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Association between frailty and hypoproteinaemia in older patients: meta-analysis and systematic review

BMC Geriatrics volume 24, Article number: 689 (2024) Cite this article

Abstract

Objective

Frailty and hypoproteinaemia are common in older individuals. Although there is evidence of a correlation between frailty and hypoproteinaemia, the relationship between frailty and hypoproteinaemia in hospitalized/critically ill and older community residents has not been clarified. Therefore, the aim of our meta-analysis was to evaluate the associations between frailty and hypoproteinaemia in different types of patients.

Methods

A systematic retrieval of articles published in the PubMed, Embase, Medline, Web of Science, Cochrane, Wanfang, and CNKI databases from their establishment to April 2024 was performed to search for studies on the associations between severity of frailty or prefrailty and hypoproteinaemia in older adults. The Newcastle‒Ottawa Scale and the Agency for Healthcare Research and Quality Scale were used to assess study quality.

Results

Twenty-two studies were included including 90,351 frail older people were included. Meta-analysis revealed an association between frailty or prefrailty and hypoproteinaemia (OR = 2.37, 95% CI: 1.47, 3.83; OR = 1.62, 95% CI: 1.23, 2.15), there was no significant difference in the risk of hypoproteinaemia between patients with severe frailty and those with low or moderate frailty (OR = 0.62, 95% CI:0.44, 0.87). The effect of frailty on the occurrence of hypoproteinaemia was more obvious in hospitalized patients/critically ill patients than in surgical patients (OR = 3.75, 95% CI: 2.36, 5.96), followed by older community residents (OR = 2.30, 95% CI: 1.18, 4.49).

Conclusion

Frailty is associated with hypoproteinaemia in surgical patients, hospitalized older patients and older community residents. Future studies should focus on the benefits of albumin supplementation in preventing or alleviating frailty and related outcomes in the future.

Peer Review reports

Introduction

With the increase in global ageing, frailty has gradually become a health issue of concern [1]. Frailty is a multidimensional geriatric syndrome involving reduced physiological reserve and increased susceptibility to stress,including physiological, psychological, social, nutritional, sensory and other aspects. Compared with nonfrail patients, frail patients are more prone to falling, developing a disability and experiencing other adverse events; thus, frailty is considered an effective indicator for predicting mortality and complications [2, 3]. Although there is no unified frailty assessment tool at present, many biochemical indicators (albumin, C-reactive protein, 25-hydroxyvitamin D, etc.) are considered related to frailty [4], and the albumin concentration is a component of the Essential Frailty Tool (EFT). In addition, the albumin concentration can be used to predict patient outcomes and mortality regardless of the patient’s comorbidities [5,6,7,8]. When a patient's appetite decreases, the ability to consume food is decreases, and in turn, gastrointestinal absorption decreases, which leads to the decreased absorption of nutrients, especially protein, and thus, a the decreased albumin index occurs.Hypoproteinaemia is considered to occur when the albumin concentration is < 35 g/L. Hypoproteinaemia is a clinical syndrome related to malnutrition and disease-related inflammatory responses, and the albumin level decreases with increasing age. Therefore, older hospitalized patients are a high-risk group with a high incidence of hypoproteinaemia [9]. Previous studies have shown that hypoproteinaemia can lead to tissue and organ oedema in patients, resulting in pleural effusion, delayed incision healing and other manifestations, which are closely related to the prognosis of patients [10]. The incidence of pulmonary infection, deep vein thrombosis, acute myocardial infarction and cardiac insufficiency among those individuals with hypoproteinaemia has been reported to be significantly greater than that among those with normal albuminaemia [11].

Studies have shown a negative correlation between frailty and hypoproteinaemia [12] and a meta-analysis, which was conducted only in the surgical population, supports this view. Therefore, the aim of this systematic review was to evaluate the relationship between frailty and hypoproteinaemia in different types of older adults.

Materials and methods

Data sources and searches

The PubMed, Embase, Medline, Web of Science, Cochrane, Wanfang and CNKI databases were searched systematically for articles published from the inception of each library to April 2024, with no language restrictions. Some grey literature was also included in our research. Owing to network limitations, our research team could not obtain master's theses in foreign languages, so we only searched for master's theses written in Chinese; moreover, some types of articles such as conference papers, abstracts, letters and animal experiments were excluded. As an example, the search formula used in EMBASE in Method S1 in the Supplementary Materials. Our study was approved by PROSPERO[CRD42023447386].

Study selection and data extraction

This systematic overview incorporates observational studies, primarily including cross-sectional and longitudinal research. A literature search was conducted according to the previous inclusion and exclusion criteria, and the retrieved studies were imported into an EndNote literature management database for literature screening; two investigators independently performed data extraction and quality assessment of the included studies. Disagreements were resolved by consensus. The extracted data included the following: first author name; year, institute, and country of publication; and type of study. Subject characteristics included the sample size, mean age, sex, frailty evaluation method, frailty incidence, and diagnostic criteria for hypoproteinaemia.

Risk-of-bias assessment

The authors (Yin and Yang) independently used the Newcastle‒Ottawa Scale (NOS) and the Agency for Healthcare Research and Quality (AHRQ) to evaluate the risk of bias [13, 14]. The NOS scale, which ranges from 1 to 9 points, judges each study on three dimensions: the selection of the study group, the comparability of groups, and the determination of the benefit outcome. A score of 5 is considered to indicate a high risk of bias, whereas scores of 5–7 and ≥ 8 are considered to indicate a moderate or low risk of bias. The risk of bias in cross-sectional studies was evaluated via the cross-sectional study quality evaluation scale recommended by the AHRQ, which consists of 11 items. The evaluation options for each item are "yes", "no" and "unclear"; the selection of "yes" is worth 1 point, and the selection of "no" or "unclear" is worth 0 points. The score of each item is added to obtain the total score, which ranges from 0 to 11 points, with 0 to 3 indicating low quality, 4 to 7 indicating medium quality, and 8 to 11 indicating high quality. The results were checked by two researchers independently, and any disagreements were resolved through discussion.

Data synthesis and analysis

The Cochrane Collaboration provides Review Manager (RevMan) version 5.3 for data analysis. The I2 test was used to analyse the heterogeneity of the included studies. When I2 was ≤ 50% and P was > 0.05, a fixed-effects model was used for the meta-analysis; otherwise, the random-effects model was used for the meta-analysis. Subgroup analysis was also performed to explore the source of heterogeneity. Sensitivity analysis was performed via Stata version 17.0 to evaluate the stability of the results, and each study was excluded one by one to observe the potential influence of each literature on the size of the combined effect. A P value < 0.05 was considered to indicate publication bias.

Results

A search of the literature databases yielded 12,858 articles. After removing duplicate studies and preliminarily reading the study titles and abstracts, we screened a total of 247 studies. Finally, 225 articles were excluded, and a total of 22 articles were included in the meta-analysis. A flow chart of the results of the literature search and screening process is shown in Fig. 1.

Fig. 1
figure 1

Flow Diagram of the Study Selection Process

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Main features of the included studies

A total of 22 studies were included, 13 in English [15,16,17,18,19,20,21,22,23,24,25,26,27] and 9 in Chinese [28,29,30,31,32,33,34,35,36], with 5 being cross-sectional studies [15, 27, 31, 34, 36], 7 being prospective studies [18,19,20, 23, 30, 33, 35], and 10 being retrospective studies [16, 17, 21, 22, 24,25,26, 28, 29, 32]. The included studies involved 90,351 patients whose average age ranged from 55 to 81 years. The studies were carried out in China [24, 27,28,29,30,31,32,33,34,35,36], the United States [16, 22, 25], Australia [18, 19, 23], Germany [20, 21], the United Kingdom [15, 26] and Japan [17]. The research subjects were surgical patients in most studies [16, 17, 20,21,22,23,24,25, 27,28,29,30, 32,33,34,35] and community residents in two studies [15, 36]. Four research subjects were hospitalized/critically ill patients [18, 19, 26, 31]. Of the 22 studies included, 19 reported an association between frailty and hypoproteinaemia, and 4 studies [15, 20, 25, 36] reported an association between prefrailty and hypoproteinaemia. Three studies [16, 17, 27] reported an association between frailty and hypoproteinaemia in terms of frailty severity. Overall, the included studies were of medium to high quality, with 11 of high quality. The main features of the included studies are shown in Table 1.The quality of each study is evaluated in the supplementary materials.

Table 1 Features of the included studies
Full size table

Frailty assessment

Among all the studies, 8 used a modified frailty index (mFI) [16, 18, 24, 25, 28, 29, 32, 33], and 6 identified frailty on the basis of the Fried frailty phenotype (FFP) [15, 19, 20, 23, 30, 36]. The clinical frailty scale (CFS) was used in four studies [17, 22, 26, 27], the Medical Research Council (MRC) score was adopted in two studies [31, 34], and an ultrasonic technique was employed in one study [35]. One study used the Canadian Study of Health and Ageing (11-CSHA) and the age-adjusted Charlson Comorbidity Index(aa-CCI) metrics for frailty assessment [21].

Definition of hypoproteinaemia

The criteria used for the diagnosis of hypoproteinaemia vary from study to study, but most studies define hypoproteinaemia as a serum albumin level of < 35 g/L [16,17,18, 21, 25,26,27,28, 31, 32]. Six studies did not provide clear diagnostic criteria for hypoproteinaemia [19, 22, 33,34,35,36]. Other studies defined hypoproteinaemia as an albumin concentration of < 33 g/L [23], < 34 g/L [24], < 42 g/L [15], < 36 g/L [20], < 25 g/L [30] or a total serum protein concentration of < 60 g/L [29].

Meta-analysis of frailty and hypoproteinaemia

Association of hypoproteinaemia in frail and nonfrail older individuals

A random-effects meta-analysis of 19 observational studies [15, 18,19,20,21,22,23,24,25,26, 28,29,30,31,32,33,34,35,36] revealed a significant association between frailty and hypoproteinaemia (OR = 2.37, 95% CI: 1.47, 3.83; Fig. 2). However, there was a high degree of heterogeneity among the studies (I2 = 93%, p < 0.00001), so the analysis was performed via a random effects model. We performed subgroup analyses according to the type of study, the region where the study was conducted, the sample size, the frailty assessment tools, and the study population, and the heterogeneity was slightly reduced but still high. The subgroup analyses are shown in Table 2.

Fig. 2
figure 2

Forest map of hypoproteinaemia in frail and nonfrail older individuals

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Table 2 Subgroup analysis of the association between frailty and hypoproteinaemia
Full size table

Subgroup analysis revealed that frailty was significantly associated with hypoproteinaemia in cross-sectional/prospective studies, studies with a sample size > 500, studies in Europe and the United States, and studies using the FFP and other types of assessment tools; in addition, equally significant associations were found between study populations and hypoproteinaemia. There were no significant associations with hypoproteinaemia in retrospective studies, Asian regional studies, studies with sample sizes ≤ 500, or studies that used the CFS or FI as assessment tools. The results of subgroup analysis are shown in the Supplementary Materials.

Relationship between hypoproteinaemia and prefrail patients

We further analysed the association between prefrailty and hypoproteinaemia (Fig. 3). In 4 studies [15, 20, 25, 36], patients with frailty were more likely to develop hypoproteinaemia than prefrail patients were (OR = 1.87, 95% CI: 1.75, 1.99, I2 = 0%). The incidence of hypoproteinaemia in prefrail patients was 1.62 times greater than that in nonfrail patients (OR = 1.62, 95% CI: 1.23, 2.15; I2 = 50%).

Fig. 3
figure 3

a Forest map of hypoproteinaemia in patients with frailty and prefrailty. b Forest map of hypoproteinaemia in patients with prefrailty and nonfrailty

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Relationship between frailty severity and hypoproteinaemia

Three studies [16, 17, 27] graded frailty according to severity. There was no significant risk of hypoproteinaemia between patients with severe frailty and those with low or moderate frailty (OR = 0.62, 95% CI: 0.44, 0.87, I2 = 16%; Fig. 4). Regardless of the degree of frailty, patients with frailty have a higher risk of hypoproteinemia than those without frailty (OR = 1.79, 95% CI: 1.03, 3.11; I2 = 80%) (OR = 2.16, 95% CI: 1.45, 3.24; I2 = 27%).

Fig. 4
figure 4

a Forest map of hypoproteinaemia in patients with low/mild and severe frailty. b Forest map of hypoproteinaemia in patients with low/mild frailty and nonfrailty. c Forest map of relationship between hypoproteinemia in patients with severe frailty and nonfrailty

Full size image

Association between frailty and hypoproteinaemia in surgical patients/hospitalized or critically ill/community residents

The results (Fig. 5) revealed that the effect of frailty on the occurrence of hypoproteinosis was more obvious in hospitalized/critical patients than in surgical patients (OR = 3.75, 95% CI: 2.36, 5.96), followed by older residents in the community (OR = 2.30, 95% CI: 1.18, 4.49), possibly because, for surgical patients, careful and comprehensive evaluation [37] by the medical team optimized their preoperative physical condition, thus reducing the occurrence of hypoproteinaemia.

Fig. 5
figure 5

Forest map of the relationship between frailty and hypoproteinaemia in surgical patients/hospitalized or critically ill and older community residents

Full size image

Sensitivity analysis and publication bias

A sensitivity analysis of 19 included studies was performed on the association between frailty and hypoproteinaemia. Heterogeneity did not change significantly after each study was excluded, indicating that the results of this study were relatively stable. Begg’s and Egger’s tests were used to statistically test the asymmetry of the funnel plot, and the results revealed no publication bias (Egger’s test, p = 0.604; Begg’s test, p = 0.576). The funnel plots are presented in the Supplementary Materials.

Discussion

This systematic review and meta-analysis explored the relationship between frailty and hypoproteinaemia through observational studies (cross-sectional, cohort studies). This investigation revealed a significant association between frailty and hypoproteinaemia, with frail patients having a 2.37-fold greater risk of developing hypoproteinaemia than nonfrail patients did. Although a previous meta-analysis focused on the association between frailty and postoperative hypoproteinaemia [38], that study included only surgical patients in the analysis, and the associations between frailty and hypoproteinaemia in hospitalized patients and community residents were not analysed. The present study included older community residents and hospitalized patients in an analysis of the relationship between frailty and hypoproteinaemia in this population. The association between frailty and hypoproteinaemia can be explained as follows. First, with increasing age, the physiological reserve of older individuals significantly decreases, susceptibility to stress significantly increases, and frailty easily occurs. Additionally, frail or older patients have certain difficulties in buying and preparing food because of the decline in their own functions. Moreover, owing to the degradation of oral physiological functions (such as decreased taste or smell, tooth loss, muscle atrophy, and deactivation of the swallowing reflex) of patients with asthenia, their interest in eating is affected, which further affects the chewing and swallowing of protein-rich foods and thus affects the intake of nutrients, especially protein [39, 40]. Second, frail older individuals often have various concomitant chronic diseases [41]. Moreover, the level of plasma albumin in older people decreases physiologically with increasing age [42], and the incidence of infection increases significantly. When infection occurs, the levels of inflammatory factors increase, mRNA expression is inhibited, albumin synthesis decreases, and the risk of hypoproteinaemia increases [43]. Finally, owing to the decreased immunity of frail older individuals, the incidence of acute infectious diseases is high. When frail older individuals develop hypoproteinaemia, a large amount of albumin penetrates into the tissue space, and its decomposition rate increases. Moreover, in patients with acute infection, the intestinal function is disrupted, the intestinal mucosal barrier is damaged, and a large amount of albumin penetrates the intestinal cavity through the intestinal mucosal microvascular wall and is lost, resulting in reduced intestinal nutrient absorption and hypoproteinaemia [44]. It is evident that enhancing patients' nutritional status, particularly through supplementing protein intake, is an effective approach to prevent or alleviate frailty. However, controversy persists in the academic community regarding the dosage, frequency, and timing of protein supplementation. Some studies suggest that the average protein requirement and recommended dietary intake are 0.6 g/kg/d and 0.8 g/kg/d, respectively [45]. In practice, protein supplementation should be tailored according to the individual circumstances of the patient or older individual.

One limitation of this study is that no subgroup analysis of potential confounders (age, sex, disease category, etc.) was performed to further explore whether such factors affect the relationship between frailty and hypoproteinaemia. This is due to the lack of detailed data on these indicators in several studies. Heterogeneity among the included studies was high. Although subgroup analysis revealed a decrease in heterogeneity, the heterogeneity was still high, which may have affected the accuracy of the findings. The results of the subgroup analysis suggested no significant associations between frailty and hypoproteinaemia in retrospective studies, Asian studies, studies with sample sizes ≤ 500, and studies that used the CFS and FI as assessment tools, which may have been due to recall bias in the retrospective studies leading to nonsignificant results. In this meta-analysis, although 12 studies in Asia were included, the number of studies was significantly smaller than that in Europe and the United States. In the future, large-scale multicentre studies should be conducted in Asia to confirm the association between frailty and hypoproteinaemia. This association still exists when FFP and other frailty assessment tools are used. However, frailty was not associated with hypoproteinaemia in the CFS or FI assessment tools. The insignificance of the CFS results may be related to the small number of participants or the inconsistent definition of frailty severity, and the insignificance of the association between FI and hypoproteinaemia may be related to the different compositions of indicators constituting FI. The different definitions of hypoproteinaemia in different studies also influenced the results.

Conclusion

Frailty was found to be associated with the risk of hypoproteinaemia. Frailty increased the risk of hypoproteinaemia, and frailty was a risk factor for hypoproteinaemia. Frailty was associated with hypoproteinaemia regardless of the frailty severity and whether the study subjects were hospitalized patients or older people living in the community. These findings emphasize the importance of timely interventions for frailty in hospitalized patients and community residents. Protein supplementation is an important way to improve hypoproteinaemia in frail patients/older people. Moreover, another concern is whether the incidence of adverse outcomes (such as mortality and complications) can be improved after protein supplementation in frail patients/older people, which suggests the need to further explore this aspect in future investigations.

Availability of data and materials

Not applicable.

Data availability

No datasets were generated or analysed during the current study.

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Authors and Affiliations

  1. Nursing Department, Affiliated Hospital of Zunyi Medical University, Zunyi, 563000, China

    Linxue Zhang, Pingping Yang, Furong Yin, Jinbo Zhang, Benli Zhao & Jiamei Zhou

  2. Nursing College, Zunyi Medical University, Zunyi, 563000, China

    Linxue Zhang, Pingping Yang, Furong Yin, Jinbo Zhang, Benli Zhao & Jiamei Zhou

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LX is responsible for plaintiff writing and data analysis, FR and PP are responsible for data extraction and verification, JB and BL are responsible for text translation and proofreading, and JM is responsible for the whole research promotion and supervision, and all authors reviewed the manuscript. All authors meet authorship criteria and read and approved the final manuscript. The author(s) would like to thank all staff who contributed to making this study possible.

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Correspondence to Jiamei Zhou.

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Zhang, L., Yang, P., Yin, F. et al. Association between frailty and hypoproteinaemia in older patients: meta-analysis and systematic review. BMC Geriatr 24, 689 (2024). https://doi.org/10.1186/s12877-024-05275-9

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Keywords

BMC Geriatrics

ISSN: 1471-2318

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