Aging Clinical and Experimental Research (2021) 33:457–462 https://doi.org/10.1007/s40520-020-01773-z SHORT COMMUNICATION Patterns of multimorbidity and risk of disability in community‑dwelling older persons Alessandra Marengoni1,2 · Roselyne Akugizibwe2 · Davide L. Vetrano2,3 · Albert Roso‑Llorach4,5 · Graziano Onder6 · Anna‑Karin Welmer2,7,8,9 · Amaia Calderón‑Larrañaga2 Received: 25 October 2020 / Accepted: 3 December 2020 / Published online: 13 February 2021 © The Author(s) 2021 Abstract The aim was to analyze the association between specific patterns of multimorbidity and risk of disability in older persons. Data were gathered from the Swedish National Study on Aging and Care in Kungsholmen (SNAC-K); 2066 60 + year-old participants living in the community and free from disability at baseline were grouped according to their multimorbidity patterns and followed-up for six years. The association between multimorbidity patterns and disability in basic (ADL) and instrumental (IADL) activities of daily living was examined through multinomial models. Throughout the follow-up, 434 (21.0%) participants developed at least one ADL and 310 (15.0%) at least one IADL. Compared to the unspecific pattern, which included diseases not exceeding their expected prevalence in the total sample, belonging to the cardiovascular/ane- mia/dementia, the sensory impairment/cancer and the musculoskeletal/respiratory/gastrointestinal patterns was associated with a higher risk of developing both ADL and IADL, whereas subjects in the metabolic/sleep disorders pattern showed a higher risk of developing only IADL. Multimorbidity patterns are differentially associated with incident disability, which is important for the design of future prevention strategies aimed at delaying functional impairment in old age, and for a better healthcare resource planning. Keywords Multimorbidity patterns · Disability · Older persons Introduction years of life lived with disability [2] and functional decline over time [3, 4]. Despite its common use in research, assess- The co-occurrence of multiple diseases in the same indi- ing the impact of simple counts of chronic diseases on health vidual, i.e., multimorbidity, is the most prevalent and bur- outcomes may be insufficient to explain the heterogene- densome condition in older adults [1], accounting for many ity across older persons’ functional status. In the past few years, patterns of systematically clustering diseases have been increasingly investigated, in an attempt to explain Alessandra Marengoni and Roselyne Akugizibwe have contributed equally to this work. 5 * Alessandra Marengoni Universitat Autònoma de Barcelona, Campus de la UAB, Alessandra.marengoni@unibs.it Bellaterra (Cerdanyola del Vallès), Spain 6 1 Department of Cardiovascular, Endocrine‑Metabolic Department of Clinical and Experimental Sciences, Diseases and Aging, Istituto Superiore Di Sanità, Rome, Italy University of Brescia, Brescia, Italy 7 2 Division of Physiotherapy, Department of Neurobiology, Aging Research Center, Department of Neurobiology, Care Care Sciences and Society, Karolinska Institutet, Stockholm, Sciences and Society, Karolinska Institutet and Stockholm Sweden University, Stockholm, Sweden 8 3 Karolinska University Hospital, Stockholm, Sweden Centro Medicina Dell’Invecchiamento, Fondazione 9 Policlinico Universitario “A. Gemelli” IRCCS, Università Stockholm Gerontology Research Center, Stockholm, Cattolica del Sacro Cuore, Rome, Italy Sweden 4 Fundació Institut Universitari per a la Recerca a l’Atenció Primària de Salut Jordi Gol i Gurina (IDIAPJGol), Gran Via Corts Catalanes 587, Barcelona, Spain 13 Vol.:(0123456789) 458 Aging Clinical and Experimental Research (2021) 33:457–462 their potential synergistic effects on several health outcomes participant had severe cognitive impairment) before partici- [5, 6]. In previous reports from our group, we showed that pation in the study. persons affected by specific multimorbidity patterns have increased risk of death [7] and dementia onset [6], compared Chronic disease assessment to those belonging to an unspecific pattern. Similarly, persons affected by specific patterns of multi- This was done using participants’ medical history, clinical morbidity may be expected to differ in their risk of develop- examination, inpatient and outpatient registers, self-reported ing functional decline and disability over time, but only few information and proxy interviews. In addition, laboratory studies have evaluated the association between multimorbid- tests and medications were used for the diagnosis of spe- ity patterns and disability, mostly at a cross-sectional level cific conditions. Chronic diseases were coded according to [5]. In the Health and Retirement Study, subjects within a the International Classification of Diseases, 10th revision pattern comprising arthritis, hypertension and depression (ICD10) and were grouped into 60 categories based on an showed the highest level of limitations in basic and instru- operationalization that has been developed and applied to mental activities of daily living compared to healthy partici- SNAC-K data in a previous proof-of-concept study (1). pants [8]. In another study, the combination of somatic and The clinical criteria for grouping the identified diagnoses mental diseases was associated with substantially greater included similarities in their pathophysiology, treatment, prospective disability than combinations comprised exclu- prognosis and prevalence. sively of somatic conditions [9]. The aim of this study was to analyze the association Disability assessment between specific patterns of multimorbidity and the six- year risk of disability in community-dwelling Swedish older The primary outcomes were incident disability in at least persons. one ADL (i.e., bathing, dressing, toilet use, urinary conti- nence, transferring self from bed and eating) and IADL (i.e., phone use, grocery shopping, food preparation, housekeep- Methods ing, laundry, use of public transport, handling finances and medication use). These were assessed using a questionnaire Study population administered by a qualified nurse, and each item was graded as “independent” or “dependent.” We carried out a prospective cohort study using data from the Swedish National study on Aging and Care in Kungshol- Covariates men (SNAC-K). SNAC-K is an ongoing longitudinal study including people aged 60 + years (range: 60–104) living Data on age, sex, education, marital status, living arrange- either in the community or in institutions in the Kungshol- ment, informal and formal care were gathered through ques- men central area of Stockholm, Sweden [10]. Participants tionnaires. Education was measured as the highest attained were randomly selected from 11 age cohorts (60, 66, 72, 78, level. Formal social care includes help with household 81, 84, 87, 90, 93, 96 and 99 + years) during the baseline chores and personal care. It is financed by the municipality wave (2001–2004), leading to a study population of 3363 and may be delivered either by the municipality or a private individuals (response rate: 73.3%). Follow-up interviews are company that has a contract with the municipality. Informal performed every 3 years for individual 78 years and above social care covers service or care assistance from relatives, and every 6 years for individuals younger than 78 years. friends, neighbors, or volunteer/non-profit organizations. The present study included data from 2741 individuals The amount of formal and informal care a person received with multimorbidity (i.e., 2 + chronic diseases) and living was recorded as hours per month. in the community at baseline, who were followed-up for 6 years. We excluded: (1) individuals with any limitations in Analysis basic or instrumental activities of daily living (i.e., ADL and IADL) at baseline (n = 592), (2) subjects receiving formal We employed a fuzzy c-means cluster analysis to classify home care at baseline (n = 51), and (3) participants with no the study participants into six homogeneous patterns of data for ADL or IADL at follow-up (n = 32). The analytical multimorbidity: psychiatric diseases; cardiovascular dis- sample consisted of 2066 participants. eases, anemia and dementia; metabolic and sleep disor- Ethical approval was obtained from the Regional Eth- ders; sensory impairments and cancer; musculoskeletal, ics Review Board in Stockholm County, and informed respiratory and gastrointestinal diseases; and unspecific consent was obtained from participants or a proxy (if the (Table S1). Participants in the unspecific pattern had 13 Aging Clinical and Experimental Research (2021) 33:457–462 459 Table 1  Baseline characteristics of participants by the different outcomes Characteristics Total N = 2066 ADL disability No ADL disability P-value IADL disability No IADL disability P-value n = 434 n = 1,027 n = 310 n = 1,205 Age, n (%) < 0.001 < 0.001 < 78 years 1,267 (61.3) 254 (58.5) 747 (72.7) 64 (20.6) 937 (77.8) ≥ 78 years 799 (38.7) 180 (41.5) 280 (27.3) 246 (79.4) 268 (22.2) Gender, n (%) < 0.001 < 0.003 Males 768 (37.2) 84 (19.4) 457 (44.5) 92 (29.7) 464 (38.5) Females 1,298 (62.8) 350 (80.6) 570 (55.5) 218 (70.3) 741 (61.5) Education, n (%) < 0.001 < 0.001 Elementary 294 (14.3) 63 (14.5) 112 (10.9) 68 (22.1) 122 (10.1) High school 1,036 (50.3) 223 (51.5) 491 (47.9) 166 (53.9) 580 (48.1) University 728 (35.4) 147 (33.9) 423 (41.2) 74 (24.0) 503 (41.7) Marital status, n (%) < 0.001 < 0.001 Unmarried 340 (16.5) 72 (16.6) 173 (16.9) 40 (12.9) 210 (17.4) Married 970 (47.2) 188 (43.3) 544 (53.0) 114 (36.8) 635 (52.7) Divorced 302 (14.7) 70 (16.1) 149 (14.5) 41 (13.2) 182 (15.1) Widow 445 (21.6) 104 (24.0) 160 (15.6) 115 (37.1) 177 (14.7) Polypharmacy, n (%) < 0.001 < 0.001 ≥ 5 drugs 701 (33.9) 185 (42.6) 269 (26.2) 157 (50.6) 324 (26.9) ≥ 10 drugs 103 (5.0) 27 (6.2) 31 (3.0) 31 (10.0) 33 (2.7) Chronic diseases, n (%) < 0.001 < 0.001 ≥ 3 chronic diseases 1,558 (75.4) 355 (81.8) 713 (69.4) 276 (89.0) 845 (70.1) ≥ 4 chronic diseases 1,046 (50.6) 254 (58.5) 452 (44.0) 228 (73.5) 524 (43.5) Multimorbidity patterns, < 0.001 < 0.001 n (%) Psychiatric 109 (5.3) 27 (6.2) 51 (5.0) 15 (4.8) 65 (5.4) Cardio/Anemia/Dementia 96 (4.6) 18 (4.1) 24 (2.3) 26 (8.4) 24 (2.0) Metabolic/Sleep 259 (12.5) 47 (10.8) 116 (11.3) 37 (11.9) 135 (11.2) Sensory/Cancer 178 (8.6) 47 (10.8) 71 (6.9) 56 (18.1) 72 (6.0) MSK/Resp/GI 320 (15.5) 83 (19.1) 143 (13.9) 65 (21.0) 170 (14.1) Unspecific 1,104 (53.4) 212 (48.8) 622 (60.6) 111 (35.8) 739 (61.3) Test: Pearson’s chi-squared Missing data: education 8, marital status 9, informal care 33 Abbreviations: GI gastro-intestinal diseases, Resp respiratory diseases, MSK musculoskeletal, Cardio cardiovascular diseases diseases that did not specifically characterize this pattern Results [11]. We used multinomial logistic regression models to test This study consisted of 1267 (61.3%) par tici- the association between multimorbidity patterns and the pants aged < 78 years and 799 (38.7%) participants different outcomes, and results were reported as relative aged ≥ 78 years (Table 1). Most of the participants in the rate ratios (RRR) with their confidence intervals. Second- study were female (n = 1298, 62.8%). Participants were ary outcomes were: (1) death during follow-up, which was distributed across the six different multimorbidity pat- derived from the Swedish death register, and (2) loss to terns as follows: psychiatric (5.3%), cardiovascular/ane- follow-up. Potential interactions between multimorbidity mia/dementia (4.6%), metabolic/sleep disorders (12.5%), patterns and sex were assessed, and sex-stratified analyses sensory impairment/cancer (8.6%), musculoskeletal/res- were carried out subsequently. Analyses were carried out piratory/gastrointestinal (15.5%) and an unspecific pattern using Stata IC/15.0, and a P-value of < 0.05 was consid- (53.4%) including diseases not exceeding their expected ered statistically significant. 13 460 Aging Clinical and Experimental Research (2021) 33:457–462 prevalence in the total sample. By the end of the 6-year non-significant. Among males, the risk of developing ADL follow-up, 434 (21.0%) of the participants developed was strengthened for the sensory impairment/cancer pattern at least one ADL. Within this group of subjects, 58.5% (RRR 2.42, 95% CI 1.14, 5.15), but no significant associa- were < 78 years, the majority were female (80.6%) and tions were observed with the other patterns. For IADL, with most had ≥ 4 chronic conditions (58.5%). During the the exception of the metabolic/sleep disorder pattern, the same period, 310 (15.0%) participants developed at least associations were strengthened for all the patterns among one IADL; they were mostly aged ≥ 78 years (79.3%) and females, including the psychiatric pattern, which became females (70.3%), 51.84% had polypharmacy and most statistically significant (RRR 2.20, 95% CI 1.02, 4.73). On had ≥ 4 chronic conditions (73.6%). the contrary, the associations with all patterns were attenu- Belonging to the cardiovascular/anemia/dementia (RRR ated and became non-significant among males (Table S2). 2.09, 95% CI 1.08, 4.06), the sensory impairment/cancer The association between the multimorbidity patterns and (RRR 1.62, 95% CI 1.05, 2.48) and the musculoskeletal/res- death or dropout can be found as supplementary material piratory/gastrointestinal (RRR 1.40, 95% CI 1.02, 1.94) pat- (Table S3). terns was significantly associated with a higher risk of devel- oping ADL, compared to the unspecific pattern (Table 2). Moreover, subjects in the cardiovascular/anemia/dementia Discussion pattern (RRR 3.11, 95% CI 1.64, 5.89), the sensory impair- ment/cancer pattern (RRR 2.11, 95% CI 1.36, 3.28), the Compared to the unspecific pattern, belonging to the car- musculoskeletal/respiratory/gastrointestinal pattern (RRR diovascular/anemia/dementia pattern, the sensory impair- 1.97, 95% CI 1.34, 2.90), and those in the metabolic/sleep ment/cancer pattern and the musculoskeletal/respiratory/ disorders pattern (RRR 1.58, 95% CI 1.00, 2.48) showed a gastrointestinal pattern was significantly associated with a higher risk of developing IADL compared with those in the higher risk of developing both ADL and IADL, whereas unspecific pattern (Table 2). subjects in the metabolic/sleep disorders pattern showed a There was no statistically significant interaction between higher risk of developing only IADL. Furthermore, in strati- the multimorbidity patterns and sex. Sex stratification fied analyses, the association between the cardiovascular/ strengthened the association between the cardiovascular/ anemia/dementia pattern and the risk of developing ADL anemia/dementia pattern and the risk of developing ADL was strengthened in women, and that between the sensory among females (RRR 3.42, 95% CI 1.42, 8.22), while impairment/cancer pattern and ADL was strengthened in the association with other patterns was weakened and men, whereas the associations with IADL development were only significant in women. These findings confirm the com- Table 2  Association (RRR and 95%CI) of multimorbidity patterns plexity and heterogeneity of multimorbidity and its conse- with the risk of developing ADL and IADL quences for older persons’ health status, suggesting the need to go beyond the simple count of chronic conditions and its Multimorbidity patterns Cases/at risk RRR (95% CI) link with increased risk of functional decline, as previously ADL established [3]. Unspecific 212/1104 Ref. Studies evaluating the topic are few and used different Psychiatric 27/109 1.50 (0.91, 2.49) methodologies in analyzing disease clustering. In the Aus- Cardio/Anemia/Dementia 18/96 2.09 (1.08, 4.06)* tralian Longitudinal Study on Women’s Health, where mul- Metabolic/Sleep 47/259 1.41 (0.95, 2.07) timorbidity patterns were identified using factor analysis, the Sensory/Cancer 47/178 1.62 (1.05, 2.48)* authors found that the cardiovascular pattern was associated MSK/Resp/GI 83/320 1.40 (1.02, 1.94)* with the greatest decline in ADL over six years, whereas the IADL neurological/mental health pattern was associated with the Unspecific 111/1104 Ref. greatest decline in IADL, compared to a group of women Psychiatric 15/109 1.79 (0.93, 3.43) that did not have multimorbidity at baseline or that were Cardio/Anemia/Dementia 26/96 3.11 (1.64, 5.89)*** multimorbid but their conditions did not group into any of Metabolic/Sleep 37/259 1.58 (1.00, 2.48)* the identified patterns [12]. Similarly, we compared specific Sensory/Cancer 56/178 2.11 (1.36, 3.28)*** multimorbidity patterns with an unspecific one including MSK/Resp/GI 65/320 1.97 (1.34, 2.90)*** diseases that did not exceed the expected prevalence in the Model adjusted by age, sex, education level, marital status total sample. Several hypotheses can be suggested concerning the dif- Abbreviations: RRR​ relative rate ratio, GI gastro-intestinal diseases, Resp respiratory diseases, MSK musculoskeletal, Cardio cardiovascu- ferential risk of disability associated with multimorbidity lar diseases, CI confidence interval patterns. First, the development of chronic diseases could P-values: *< 0.05, **≤ 0.01, ***≤ 0.001 be an intermediate link among various pathophysiological 13 Aging Clinical and Experimental Research (2021) 33:457–462 461 processes happening in older age. In fact, aging-related bio- Authors’ Contribution Conception or design of the work was contrib- logical processes such as chronic inflammation and cellular uted by AM, RA, DLV, ACL. Data analysis was contributed by RA, ARL. Interpretation of the results was contributed by all coauthors. senescence may represent the root mechanisms leading to Drafting of the article was contributed by AM, RA, ACL. Critical revi- disability through chronic diseases [13]. In a previous report, sion of the manuscript was contributed by all coauthors. Final approval we showed that inflammatory marker levels differ accord- of the manuscript was contributed by all coauthors. All the authors ing to specific patterns of multimorbidity, being highest in fulfill the ICMJE criteria for authorship. the cardiovascular multimorbidity pattern [11]. Another Funding Open Access funding provided by Karolinska Institute. This hypothesis is that the combinations of specific diseases may work was supported by the funders of the Swedish National study on enhance sarcopenia and the associated disability onset [14], Aging and Care (SNAC): the Ministry of Health and Social Affairs, which could be especially relevant in the case of the pattern Sweden; the participating County Councils and Municipalities; and including musculoskeletal and respiratory diseases, as both the Swedish Research Council. Specific grants were received from The Swedish Research Council for Medicine (VR; 521-2013-8676; conditions are often characterized by loss of lean muscle 2017-06088; 2016-00981); the Swedish Research Council for Health, mass [15, 16]. One additional possible theory is that com- Working life and Welfare (Forte; 2016-07175; 2017-01764); The Ital- binations of diseases that affect functional ability through ian Ministry of Health (PE-2016-02364885). The funders had no role different mechanisms may have a worse effect on functional in study design, data collection and analysis, decision to publish, or preparation of the manuscript. decline than comorbidities sharing common etiologic or pathophysiologic mechanisms [17]. In fact, our findings Compliance with ethical standards showed that the pattern including conditions affecting three different organ systems, i.e., cardiac diseases, dementia and Conflict of interest All authors declare that no organizations have at- anemia, was one of the most burdensome in terms of asso- tempted to influence the study or the writing of the manuscript. They ciated disability risk. Finally, recent evidence suggests that have had no financial relationships in the previous three years with any psychiatric disturbances, such as generalized anxiety disor- organizations that might have an interest in influencing the submitted work and no other relationships or activities that could appear to have ders, are more strongly associated with disability in women influenced the submitted work. than in men [18]. This is in line with our finding whereby the psychiatric pattern was only associated with incident Statement of human and animal rights The present study has been disability in females. approved by the appropriate ethics committee and has therefore been performed in accordance with the ethical standards laid down in the Among the limitations of this study are the fact that the 1964 Declaration of Helsinki and its later amendments. main exposure (i.e., multimorbidity patterns) was only measured at baseline, and the limited transportability of the Informed consent Written informed consent was obtained from all par- findings, given that SNAC-K participants are on average ticipants. For persons living in institutions and for people with demen- tia, a proxy respondent (a next of kin) was also asked for consent in wealthier and healthier than the general older population in addition to the participant (refer to SNAC-K website for details at https​ Sweden. Our strict exclusion criteria is likely to have limited ://www.snac-k.se/). the generalizability of our findings. Data sharing Data are from the SNAC-K project, a population-based study on aging and care (http://www.snac-k.se/). Access to these origi- nal data is available to the research community upon approval by the Conclusions SNAC-K data management and maintenance committee. Applications for accessing these data can be submitted to Maria Wahlberg (Maria. Wahlberg@ki.se) at the Aging Research Center, Karolinska Institutet. Findings from our study suggest that specific multimorbid- ity patterns may differentially lead to functional decline, Open Access This article is licensed under a Creative Commons Attri- which is important for better understanding the relationship bution 4.0 International License, which permits use, sharing, adapta- between diseases and disability, for the design of future pre- tion, distribution and reproduction in any medium or format, as long vention strategies aimed at delaying functional impairment as you give appropriate credit to the original author(s) and the source, in old age, and for a better healthcare resource planning. provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not Supplementary information The online version contains supplemen- permitted by statutory regulation or exceeds the permitted use, you will tary material available at (https​://doi.org/10.1007/s4052​0-020-01773​ need to obtain permission directly from the copyright holder. To view a -z). copy of this licence, visit http://creat​iveco​mmons​.org/licen​ses/by/4.0/. Acknowledgements We thank the SNAC-K participants and the SNAC-K Group for their collaboration in data collection and management. 13 462 Aging Clinical and Experimental Research (2021) 33:457–462 References Swedish National study on Aging and Care (SNAC). Aging Clin Exp Res 16:158–168 11. Marengoni A, Roso-Llorach A, Vetrano DL, et al (2020) Patterns 1. 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