 211 doesn’t have complete data of hand grip, Short Physical Performance Battery (SPPB), calf circumference, weight and/or height. Finally, 1598 subjects were included, calculating a power of 100% for an RR > 2.5 based on Nishigori et al results (Nishigori et al., 2016).

2.2. Definition of variables

2.2.1. Outcome variable

Community-acquired pneumonia was defined by the clinical-radiological diagnosis criteria of internist, pneumologist and/or geriatrician at Centro Medico Naval ‘Cirujano Mayor Santiago Tavara” in the patient’s medical history for one year after admission to the cohort. It is considered a patient with pneumonia if at least one episode of pneumonia occurred during the follow-up year We include the following ICD 10: J13-J16.

2.2.2. Exposure variable

Sarcopenia was defined based on the European Working Group on Sarcopenia in Older People criteria, who defined this syndrome characterized by low muscle mass and low strength and/or poor physical performance (Cruz-Jentoft et al., 2010),

Low muscle mass was considered when calf circumference is less than 31 cm based on the review of Rolland et al. (Rolland et al., 2003). Muscle strength by the methodology of Fried et al., which determined patients were unable to perform handgrip test and the 20% of people who obtained the lowest results, adjusted for BMI and stratified by sex were considered as decreased muscle strength (Fried et al., 2001). At least, SPPB less than 6 is considered poor physical performance by the results of Guralnik et al. (2000),

2.2.3. Co-variables

We included socio-demographic variables such: sex, age, marital status, education, military rank, years of retirement, live alone, drink alcohol consumption and smoking habit. We dichotomized our education variable as complete (> 11 years) or (10 years or less). The variable military rank has been used as a proxy of socioeconomic status as has been used in various studies (Blattner et al., 2018; Mullie et al., 2013).

The variable alcohol consumption was defined by the question: Do you usually drink alcoholic beverages?

Three questions were used to define the variable smoke: Have you ever smoked? Have you ever smoked daily for six months or more sometime in your life? Do you smoke now? Smoking habit was considered positive if they affirmed the first two and/or the last question.

Subjects were asked about these medical conditions: diabetes mellitus 2, high blood pressure, chronic kidney disease, heart failure and history of depression. The number of hospitalizations was obtained by asking the subjects how many times they had been hospitalized last year.

Additionally, four indexes and tests were considered in this study as covariates. Barthel index was used to identify the functional status of basic activities of daily living and was divided according to the recommendation of Shah, Vanclay, and Cooper (1989) in: total dependence (0–20), severe (21–60), moderate (61–90), low (91–99) and independence (100); Lawton-Brody index evaluates instrumental activities of daily living and was considered as a numerical variable; Yesavage questionnaire (5-items) evaluates depression with a cut point higher or equal than 3. Finally, MMSE, a numerical variable detects cognitive impairment.

Incomplete data is when a variable does not have the total data of the participants.

2.3. Statistical analysis

Chi-square test was used to analyze our outcome variable with categorical variables. T-student or U of Mann Whitney was used for the numerical variables with pneumonia, depending on variance homogeneity and normality. Finally, a crude and adjusted Poisson regression analysis was performed to calculate the risk ratio (RR) between sarcopenia and pneumonia and other associated confounders. We used Stata version 14.0 (Stata Corporation, College Station, TX, USA) to conduct all the analyses and a p-value < 0.05 was considered statistically significant.

2.4. Ethics

Our study was approved by two Institutional Review Board, the Centro Medico Naval “Cirujano Mayor Tavara” (Memorandum N°. 054) and the Universidad Peruana de Ciencias Aplicadas, (PI053–16).

3. Results

A total of 1598 subjects were included in the study, 59.0% were males (n = 943) and the mean age was 78.3 years (SD 8.6). 74.2% (n = 1175) were married, 73.6% (n = 1166) finished their studies and 50.9% (n = 807) had the rank of subaltern. High blood pressure, history of depression and diabetes mellitus 2 as the most frequent comorbidities: 62.6% (n = 996), 21.6%(n = 341) and 17.0%(n = 269) respectively. The mean of IBM was 25.9(SD 5.5) with a prevalence of overweight of 27.0% (n = 242). The frequency of sarcopenia was, 15.1% (n = 241). Table 1, shows sociodemographic characteristics by sarcopenia status.

Table 1.

Sociodemographic characteristics of patients participating in the study, Centro Médico Naval Cirujano Mayor Santiago Távara, 2010–2015 (N = 1598).

Characteristics With Sarcopenia Without Sarcopenia


n % n %
Total 241 15.1 1357 84.9
Sex
 Man 811 40.2 109 45.2
 Woman 546 59.8 132 54.8
Age (Mean, SD) 82.9 8.9 77.5 8.3
Marital statusa
 Single 5 2.1 41 3.1
 Married 176 73.6 999 74.3
 Widower/divorced 49 20.5 251 18.6
 Cohabitant 9 3.7 54 4.0
Education
 < 11 years 73 30.5 345 25.6
 ≥ 11 years 166 69.5 1000 74.4
Military ranka
 Officer 16 6.7 152 11.2
 Subaltern 103 43.1 704 52.3
 Civilian 120 50.2 491 36.5
Years of retirement (Mean, SD) 20.4 10.3 20.5 9.9
Live alonea
 Yes 43 17.8 186 13.8
 No 198 82.2 1164 86.2
Alcohol consumption
 Yes 116 48.1 605 44.6
 No 125 51.9 752 55.4
Smoking habit
 Yes 179 74.3 952 70.1
 No 62 25.7 405 29.9
a

Incomplete data.

Table 2, shows the percentage of subjects for each component of sarcopenia in our population. Of all patients with sarcopenia, 100% (n = 241) decreased muscle mass, 57.3% (n = 138) decreased muscle strength and 73.9% (n = 178) decreased physical performance.

Table 2.

Percentage of individuals for each component of Sarcopenia (N=1598).

Characteristicsa Definition n (%)
Low muscle mass Calf circumference less than 31 cm 941(58.9)
Low muscle strength The 20% of patients who obtained the lowest results in the grip test (adjusted for BMI and stratified by sex)
Men
Strength ≤ 19.1 for BMI ≤ 22.4
Strength ≤ 19.6 for BMI 22.5–24.8
Strength ≤ 19.6 for BMI 24.9–28.2
Strength ≤ 17.2 for BMI ≥ 28.3
Women
Strength ≤ 16.9 for BMI ≤ 22
Strength ≤ 15.2 for BMI 22.1–24.2
Strength ≤ 15.1 for BMI 24.3–27.8
Strength ≤ 19.8 for BMI ≥ 27.9
228(14.3)
Poor physical performance SPPB < 6 333(20.8)
a

Sarcopenia is defined as low muscle mass and at least one of the following:Low muscle strength and/or poor physical performance.

The accumulated incidence of community-acquired pneumonia in our study was 15.14% (95%CI 13.4–16.9). and the risk of presenting pneumonia in sarcopenic patients was 3.88 (95%CI 2.82–5.33) more than in non-sarcopenic patients.

Risk factors of pneumonia in our population are shown in Table 3. Bivariate analysis showed a significant relationship between smoking, Lawton and Brody scale, Yesavage test, Mini-mental state examination and sarcopenia with pneumonia (Table 4). Multivariate Poisson regression model found a significant relationship between smoking and sarcopenia (Table 5).

Table 3.

Clinical characteristics of patients participating in the study, Centro Medico Naval Cirujano Mayor Santiago Tavara, 2010–2015 (N = 1598).

With Sarcopenia Without Sarcopenia



Characteristics n % n %


Diabetesa
Yes 44 18.3 225 16.8
No 197 81.7 1114 83.2
High blood pressurea
Yes 143 59.3 853 63.2
No 98 40.7 497 36.8
Chronic kidney disease
Yes 57 23.6 243 18.1
No 184 76.4 1096 81.9
Heart failure
Yes 8 3.3 83 6.1
No 233 96.7 1274 93.9
History of depression
Yes 44 18.5 297 22.2
No 194 81.5 1041 77.8
Body mass index (Mean, SD) 26.2 5.9 25.8 5.4
Lawton-Brody index (Mean, SD)a 3.4 2.2 4.9 1.9
Barthel index*
Total dependent 5 2.1 21.0 1.6
Severe dependent 14 5.8 39.0 2.9
Moderate dependent 83 34.4 616.0 45.6
Mild dependent 30 12.5 199.0 14.7
Independent 109 45.2 476.0 35.2
Yesavage questionnaire (5-items)
With depression 145 60.2 262 19.3
Without depression 96 39.8 1095 80.7
Mini-Mental state examination (Mean, SD) 23.0 5.1 25.8 3.7
Hospitalizations in the last yeara
Never 99 41.1 670 49.8
1 119 49.4 554 41.2
2 23 9.5 121 9.0
a

Incomplete data.

Table 4.

Characteristics according to pneumonia of patients participating in the study, Centro Medico Naval Cirujano Mayor Santiago Tavara, 2010–2015 (N=1598).

Characteristics With Pneumonia Without Pneumonia


n % n % p value
Total 242 15.1 1356 84.9
Sex
Man 137 14.5 806 85.5 0.410
Woman 105 16.0 550 84.0
Age (Mean, SD) 79.3 9.1 78.1 85.5 0.203
Marital statusa
Single 5 10.9 41 89.1 0.557
Married 186 15.8 989 84.2
Widower/divorced 40 13.3 260 86.7
Cohabitant 11 17.5 52 82.5
Education
Less than 11 years 57 13.6 361 86.4 0.314
Greater or equal to 11 years 183 15.7 983 84.3
Military ranka
Officer 19 11.3 149 88.7 0.108
Subaltern 117 14.5 690 85.5
Civilian 106 17.4 505 82.7
Years of retirement (Mean, SD) 20.8 10.3 20.4 9.9 0.820
Live alonea
Yes 43 18.8 186 81.2 0.104
No 199 14.6 1163 85.4
Alcohol consumption
Yes 114 15.8 607 84.2 0.500
No 128 14.6 749 85.4
Smoking habit
Yes 186 16.5 945 83.5 0.024*
No 56 12.0 411 88.0
High blood pressurea,b
Yes 153 15.4 843 84.6 0.758
No 88 14.8 507 85.2
Diabetesa,b
Yes 43 16.0 226 84.0 0.738
No 199 15.2 1112 84.8
Chronic kidney diseasea,b
Yes 53 17.7 247 82.3 0.209
No 189 14.8 1091 85.2
Heart failureb
Yes 12 13.2 79 86.8 0.592
No 230 15.3 1277 84.7
History of depressiona,b
Yes 56 16.4 285 83.6 0.488
No 184 14.9 1051 85.1
Lawton-Brody index (Mean, SD)a,c 3.9 3.9 4.8 2.0 0.001*
Barthel indexa,b
Total dependent 6 23.1 20 76.9 0.051
Severe dependent 14 26.4 39 73.6
Moderate dependent 102 14.6 597 85.4
Mild dependent 26 11.4 203 88.6
Independent 92 15.7 493 84.3
Yesavage questionnairea,b (5-items)
With depression 96 23.6 331 76.4 0.001*
Without depression 146 12.3 1045 87.7
Mini-Mental state examination (Mean, SD)c 24.0 4.5 25.7 3.9 0.001*
Hospitalizations in the last yeara,b
Never 119 15.5 650 84.5 0.97
1 101 15.0 572 84.0
2 22.0 15.3 122 84.7
Sarcopeniab
Yes 106 44.0 135 56.0 0.001*
No 136 10.0 1221 90.0

p values in bold shows statistically significant association.

a

Incomplete data.

b

Chi-square test.

c

U-Mann Whitney test.

Table 5.

Poisson regression model crude and adjusted for the risk of pneumonia in elderly patients, Centro Medico Naval Cirujano Mayor Santiago Tavara, 2010–2015 (N=1598).

Variable RR crude (IC95%) p value RR adjusted (IC95%) p value
Sarcopenia 4.38(3.40–5.66) 0.001 3.88(2.82–5.33) 0.001*
Age 1.01(0.99–1.03) 0.068 0.99(0.98–1.00) 0.313
Sex 0.91(0.70–1.16) 0.448 0.96(0.74–1.26) 0.778
Smoking habit 1.37(1.01–1.85) 0.038 1.41(1.03–1.95) 0.035*
Lawton-Brody index 0.86(0.81–0.90) 0.001 0.93(0.85–1.02) 0.136
Yesavage questionnaire (5-items) 1.92(1.49–2.49) 0.001 0.70(0.45–1.10) 0.121
Mini-Mental state examination 0.92(0.89–0.95) 0.001 0.96(0.92–1.00) 0.081

p values in bold shows statistically significant association.

4. Discussion

Prevalence of sarcopenia in our population was 15.1% (95% CI: 13.3–16.8) which is similar to the prevalence reported in another study in Peru (17.6%) (Tramontano et al., 2017). Similar prevalence is reported in a geriatric population of Brazil: 16.1% in women and 14.4% in men (da S. Alexandre, Duarte, Santos, Wong, & Lebrão, 2014); while in Bogota the prevalence is lower (11.5%) (Samper-Ternent et al., 2016). In contrast, the prevalence in Mexico was 33.8% which differs from the countries already described and may be due to different characteristics such overweight with a prevalence of 48.1%, higher than our country (Arango-Lopera, Arroyo, Gutiérrez-Robledo, & Pérez-Zepeda, 2012). Likewise, these studies described different methods, criteria, and cutoff points to define sarcopenia.

Respect to community-acquired pneumonia worldwide, we found incidence rates of 13.95 per 1000 older adults per year approximately in Spain (Ochoa-Gondar et al., 2008) and 18.3 cases per 1000 per year in the United States (Simonetti, Viasus, Garcia-Vidal, & Carratalà, 2014). However, there is lack of information about the cumulative incidence of pneumonia in geriatric population participating in a cohort with clinical and hospitalization care like our study.

Risk factors identified in the subjects of our study were smoking and sarcopenia. The presence of sarcopenia increased 3.88 times the risk of this infection; this can be explained probably because it alters the immune system by decreasing muscle IL-15 production, which is important in natural killer cells functioning (Lutz & Quinn, 2012) and there is a dysregulation of the fosfatidilinositol 3 kinase pathway (PI3k / Akt) whose dysfunction alters neutrophils migration and phagocytosis (Wilson, Jackson, Sapey, & Lord, 2017). Besides, in the sarcopenia exist a generalized muscle strength loss, including respiratory muscles (Yardimci et al., 2016). For these reasons, the patient is in a state of immunosuppression and is prone to pneumonia. In our study, smoking that showed an increased risk of pneumonia in 41%. This is a risk factor very studied in relation to pneumonia and it has been demonstrated that there are anatomical factors, such as the alteration of the bronchial mucosa, and immunological factors, such as the alteration of the opsonization capacity, phagocytosis and the maturation of dendritic cells; that makes it prone to the growth of the germs in the Broncho-alveolar tree (Almirall, Blanquer, & Bello, 2014).

Recently dysphagia due to sarcopenia (i.e. “sarcopenic dysphagia”) has been reported as a new concept. Sarcopenic dysphagia results from low swallowing and general skeletal muscle mass and strength. The characteristic changes in swallowing muscles occur primarily in oral and pharyngeal muscles along with other associated factors (van der Maarel-Wierink, Vanobbergen, Bronkhorst, Schols, & de Baat, 2011). A meta-analysis on aspiration pneumonia in frail older people revealed that dysphagia is a significant risk factor for aspiration pneumonia (Sakai & Sakuma, 2017).

Other studies have demonstrated the association between pneumonia with high blood pressure, diabetes mellitus 2, chronic kidney disease, alcoholism, and gender (Bahat et al., 2010; Calle et al., 2014; Koivula, Sten, & Mäkelä, 1994; Loeb, McGeer, McArthur, Walter, & Simor, 1999; Riquelme et al., 1996). But, our study has not appreciated those associations possibly because some variables were self-reported such alcohol intake, smoking, high blood pressure, diabetes mellitus 2, chronic kidney disease, heart failure, history of depression. Similarly, subjects were selected because they belonged to an ambulatory geriatric program at Centro Medico Naval, which is not the case in other cohorts.

A previous study has shown that cognitive ability has a relation to physical fragility in older adults (Gale, Ritchie, Cooper, Starr, & Deary, 2017). However, in our study was not associated because patients with severe dementia were excluded, so the variable lost significance.

Sarcopenia is a broad geriatric syndrome that includes functional aspects and possibly early onset. These involve functional factors that can be evaluated through geriatric tests such as Lawton-Brody and Barthel indexes. In addition, as depression has been shown to be related to the risk of pneumonia (Riquelme et al., 1996), we have the Yesavage test tool to allow us to screen for depression. For these reasons, it is important a complete geriatric evaluation in our elderly patients.

Sarcopenia and frailty factors are associated with pneumonia and the risk of disability in the older adults, models of evidence-based programs for the prevention and management of these problems should be considered in order to fit health services to the real needs of the Older Adults, including patient-centered clinical decisions based on the comprehensive geriatric assessment.

Our investigation had some limitations. First, the sample was chosen by convenience and only retired veterans and their relatives attended in the hospital were selected; for this reason, a selection bias was generated because they do not represent elderly people in Peru. In addition, it was a secondary analysis of database, we can only use comorbidities described in the original study and could exist information bias due to possible improper registration. On the other hand, the diagnostic test for measurement of muscle mass in our study was calf circumference; although we know other accessible tests have more sensitivity as bioimpedance or dual energy X-absorptiometry (DEXA) but were not available for this study. Diagnosis of community-acquired pneumonia was based on the medical history of subjects with possible information bias.

Additionally, some variables with missing information were associated with our outcome variable, which means that some bias may be present and affect our conclusions. However, missing data were not associated with sarcopenia or community-acquired pneumonia.

This study shows an elevated risk of pneumonia in patients with sarcopenia, which could be explained by the presence of immunological alterations, loss of respiratory muscle strength and difficulty of swallowing, particularly in adults with higher rates of malnutrition like our community. Finally, these findings allow us to evaluate future measures for the prevention of sarcopenia and in the future to evaluate the impact of the treatment of this syndrome in the reduction of community-acquired pneumonia or other infections, which is a field not yet studied.

Acknowledgements

We are grateful to Centro de Investigacion del Envejecimiento (CIEN) of Universidad San Martin de Porres (USMP) for providing us with the database for the study. To the faculty team of research of the medical school of Universidad de Ciencias Aplicadas (UPC) for their appreciations and comments.

Jorge L. Maguiña is a doctoral candidate studying Epidemiological Research at Universidad Peruana Cayetano Heredia under FONDECYT/CIENCIACTIVA scholarship EF033–235-2015 and supported by training grant D43 TW007393 awarded by the Fogarty International Center of the US National Institutes of Health.

Footnotes

Conflict of interest

The authors declare that they have no conflicts of interest concerning this article.

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