Open Access Original
Article

DOI: 10.7759/cureus.47520

Poor Social Functioning: A Potentially Modifiable
Risk Factor for Pneumonia in the Elderly
Sugihiro Hamaguchi 1, 2 , Sho Sasaki 3, 2 , Sayaka Shimizu 3, 4 , Hajime Yamazaki 3, 2 , Ryohei Yamamoto 2, 3 ,Akihiro Ozaka 5, 2 , Hiroaki Nakagawa 2, 1 , Taro Takeshima 6, 2 , Joseph Green 7 , Shunichi Fukuhara 2, 3, 5, 8

Review began 10/07/2023
Review ended 10/18/2023
Published 10/23/2023© Copyright 2023
Hamaguchi et al. This is an open accessarticle distributed under the terms of theCreative Commons Attribution License CCBY 4.0., which permits unrestricted use,
distribution, and reproduction in any
medium, provided the original author andsource are credited.

1. Department of General Internal Medicine, Fukushima Medical University, Fukushima, JPN 2. Center for Innovative
Research for Communities and Clinical Excellence (CiRC2LE), Fukushima Medical University, Fukushima, JPN 3.
Section of Clinical Epidemiology, Department of Community Medicine, Graduate School of Medicine, Kyoto University,
Kyoto, JPN 4. Research Section, Patient Driven Academic League (PeDAL), Tokyo, JPN 5. Department of General
Medicine, Shirakawa Satellite for Teaching and Research (STAR), Fukushima Medical University, Shirakawa, JPN 6.
Center for University-Wide Education, School of Health and Social Services, Saitama Prefectural University, Saitama,
JPN 7. Graduate School of Medicine, The University of Tokyo, Tokyo, JPN 8. Department of Health Policy andManagement, Johns Hopkins Bloomberg School of Public Health (JHSPH), Baltimore, USA
Corresponding author: Sugihiro Hamaguchi, hamasugi@fmu.ac.jp

Abstract
Background
Most risk factors for developing community-acquired pneumonia (CAP) are age-related and chronic medical
conditions; modifying these factors can be challenging, especially in the elderly. Poor social functioning,
however, has a negative impact on medical conditions but can be improved through interventions.
Therefore, the social functioning domain of health-related quality of life (HRQOL) may be a modifiable risk
factor for the development of CAP. This study investigated the association between poor social functioning
and the incidence of CAP in elderly individuals.

Methodology
We conducted a retrospective cohort study using a dataset from 2018 to 2021, derived from an annual
questionnaire-based survey of a cohort of community-dwelling people aged 75 years or older (the Sukagawa
Study). The dataset included social functioning subscale scores of HRQOL obtained from the Eight-Item
Short Form (SF-8) questionnaire. Health insurance claims data were matched with these HRQOL data. For
each participant, the exposure (HRQOL) was measured, and outcomes (incidence of CAP) were observed
yearly from 2018 through 2021.

Results
The four observation years had a total of 17,016 observation periods among 6,513 participants. The annual
incidence rate of CAP was 0.90-1.77%. Lower social functioning was associated with a higher risk of CAP.
Specifically, for each standard deviation difference in social functioning score, the adjusted rate ratio for
CAP incidence was 1.26 (95% confidence interval (CI) = 1.08-1.48). In a subgroup analysis, the association
between social functioning and CAP differed by sex (p = 0.037). Specifically, the adjusted rate ratio for CAP
incidence was 1.41 (95% CI = 1.17-1.70) in men and 1.00 (95% CI = 0.76-1.35) in women.

Conclusions
Poor social functioning is an important risk factor for CAP in the elderly, especially in men. Interventions
that improve social functioning may help to prevent CAP.

Categories: Geriatrics, Infectious Disease, Pulmonology
Keywords: community-acquired pneumonia, risk factors for pneumonia, pneumonia in the elderly, social
functioning, health-related quality of life

Introduction
In Japan, pneumonia is an important cause of morbidity and mortality. In part because of Japan’s current
demographic structure and trends, most risk factors for death among patients in Japan who havecommunity-acquired pneumonia (CAP) are age-related, chronic conditions [1]. The result is that preventing
patients with CAP from dying is often difficult [2]. Therefore, in a society with a large proportion of elderly
people, it might be more effective to put some emphasis on preventing pneumonia rather than focusing only
on preventing death after pneumonia is diagnosed.
Risk factors for CAP include age, smoking, environmental exposure (e.g., metal, dust, fumes), malnutrition,
previous CAP infection, chronic obstructive pulmonary disease (COPD)/asthma, functional impairment,poor dental health, use of immunosuppressive therapy, and use of gastric-acid-suppressing drugs [3].

How to cite this article
Hamaguchi S, Sasaki S, Shimizu S, et al. (October 23, 2023) Poor Social Functioning: A Potentially Modifiable Risk Factor for Pneumonia in the
Elderly. Cureus 15(10): e47520. DOI 10.7759/cureus.47520

However, modifying those risk factors is either impossible (e.g., age) or challenging, especially in elderly
individuals. To reduce the incidence of CAP in rapidly aging countries such as Japan, additional studies areneeded to identify modifiable risk factors.
Pneumonia is associated with reduced health-related quality of life (HRQOL) in elderly patients [4-6]. In
most research on this topic, HRQOL is the outcome variable, but poor HRQOL can be a causal risk factor forsome medical conditions. For example, poor HRQOL was found to be a predictor of hospitalization andmortality among patients undergoing hemodialysis [7], while a separate study showed that having moresocial ties was associated with greater resistance to upper respiratory tract infections [8]. In addition, theresults of a pilot randomized controlled trial conducted during the coronavirus disease 2019 (COVID-19)
pandemic demonstrated that in older adults an eight-week online interactive course using LINE (a freeware
app for instant communications with exchanging texts, images, videos, and audios on electronic devices)
reduced loneliness, as well as improved scores on the HRQOL domains of psychological health and social
relationships [9]. Together, these findings suggest that the social aspect of HRQOL is modifiable and that it
may be a risk factor for CAP.
Additionally, some studies have identified that being male is a risk factor for both pneumonia incidence andmortality, albeit for reasons that remain unknown [2,10]. In light of sex disparities observed in social
participation [11], it is postulated that sex-specific variations may exist in the association between the social
aspect of HRQOL and the incidence of pneumonia.
In this retrospective cohort study, we examined the relationship between the social aspect of HRQOL andthe incidence of CAP in elderly individuals. We also conducted a subgroup analysis defined by sex toinvestigate sex-specific differences.

Materials And Methods
Participants and setting
Much of the data came from the Sukagawa Study, a community-based cohort study that includes individuals
aged 75 years or older residing in Sukagawa City, Fukushima Prefecture, Japan. According to the cohort
profile of the Sukagawa Study, Sukagwa city is considered a representative of the provincial cities in Japan interms of research purposes [12]. The data were collected over four years, i.e., 2018 to 2022. To address gaps
in the data, we also incorporated information obtained in the same study in 2015, 2016, and 2017 using
multiple imputations. The Sukagawa Study is an annual questionnaire-based survey of all Sukagawa City
residents aged 75 years or older who voluntarily provide consent to participate during the initialquestionnaire administration. Data were collected using paper-based instruments. Comprehensive socialand health-related data were collected.
After consenting to enrollment in the registry, participants received documents outlining their prerogative
to withdraw consent at any time, along with a consent withdrawal form. Data derived from thequestionnaires were later combined with demographic data; disease-related information according to theInternational Classification of Diseases, Tenth Revision (ICD-10); prescription drug records; details
regarding nursing care; and periodic updates on mortality and relocation status sourced from the data of the
Healthcare Claims Database, healthcare institutions, and government authorities.
This cohort has already been described in detail [12]. Data regarding individuals who had dementia andthose who needed at least a moderately high level of nursing care (level 3 or higher, see below) were excluded
from the analysis because their social functioning was already minimal. The diagnosis of dementia wasbased on the Mini-Cog [13], a dementia screening instrument administered yearly, with a score of 2 or lessindicating the presence of dementia. The nursing care levels used were those of Japan’s long-term careinsurance system [14] which is under the purview of municipal administrations and classifies nursing careneeds into five levels, with level 1 indicating the least disabled and level 5 indicating the most disabled.

Exposure
The exposure was the score on the Social Functioning question item of the Eight-Item Short Form (SF-8)[15]. The SF-8 is a self-administered questionnaire that has one item to measure each of the eight domainsof HRQOL, namely, physical functioning, role-physical, bodily pain, general health, vitality, social
functioning, role-emotional, and mental health. It has been studied psychometrically and clinically and has
been used in Japan [16]. SF-8 data were scored using standardized national norms. The scores can beinterpreted by comparison with scores from a representative sample of the general population of Japan, withmean = 50, and one standard deviation (SD) = 10.

OutcomeThe outcome was the incidence rate of CAP during each year-long observation period. CAP was defined aseither a simple chest X-ray image or computed tomography (CT) scan obtained during an outpatient
visit including that with subsequent emergency hospitalization on the same day, which was consistent with

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one of the following ICD-10 diagnoses: lobar pneumonia, diffuse pneumonia, acute pneumonia, senile
pneumonia, bacterial bronchopneumonia, influenza rod pneumonia, pneumococcal pneumonia, rod
pneumonia, staphylococcal pneumonia, methicillin-resistant Staphylococcus aureus pneumonia,
enterococcal pneumonia, Pseudomonas aeruginosa pneumonia, mycoplasma pneumonia, legionella
pneumonia, and COVID-19 pneumonia.

Study design
The exposure and the outcome were measured once each year, as shown in Figure 1. SF-8 data were collectedfrom questionnaires distributed in March of each year. Each one-year period of observation for incident
cases of CAP began on April 1.

FIGURE 1: Study design.
Data were collected over four observation periods, each of which lasted for one year. Eight-Item Short Form (SF8) data were collected from questionnaires distributed in March of each year. Each one-year period of observation
for incident cases of community-acquired pneumonia began on April 1.

Confounders
Based on previous research, especially based on evidence from the systematic review [3], we considered thefollowing 12 variables to be potential confounding factors: age, sex, current smoking status, malnutrition,
history of pneumonia, COPD, asthma, peptic ulcer, care level (an equivalent of functional impairment) [14],the number of remaining teeth (as a proxy for general oral hygiene), rheumatic disease, and malignancy. Allof these variables were assessed at the time of exposure measurement. Malnutrition was defined as a bodymass index of less than 18.5 kg/m 2, according to the criteria of the European Society of Clinical Nutrition
and Metabolism [17]. Pneumonia, COPD, asthma, peptic ulcer, rheumatic disease, and malignancy wereconsidered present if their ICD-10 codes could be confirmed using insurance claim data. The number ofremaining teeth was classified as 0, 1-9, 10-19, or 20 or more. Peptic ulcer was considered to be present if
the participant had received a prescription for a proton pump inhibitor, an H2 antagonist, or a potassiumcompetitive acid blocker.

Ethics approval
This study adhered to the tenets of the Declaration of Helsinki and was approved by the Internal Ethics
Review Board of Fukushima Medical University (approval number: 2975). The ethics board waived therequirement for written informed consent because this study was retrospective.

Statistical analysis
Descriptive analysis was used to describe the patients’ backgrounds at the beginning of the observation
periods. Normally distributed continuous variables are described as mean and SD or as median andinterquartile range. Non-normally distributed and categorical variables are described as the number andproportion.
To verify the association between exposure and outcomes, we estimated the rate ratio using generalized
estimating equations (GEEs) with robust analysis of variance. This approach accounted for the clustering ofdata within individuals. The rate ratio was estimated using the log link function and the Poisson distribution
model. First, the crude relationship between the exposure and outcome was estimated, followed bymultivariate analysis. The multivariate model included adjustments for the confounding factors describedabove. Because dropouts, including deaths, competed with the outcome, the observation period during
which a dropout occurred and subsequent information were excluded from the analysis (Figure 1).

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We also analyzed data in sex-defined subgroups. In this analysis, we used a model in which sex was excluded
from the explanatory variables. We also obtained p-values for the interaction between sex and social
functioning subscale scores from that model.
Missing data, except for missing exposure and outcome data, were handled with multiple imputation bychained equation (MICE) [18]. To increase the precision of estimates from that process, MICE also used
Sukagawa Study data obtained in 2015, 2016, and 2017, which were not used in other analyses. Two-tailed
p-values of less than 0.05 were taken to indicate statistical significance. All statistical analyses were doneusing Stata version 18.0 (Stata Corp., College Station, TX, USA).

Results
Study flow and baseline characteristics
As shown in Figure 2, 17,016 (n = 6,513) of the 20,938 (n = 7,480) observation periods in the Sukagawa Study
from 2018 to 2021 were included in the analysis. The baseline characteristics of the participants are
summarized in Table 1. The annual incidence of CAP was 0.90% to 1.77% from 2018 to 2021.

FIGURE 2: Study flowchart.

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Measured

Missing

n = 17,016
Male

7,646 (44.9%)0

Age in years (mean and SD)

81.0 (4.6)

0Body mass index (mean and SD)

23.3 (3.2)

3,034 (17.8%)

Smoking status

585 (3.4%)

Non-smoker

10,067 (59.2%)

Past smoker

5,294 (31.1%)

Current smoker

1,070 (6.3%)

Teeth remaining

12,457 (73.2%)

0935 (5.5%)

1–9

1,193 (7.0%)

10–19

1,079 (6.4%)

20+

1,352 (7.9%)

Nursing care level

28 (0.2%)

0

16,899 (99.3%)

1

51 (0.3%)

2

38 (0.2%)

Known risk factors for CAP
History of pneumonia

658 (3.9%)

0Asthma4,244 (25.2%)

0

COPD

6,073 (35.7%)

0Rheumatic disease953 (5.6%)0Peptic ulcer disease

3,148 (18.5%)0Cancer3,658 (21.5%)0Metastatic cancer

569 (3.3%)

0

TABLE 1: Baseline characteristics.
SD: standard deviation; CAP: community-acquired pneumonia; COPD: chronic obstructive pulmonary disease

Number of cases of CAP
In 2018, 2019, 2020, and 2021, the annual incidence rates of CAP were 1.77, 1.55, 0.94, and 0.90,
respectively. During the four years of this study, 223 cases of CAP were recorded: each of the 195
participants had one case and each of the 14 participants had two cases.

Association between social functioning score and CAP incidence
According to the results of the univariate analysis, having social functioning scores lower than the national
norm was directly related to CAP incidence. That relationship was robust to the adjustments forconfounders included in the multivariate model (Table 2).

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5 of 9Point estimate

95% CI

Unadjusted rate ratio

1.45

1.23–1.70

Multivariate-adjusted rate ratio

1.26

1.08–1.48

TABLE 2: Association between social functioning score and incidence of CAP in the subsequentyear.
In multivariate analysis, we adjusted for age, sex, current smoking status, malnutrition, history of pneumonia, COPD, asthma, peptic ulcer, level of care,number of remaining teeth, rheumatic disease, and malignancy. The point estimates are rate ratios of CAP incidence per one-SD-lower-than-the-nationalnorm score on the SF-8 social functioning item.
CAP: community-acquired pneumonia; CI: confidence interval; COPD: chronic obstructive pulmonary disease; SD: standard deviation; SF-8: Eight-Item
Short Form

Subgroup analysis by sex
According to the results of the subgroup multivariate analysis, the association between low social
functioning scores and subsequent CAP incidence was stronger among men than among women. Theinteraction between social functioning scores and sex was statistically significant (p = 0.037) (Table 3).

Multivariate-adjusted rate ratio

Point estimate

95% CIMen

1.42

1.17–1.70

Women

1.01

0.76–1.35

TABLE 3: Association between social functioning score and CAP incidence, stratified by sex.
In multivariate analysis, we adjusted for age, current smoking status, malnutrition, history of pneumonia, COPD, asthma, peptic ulcer, level of care, numberof remaining teeth, rheumatic disease, and malignancy. The point estimates are multivariate-adjusted rate ratios of CAP incidence per one-SD-lower-thanthe-national-norm score on the SF-8 social functioning item. The interaction between social functioning scores and sex was statistically significant (p =0.037).
CAP: community-acquired pneumonia; CI: confidence interval; COPD: chronic obstructive pulmonary disease; SD: standard deviation; SF-8: Eight-Item
Short Form

Discussion
The results presented above show that poor social functioning was associated with the subsequent incidenceof CAP. Moreover, the association between social functioning and CAP was stronger in men than in women.
Both of these results came from analyses that were adjusted for age and other likely confounders.
In the participants as a whole, having a social functioning score that was one SD (i.e., 10 points) lower thanthe Japanese national norm was associated with a 26% higher risk of CAP incidence in the following year.
The subgroup analysis showed that the higher risk of CAP incidence mentioned above was confined almost
completely to men. Specifically, low social functioning in men was associated with a 41% higher risk of CAP
incidence in the following year, whereas in women the size of that effect was almost zero.
To our knowledge, no previous study has assessed HRQOL as a potential risk factor for CAP in elderly
people. We found only one study in which QOL was used as a potential risk factor for CAP development [19].
However, in that study the performance status (PS) index [20] was used as a surrogate for QOL, and the CI
for the adjusted odds ratio included 1: 3.17, 95% CI = 0.55-18.04. The PS index reflects physical impairment
in cancer patients; it is not a patient-reported outcome measure and is instead typically assessed byhealthcare providers. It is also unidimensional [20]. Therefore, the PS index is not considered to be useful asa substitute for a measure of HRQOL. In contrast, the SF-8 is a patient-reported and multidimensional
measure that includes an item asking directly about the social aspect of HRQOL. Furthermore, physicalfunctional impairment, which is the main component of the PS index, is a known risk factor for CAP [3]. In
contrast, we focused on the social aspect of HRQOL.
Social functioning can be greatly influenced by the quality and quantity of social connections andrelationships [21]. A meta-analysis of 148 studies found an association between social relationships and2023 Hamaguchi et al. Cureus 15(10): e47520. DOI 10.7759/cureus.47520

6 of 9mortality [22]. Considering that pneumonia is among the leading causes of death in elderly people, it isplausible that social functioning is linked to pneumonia-related mortality.
As noted above, the association between poor social functioning and subsequent CAP incidence was muchstronger in men than in women. Some studies have identified that women have more social interaction
related to health than men and that women may benefit from social capital more than men [23,24].
Therefore, the minimal association with the occurrence of pneumonia in women may be explained by thepotential protective effect of stronger social relationships. A recent study classified elderly people in Japan
into one of the following three groups: “Active,” “Socially isolated,” or “Less motivated,” and found that men
were more likely to be in the “Socially isolated” group. People in that group had the lowest probability ofinteracting with others, limited social participation, and a reduced sense of safety [25]. Thus, older men in
Japan have relatively poor social relationships, which appears to put them at a greater risk of CAP incidence.
The results of this study have at least one important practical implication: Interventions aimed at improvingsocial functioning might prevent some cases of CAP. Social functioning is a multidimensional domain of
HRQOL which is strongly affected by social relationships. Therefore, it can potentially be improved throughsome interventions to increase social interaction. For example, a pilot study of a randomized controlled trial
showed that an eight-week online interactive course using LINE reduced loneliness and improved thepsychological health and social relationship domains of QOL among elderly individuals during the COVID19 pandemic [9]. Further, a community-based interventional longitudinal study found that more frequent
participation in eight-week social interaction sessions improved the QOL of elderly individuals whencompared with less frequent participation. Therefore, interventions designed to improve the social
functioning of elderly individuals, particularly men with poor social functioning, may help to prevent CAP.
Our study has some limitations. First, for outcome measurement (CAP incidence), we used the data derived
from insurance claim data. Therefore, in some cases, the recorded diagnosis may differ from the actual
medical condition. However, the outcome criterion included the requirement for chest radiography, whichshould reduce the likelihood of false positives and false negatives. Furthermore, the use of ICD-10 codes tonotate medical records of pneumonia has been reported to be a valid method and superior to the use of
symptoms and signs or radiological findings [26]. Therefore, we believe that the outcome definition we usedin our study was not out of standard for research purposes. Second, the potential confounding factors of
immunosuppressant use and antacid use were replaced with proxies (rheumatic disease, cancers, and peptic
ulcer disease) owing to the absence of prescription information. Given that those disorders are veryfrequently accompanied by the use of the drugs in question, we believe that using those proxies is unlikely
to have introduced important bias. Third, we used SF-8, an abbreviated version of the SF-36. Although the
SF-36 is a well-established, reliable, and valid HRQOL instrument that is used worldwide, including 36 more
items in the already very limited space of the questionnaire for this community-based survey waschallenging. We found the SF-8 to be much more feasible in this setting. Importantly, when using the SF-8
the compromise is minimal. Not only are the SF-36 and SF-8 in the same lineage but both have comparable
reliability and validity [27]. Fourth, among confounders, the remaining teeth had several missing data
(73.2% missing). These missing measurements were due to the fact that the number of remaining teeth wasmeasured only in 2018. In other words, the number of remaining teeth was an item that was not missing for
97% of the 4,700 subjects in 2018. As oral health is a significant risk factor for developing pneumonia
according to the systematic review, MICE was used to address the missing number of remaining teeth tominimize bias in the results [28]. Finally, environmental factors (e.g., dust exposure) are known to be risk
factors for CAP incidence but were not measured. Previous studies have utilized regional values, such as
particulate matter 2.5, rather than patient-specific information, for these factors. As we used data from aquestionnaire survey and health insurance claims, measurement of these factors was not feasible.

Conclusions
Poor social functioning may be a modifiable risk factor for CAP incidence in elderly people, particularly inmen. In these people, the hypothesis that interventions to improve social functioning will reduce theincidence rate of CAP should be tested.

Additional Information
Author Contributions
All authors have reviewed the final version to be published and agreed to be accountable for all aspects of thework.
Concept and design: Sugihiro Hamaguchi, Sho Sasaki, Shunichi Fukuhara, Joseph Green
Acquisition, analysis, or interpretation of data: Sugihiro Hamaguchi, Sho Sasaki, Sayaka Shimizu,
Hajime Yamazaki, Ryohei Yamamoto, Akihiro Ozaka, Hiroaki Nakagawa, Taro Takeshima, Shunichi Fukuhara
Drafting of the manuscript: Sugihiro Hamaguchi, Shunichi Fukuhara, Joseph Green

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Critical review of the manuscript for important intellectual content: Sugihiro Hamaguchi, Sho Sasaki,
Sayaka Shimizu, Hajime Yamazaki, Ryohei Yamamoto, Akihiro Ozaka, Hiroaki Nakagawa, Taro Takeshima,
Shunichi Fukuhara, Joseph Green
Supervision: Shunichi Fukuhara

Disclosures
Human subjects: Consent was obtained or waived by all participants in this study. The Internal Ethics
Review Board of Fukushima Medical University School of Medicine issued approval 2975. The ethics board
waived the requirement for written informed consent because this study was retrospective. Animal
subjects: All authors have confirmed that this study did not involve animal subjects or tissue. Conflicts ofinterest: In compliance with the ICMJE uniform disclosure form, all authors declare the following:
Payment/services info: All authors have declared that no financial support was received from anyorganization for the submitted work. Financial relationships: All authors have declared that they have nofinancial relationships at present or within the previous three years with any organizations that might havean interest in the submitted work. Other relationships: All authors have declared that there are no otherrelationships or activities that could appear to have influenced the submitted work.

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2023 Hamaguchi et al. Cureus 15(10): e47520. DOI 10.7759/cureus.47520

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