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Abstract

Patients with undernutrition at admission have higher risks to worsen their nutritional status, which is linked to an increase in morbidity and mortality. This study investigated the prevalence of undernutrition at admission and its associated factors. A cross-sectional study was conducted on patients aged 18 to 59 years old in Internal Medicine ward at Dr. Cipto Mangunkusumo National General Hospital, Jakarta, Indonesia, between July and September 2019. Factors that might be associated with undernutrition at admission, such as age, sex, marital status, Charlson Comorbidity Index (CCI) and type of comorbidity, depression, and neutrophil–lymphocyte ratio (NLR), were assessed. Bivariate and multivariate analyses were used to determine the associated factors. Sixty hospitalized patients with median age of 42 years and 76.7% with married status joined the study. The most common reason for hospitalization was acute gastrointestinal disease with gallstones as the most common comorbidity. Undernutrition exists in 26.7% of subjects. High CCI score was observed among 11.7% subjects and half of subjects had NLR category ≥5. Bivariate analysis revealed that unmarried status, age ≥40 years, and malignancy were associated with undernutrition at admission. Logistic regression analysis showed malignancy as an independent predictor of undernutrition during the initial hospital admission (odds ratio [OR] = 11.8; 95% confidence interval [CI]: [1.1, 125.7]). The prevalence of undernutrition at admission was 26.7%. Factors associated with an increased prevalence of undernutrition at admission were age <40 years, unmarried status, and malignancy. Malignancy was an independent factor of the prevalence of undernutrition at admission.

Keywords

BMI hospital Indonesia internal medicine undernutrition at admission

Introduction

Hospital malnutrition remains a global problem, with reported prevalence rates varying between 20.0% and 65.5% (Barker et al., 2011; Syam et al., 2018). Malnutrition is an imbalance of nutritional state, encompassing overnutrition and undernutrition (Barker et al., 2011). Global Leadership Initiative on Malnutrition (GLIM) defines malnutrition as a combination of one phenotypic criteria (non-volitional weight loss, low body mass index [BMI], or reduced muscle mass) and one etiologic criteria (reduced food intake or inflammation/disease burden) (Cederholm et al., 2019). This condition is related to an increased number of morbidity and mortality, prolonged hospitalization, and an increased cost of care; therefore, early identification of nutritional status is important for all hospitalized patients (Correia & Waitzberg, 2003).

GLIM introduced two-step approach for diagnosing malnutrition in clinical practice, which is screening to identify population at risk followed by assessment to diagnose and grade the severity of malnutrition. The screening process can be conducted using any validated screening tool, such as Nutritional Risk Screening-2002 (NRS-2002), Mini Nutritional Assessment-Short Form (MNA-SF), Malnutrition Universal Screening Tool (MUST), and Subjective Global Assessment (SGA) depending on the population (Cederholm et al., 2019). American Society for Parenteral and Enteral Nutrition (ASPEN) recommends nutritional status screening within 24 hr upon admission. A patient with a risk of malnutrition should be referred to a clinical nutritionist for treatment to prevent further deterioration (White et al., 2012).

The nutritional status at admission can affect the incidence of worsening nutritional status during hospitalization (Zhu et al., 2017). In 2003, Feed Or Ordinary Diet (FOOD) study conducted a study in 18 countries and found several increased complications among undernourished patients at admission, such as gastrointestinal bleeding, pneumonia, and other infectious diseases (FOOD Trial Collaboration, 2003).

To date, Indonesia has still limited data on factors related to undernutrition at admission (Syam et al., 2018; Syamsiatun et al., 2004). This study aims to assess the prevalence of undernutrition at admission among Internal Medicine patients in Indonesia and its association with age, sex, marital status, type of comorbidity, depression, Charlson Comorbidity Index (CCI), and neutrophil–lymphocyte ratio (NLR).

Materials and Methods

A cross-sectional study using consecutive sampling method was carried out in the Internal Medicine ward at Cipto Mangunkusumo National General Hospital, Jakarta, Indonesia, between July and September 2019. We selected patients aged between 18 and 59 years old who were fully conscious. Pregnant patients, edema, history of diuretics use, psychiatric patients, and patients admitted for elective intervention were not included in the study. As we use NLR to assess the occurrence of inflammation in this study, patients with a history of steroid and immunosuppressant use prior to hospitalization, HIV-AIDS, hematologic malignancies, febrile neutropenia, and post-chemoradiation patients were also not included.

Study subjects underwent a series of assessments including demographic data, medical interviews to look for patient’s diseases, Beck Depression Inventory (BDI)-II Indonesia to detect depression (Ginting et al., 2013), BMI to determine nutritional status, CCI to know the existence of comorbidity, and NLR.

Body weight measurements were carried out using Electronic Bed Scale Sung Sim® E543-040 series with the precision of 0.1 kg. Height was determined using a conversion formula of knee-height according to Paramita (2012). BMI was obtained by dividing weight (kg) by height² (m²), and BMI <18.5 kg/m² was considered as undernutrition according to WHO (World Health Organization, 1995).

Statistical analysis was performed using IBM^® SPSS^® Statistics version 20. Bivariate analyses for categorical variables were performed with chi-square test or Fisher exact test as applicable. Multivariate analysis with logistic regression backward method was performed on variables with p <.25 on the bivariate analysis. Statistical significance was at p < .05. The study protocol has been approved by Ethics and Research Committee of the Faculty of Medicine, University of Indonesia (approval letter KET-389/UN2.F1/ETIK/PPM.00.02/2019).

Results

A total of 60 patients participated in the study between July and September 2019, with a median age of 42 (min–max: 18–59) years. Table 1 shows subject’s characteristics. More than half of subjects were men and mostly married. Nearly half of subjects were hospitalized due to acute gastrointestinal diseases such as hematemesis, melena, cholangitis, cholecystitis, and obstructive jaundice. The mean BMI was 22.3 ± 4.7 kg/m², and nearly a third of subjects were undernourished at admission. Most subjects had CCI score <5. We found as many as one third of subjects suffered from depression as indicated by BDI, and half of the subjects had NLR score ≥5. The most common comorbidity was gallstones (25%), followed by hypertension (20%) and malignancy (15%).

Table 1.

Characteristics of the Research Participants (n = 60).

Variable	Category	Proportion (n, %)	p value
Gender	Male	34 (56.7)	.302
Age	18–29 years	11 (18.3)	.469
	30–39 years	18 (30.0)
	40–49 years	13 (21.7)
	50–59 years	18 (30.0)
Marital status	Married	46 (76.7)	<.001
Reason for hospitalization	Acute gastrointestinal diseases	29 (48.3)	<.001
	Infection	9 (15.0)
	Non-hemorrhagic severe anemia	9 (15.0)
	Acute coronary syndrome	8 (13.3)
	Electrolyte imbalance	2 (3.3)
	Hyperglycemic crisis	3 (5.0)
CCI category ≥5	Yes	7 (11.7)	<.001
NLR category ≥5	Yes	30 (50.0)	1.00
Depression	Yes	20 (33.3)	.01
Undernutrition at admission	Yes	16 (26.7)	<.001
Comorbidities	Gallstones	15 (25.0)	N/A
	Hypertension	12 (20.0)
	Malignancy	9 (15.0)
	Diabetes mellitus	7 (11.7)
	Chronic liver disease	8 (13.3)
	Coronary heart disease	8 (13.3)
	Systemic lupus erythematosus	7 (11.7)
	Chronic kidney disease	7 (11.7)

Note. CCI = Charlson Comorbidity Index; NLR = neutrophil–lymphocyte ratio.

Factors associated with undernutrition at admission on bivariate analysis were unmarried status, age ≥40 years, and malignancy as shown in Table 2. The independent variable with p value <.25 from the results of bivariate analysis were unmarried status (p = .006), men gender (p = .152), CCI score ≥ 5 (p = .074), age ≥ 40 years (p = .028), gallstones (p = .050), malignancy (p = .008), and chronic liver disease (p = .192). Adjusted multivariate analysis showed that malignancy was an independent predictor of undernutrition upon hospital admission (p = .040; odds ratio [OR] = 11.8, 95% confidence interval [CI] = [1.1, 125.7]).

Table 2.

Analysis of Factors Associated With Undernutrition at Admission.

Variables	Undernourished		p value	Crude OR [95% CI]	Adjusted OR [95% CI]
Variables	Yesn (%)	Non (%)	p value	Crude OR [95% CI]	Adjusted OR [95% CI]
Unmarried	8 (57.1)	6 (42.9)	.006*	6.3 [1.7, 23.3]	3.10 [0.5, 21.0]
NLR ≥5	6 (20.0)	24 (80.0)	.381	0.5 [0.2, 1.6]	N/A
Depression	7 (35.0)	13 (65.0)	.470	1.9 [0.6, 6.0]	N/A
Male	12 (35.3)	22 (64.7)	.152	0.3 [0.1, 1.2]	0.6 [0.1, 3.3]
CCI ≥5	4 (57.1)	3 (42.9)	.074	4.6 [0.9, 23.2]	1.4 [0.1, 20.6]
Age ≥40 years	4 (12.9)	27 (87.1)	.028*	0.2 [0.1, 0.8]	0.2 [0.03, 1.3]
Gallstones	1 (6.7)	14 (93.3)	.050	0.1 [0.02, 1.2]	0.4 [0.03, 3.9]
Malignancy	6 (66.7)	3 (33.3)	.008*	8.2 [1.7, 38.6]	11.8 [1.1, 125.7]*
Hypertension	2 (16.7)	10 (83.3)	.486	0.5 [0.1, 2.5]	N/A

Note. OR = odds ratio; CI = confidence interval; NLR = neutrophil–lymphocyte ratio; CCI = Charlson Comorbidity Index.

Statistically significant, p < .05.

Discussion

Hospital malnutrition remains a global problem. The prevalence of hospital malnutrition ranged between 20.0% and 65.5% globally (Barker et al., 2011; Syam et al., 2018), while in Indonesia it is estimated that the prevalence of hospital malnutrition accounts for 13.0% to 65.5% (Barker et al., 2011; Budiningsari & Hadi, 2004; Dwiyanti & Hadi, 2004; Kusumayanti & Hadi, 2004; Syamsiatun et al., 2004). These different prevalence rates might be due to various population of the subjects and the diversity of diagnostic tools used in the studies. Malnutrition at hospital admission is related to prolonged hospital stay and increased morbidity and mortality, which can lead to increased cost of care (Chermesh et al., 2015). Undernourished patients at hospital admission also have a higher risk of declining nutritional status during hospitalization (Susetyowati et al., 2010). Therefore, it is very important to identify this group of patients and associated factors to prevent further deterioration of nutritional status during hospitalization.

This study was conducted in Internal Medicine ward at Cipto Mangunkusumo National General Hospital, which is a national referral hospital in Indonesia. This study observed 26.7% prevalence of undernourished subjects, which was similar to the results of a study conducted by Syam et al. (2018) in the same hospital, which was 22.7%. Subjects in our study had relatively stable medical conditions, which was different from Syam et al.’s study. This was observable from the low percentage of subjects with CCI score ≥ 5 (11.7%). The prevalence of comorbidity in our subjects was low (11.7%–25.0%), with gallstones as the most common comorbidity. Another study from developing countries conducted by Huong et al. (2014) obtained the prevalence of undernutrition at admission as 33.3%. This might be due to the older population (52.8 ± 16.9 years) with varying degrees of disease severity when compared to our study.

In our study, factors associated with malnutrition at admission based on the bivariate analysis were age, marital status, and malignancy. Gender was found unrelated to undernutrition at admission. Although this is consistent with the findings of Syam et al.’s (2018) study, other studies reported different results (Banks et al., 2007; Chermesh et al., 2015). This indicates that the role of gender in undernutrition remains controversial upon hospital admission. We did not find any association between depression and undernutrition at admission, which was in contrast with a study by Prasetyo et al. (2015). This study was performed among geriatric population in a psychiatric center, therefore leading to higher prevalence of depressive patients.

This study found that CCI scores were not associated with undernutrition at admission while Chermesh et al. (2015) found that patients with CCI scores ≥ 5 were associated with 1.3 times the incidence of malnutrition at admission. This difference might be due to the lesser comorbidities experienced in our subjects, as observable from the low percentage of patients with CCI ≥ 5 (11.7%) in our study. NLR scores were not associated with undernutrition at admission. This is consistent with the results by Fruchtenicht et al. (2018) in Brazil. We hypothesize that this insignificant result could be due to the duration of the inflammatory changes which was not long enough to cause significant changes in nutritional status. The low comorbidities status found among most of our subjects also contributed to a less systemic inflammation (Miller et al., 2013).

Age ≥ 40 years was associated with 80% reduction risk of undernutrition at admission in our study. This might be due to the alteration of body composition that is associated with aging. Aging causes an increase in body weight with a doubled increase in fat mass in men and women during middle age (Kuczmarski et al., 1994; Sheehan et al., 2003). This increase in body weight could be influenced by reduced physical activity in older age (Jakicic, 2002). However, weight loss contradictorily occurs after 60 years old. A further increase in fat mass with the main distribution in the abdominal area is followed by a decrease in fat-free mass among elderly (Sheehan et al., 2003).

Our study discovered that marital status was related to undernutrition at admission. Unmarried patients had an increased risk of 6.3× in experiencing undernutrition at admission. A previous study found that people who were married had heavier weight (Sobal & Rauschenbach, 2003). Another study had found that marital status was associated with 3.3× the risk of weight gain in men within 10 years (Kahn & Williamson, 1990). This might be because marital status is related to improved individual well-being. In addition, there is an increase in energy intake in married couples due to change of diet and eating habits (Hanson et al., 2007).

Malignancy is a type of comorbidity that affects the occurrence of undernutrition at admission in this study. Undernutrition in patients with malignancy occurs due to increased metabolic needs due to the presence of malignant cells, decrease in nutrient reserve in the body, as well as severe decrease of appetite. This unmet nutritional need results in a decreased energy intake, impaired nutrient absorption, and increased nutrient loss due to the presence of malignant cells. In addition, tumor cells can release compounds that cause increased protein catabolism, increased gluconeogenesis, and increased acute phase protein synthesis. When this condition continues untreated, patients with malignancy would suffer from cachexia (Wulandari, 2015). Malnutrition at admission in these malignant patients could be worsened by a decrease in nutritional status during hospitalization, together with all of its outcomes. Based on a study conducted by Nourissat et al. (2008) as much as 8.6% of cancer patients were undernourished and 21.9% of these undernourished patients lost weight after 2 weeks. According to a study by Susetyowati et al. (2010) using Patient Generated Subjective Global Assessment (PG-SGA), 86% of patients with malignancy and malnutrition at admission suffered from weight loss during hospitalization. Approximately one fifth of patients with malignancy died from undernutrition complications when compared to the mortality by the malignancy itself (Wulandari, 2015). This emphasizes the needs for special attention to hospitalized patients with malignancy, especially those who have experienced undernutrition upon hospital admission.

Our study showed that subjects with gallstones had lower tendency to suffer from malnutrition at admission. This is in conformity with the risk factors for gallstones, which are female, age ≥40 years, multiparity, and obesity. The formation of gallstones is due to the presence of certain substances that caused supersaturated bile. This eventually forms crystals that trap in the mucus of the gallbladder to form biliary sludge, resulting in gallstones. Because 80% of gallstones are cholesterol stones, these patients are strongly advised to consume diet low in cholesterol and saturated fat, restrict fats intake, and lost weight (Sharma & Tandon, 2012). However, we did not find any statistical significance between malnutrition at admission and gallstones (p = .05).

Our study has advantages and limitations. The advantage of using BMI to assess nutritional status in this study is practical and objective in nature. However, the use of BMI to determine the nutritional status yields lesser research participants due to the exclusion of patients with edema. Lately, there are several validated tools that can address this limitation such as NRS-2002, MNA-SF, MUST, or SGA (Schueren et al., 2014). This cross-sectional study design we used is not able to show the causal relationship between undernutrition at admission and its associated factors.

Conclusion and Recommendations

The study revealed that the prevalence of undernutrition at admission among Internal Medicine ward patients was 26.7%. Factors associated with an increased prevalence of undernutrition at admission were age <40 years, unmarried status, and malignancy. Malignancy is an independent factor associated with undernutrition at admission among Internal Medicine ward patients.

The authors recommend that nutritional screening should be done in all patients upon admission to the hospital. Specific population that need special attention regarding nutritional monitoring are young patients (age <40 years), unmarried patients, and patients with malignancy. Further research must be done in multiple sites so that the findings could be used widely.

Footnotes

Author Contributions

N.C.B. conceived the study question and contributed to the study design, undertook data collection, data analysis and interpretation, and writing the manuscript. D.S. contributed to the study design, undertook data collection and data analysis, and contributed to data interpretation, and supervised the manuscript writing. D.H.S.D. conceived the study question, and contributed to the study design, supervised data collection, data analysis and interpretation, and writing the manuscript. I.R. conceived the study question, and contributed to the study design, supervised data collection, data analysis and interpretation, and supervised the manuscript writing. D.P. conceived the study question, and contributed to the study design, supervised data collection, data analysis and interpretation, and supervised the manuscript writing.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical Approval

The study protocol has been approved by Ethics and Research Committee of the Faculty of Medicine, University of Indonesia (approval letter KET-389/UN2.F1/ETIK/PPM.00.02/2019).

ORCID iDs

Nur Chandra Bunawan

Dyah Purnamasari

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Risk Factors for Undernutrition at Admission Among Adult Hospitalized Patients at a Referral Hospital in Indonesia

Abstract

Keywords

Introduction

Materials and Methods

Results

Discussion

Conclusion and Recommendations

Footnotes

Author Contributions

Declaration of Conflicting Interests

Funding

Ethical Approval

ORCID iDs

References