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

Risk Factors for Undernutrition at Admission Among Adult Hospitalized Patients at a Referral... 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 grade the severity of malnutrition. The screening process can Introduction be conducted using any validated screening tool, such as Hospital malnutrition remains a global problem, with reported Nutritional Risk Screening-2002 (NRS-2002), Mini prevalence rates varying between 20.0% and 65.5% (Barker Nutritional Assessment-Short Form (MNA-SF), Malnutrition et al., 2011; Syam et al., 2018). Malnutrition is an imbalance Universal Screening Tool (MUST), and Subjective Global of nutritional state, encompassing overnutrition and undernu- Assessment (SGA) depending on the population (Cederholm trition (Barker et al., 2011). Global Leadership Initiative on et al., 2019). American Society for Parenteral and Enteral Malnutrition (GLIM) defines malnutrition as a combination Nutrition (ASPEN) recommends nutritional status screening of one phenotypic criteria (non-volitional weight loss, low within 24 hr upon admission. A patient with a risk of malnu- body mass index [BMI], or reduced muscle mass) and one etiologic criteria (reduced food intake or inflammation/dis- Universitas Indonesia-Dr Cipto Mangunkusumo National General ease burden) (Cederholm et al., 2019). This condition is Hospital, Jakarta, Indonesia related to an increased number of morbidity and mortality, Southeast Asian Minister of Education Organization Regional Centre for prolonged hospitalization, and an increased cost of care; Food and Nutrition (SEAMEO RECFON), Jakarta, Indonesia therefore, early identification of nutritional status is important Corresponding Author: for all hospitalized patients (Correia & Waitzberg, 2003). Dyah Purnamasari, Endocrinologist, Department of Internal Medicine, GLIM introduced two-step approach for diagnosing mal- Faculty of Medicine, Universitas Indonesia-Dr. Cipto Mangunkusumo nutrition in clinical practice, which is screening to identify National General Hospital, Jl. Salemba Raya no. 6, Jakarta 10430, Indonesia. population at risk followed by assessment to diagnose and Email: dyah_p_irawan@yahoo.com Creative Commons CC BY: This article is distributed under the terms of the Creative Commons Attribution 4.0 License (https://creativecommons.org/licenses/by/4.0/) which permits any use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). 2 SAGE Open trition should be referred to a clinical nutritionist for treat- Results ment to prevent further deterioration (White et al., 2012). A total of 60 patients participated in the study between July The nutritional status at admission can affect the inci- and September 2019, with a median age of 42 (min–max: dence of worsening nutritional status during hospitalization 18–59) years. Table 1 shows subject’s characteristics. More (Zhu et al., 2017). In 2003, Feed Or Ordinary Diet (FOOD) than half of subjects were men and mostly married. Nearly study conducted a study in 18 countries and found several half of subjects were hospitalized due to acute gastrointestinal increased complications among undernourished patients at diseases such as hematemesis, melena, cholangitis, cholecys- admission, such as gastrointestinal bleeding, pneumonia, and titis, and obstructive jaundice. The mean BMI was 22.3 ± 4.7 other infectious diseases (FOOD Trial Collaboration, 2003). kg/m , and nearly a third of subjects were undernourished at To date, Indonesia has still limited data on factors related admission. Most subjects had CCI score <5. We found as to undernutrition at admission (Syam et al., 2018; Syamsiatun many as one third of subjects suffered from depression as et al., 2004). This study aims to assess the prevalence of indicated by BDI, and half of the subjects had NLR score ≥5. undernutrition at admission among Internal Medicine patients The most common comorbidity was gallstones (25%), fol- in Indonesia and its association with age, sex, marital status, lowed by hypertension (20%) and malignancy (15%). type of comorbidity, depression, Charlson Comorbidity Index Factors associated with undernutrition at admission on (CCI), and neutrophil–lymphocyte ratio (NLR). bivariate analysis were unmarried status, age ≥40 years, and malignancy as shown in Table 2. The independent variable Materials and Methods with p value <.25 from the results of bivariate analysis were unmarried status (p = .006), men gender (p = .152), CCI A cross-sectional study using consecutive sampling method score ≥ 5 (p = .074), age ≥ 40 years (p = .028), gallstones was carried out in the Internal Medicine ward at Cipto (p = .050), malignancy (p = .008), and chronic liver disease Mangunkusumo National General Hospital, Jakarta, Indonesia, (p = .192). Adjusted multivariate analysis showed that between July and September 2019. We selected patients aged malignancy was an independent predictor of undernutrition between 18 and 59 years old who were fully conscious. upon hospital admission (p = .040; odds ratio [OR] = 11.8, Pregnant patients, edema, history of diuretics use, psychiatric 95% confidence interval [CI] = [1.1, 125.7]). patients, and patients admitted for elective intervention were not included in the study. As we use NLR to assess the occur- rence of inflammation in this study, patients with a history of Discussion steroid and immunosuppressant use prior to hospitalization, HIV-AIDS, hematologic malignancies, febrile neutropenia, Hospital malnutrition remains a global problem. The preva- and post-chemoradiation patients were also not included. lence of hospital malnutrition ranged between 20.0% and Study subjects underwent a series of assessments includ- 65.5% globally (Barker et al., 2011; Syam et al., 2018), while ing demographic data, medical interviews to look for in Indonesia it is estimated that the prevalence of hospital patient’s diseases, Beck Depression Inventory (BDI)-II malnutrition accounts for 13.0% to 65.5% (Barker et al., Indonesia to detect depression (Ginting et al., 2013), BMI to 2011; Budiningsari & Hadi, 2004; Dwiyanti & Hadi, 2004; determine nutritional status, CCI to know the existence of Kusumayanti & Hadi, 2004; Syamsiatun et al., 2004). These comorbidity, and NLR. different prevalence rates might be due to various population Body weight measurements were carried out using of the subjects and the diversity of diagnostic tools used in Electronic Bed Scale Sung Sim® E543-040 series with the the studies. Malnutrition at hospital admission is related to precision of 0.1 kg. Height was determined using a conver- prolonged hospital stay and increased morbidity and mortal- sion formula of knee-height according to Paramita (2012). ity, which can lead to increased cost of care (Chermesh et al., 2 2 BMI was obtained by dividing weight (kg) by height (m ), 2015). Undernourished patients at hospital admission also and BMI <18.5 kg/m was considered as undernutrition have a higher risk of declining nutritional status during hos- according to WHO (World Health Organization, 1995). pitalization (Susetyowati et al., 2010). Therefore, it is very ® ® Statistical analysis was performed using IBM SPSS important to identify this group of patients and associated Statistics version 20. Bivariate analyses for categorical factors to prevent further deterioration of nutritional status variables were performed with chi-square test or Fisher during hospitalization. exact test as applicable. Multivariate analysis with logistic This study was conducted in Internal Medicine ward at regression backward method was performed on variables Cipto Mangunkusumo National General Hospital, which is a with p <.25 on the bivariate analysis. Statistical signifi- national referral hospital in Indonesia. This study observed cance was at p < .05. The study protocol has been approved 26.7% prevalence of undernourished subjects, which was by Ethics and Research Committee of the Faculty of similar to the results of a study conducted by Syam et al. Medicine, University of Indonesia (approval letter KET- (2018) in the same hospital, which was 22.7%. Subjects in 389/UN2.F1/ETIK/PPM.00.02/2019). our study had relatively stable medical conditions, which Bunawan et al. 3 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. Table 2. Analysis of Factors Associated With Undernutrition at Admission. Undernourished Yes No Variables n (%) n (%) 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. was different from Syam et al.’s study. This was observable In our study, factors associated with malnutrition at from the low percentage of subjects with CCI score ≥ 5 admission based on the bivariate analysis were age, marital (11.7%). The prevalence of comorbidity in our subjects was status, and malignancy. Gender was found unrelated to low (11.7%–25.0%), with gallstones as the most common undernutrition at admission. Although this is consistent comorbidity. Another study from developing countries con- with the findings of Syam et al.’s (2018) study, other stud- ducted by Huong et al. (2014) obtained the prevalence of ies reported different results (Banks et al., 2007; Chermesh undernutrition at admission as 33.3%. This might be due to et al., 2015). This indicates that the role of gender in under- the older population (52.8 ± 16.9 years) with varying degrees nutrition remains controversial upon hospital admission. of disease severity when compared to our study. We did not find any association between depression and 4 SAGE Open undernutrition at admission, which was in contrast with a malignancy would suffer from cachexia (Wulandari, 2015). study by Prasetyo et al. (2015). This study was performed Malnutrition at admission in these malignant patients could among geriatric population in a psychiatric center, there- be worsened by a decrease in nutritional status during hospi- fore leading to higher prevalence of depressive patients. talization, together with all of its outcomes. Based on a study This study found that CCI scores were not associated with conducted by Nourissat et al. (2008) as much as 8.6% of can- undernutrition at admission while Chermesh et al. (2015) cer patients were undernourished and 21.9% of these under- found that patients with CCI scores ≥ 5 were associated with nourished patients lost weight after 2 weeks. According to a 1.3 times the incidence of malnutrition at admission. This study by Susetyowati et al. (2010) using Patient Generated difference might be due to the lesser comorbidities experi- Subjective Global Assessment (PG-SGA), 86% of patients enced in our subjects, as observable from the low percentage with malignancy and malnutrition at admission suffered of patients with CCI ≥ 5 (11.7%) in our study. NLR scores from weight loss during hospitalization. Approximately one were not associated with undernutrition at admission. This is fifth of patients with malignancy died from undernutrition consistent with the results by Fruchtenicht et al. (2018) in complications when compared to the mortality by the malig- Brazil. We hypothesize that this insignificant result could be nancy itself (Wulandari, 2015). This emphasizes the needs due to the duration of the inflammatory changes which was for special attention to hospitalized patients with malignancy, not long enough to cause significant changes in nutritional especially those who have experienced undernutrition upon status. The low comorbidities status found among most of hospital admission. our subjects also contributed to a less systemic inflammation Our study showed that subjects with gallstones had lower (Miller et al., 2013). tendency to suffer from malnutrition at admission. This is in Age ≥ 40 years was associated with 80% reduction risk conformity with the risk factors for gallstones, which are of undernutrition at admission in our study. This might be female, age ≥40 years, multiparity, and obesity. The forma- due to the alteration of body composition that is associated tion of gallstones is due to the presence of certain substances with aging. Aging causes an increase in body weight with a that caused supersaturated bile. This eventually forms crys- doubled increase in fat mass in men and women during mid- tals that trap in the mucus of the gallbladder to form biliary dle age (Kuczmarski et al., 1994; Sheehan et al., 2003). This sludge, resulting in gallstones. Because 80% of gallstones increase in body weight could be influenced by reduced are cholesterol stones, these patients are strongly advised to physical activity in older age (Jakicic, 2002). However, consume diet low in cholesterol and saturated fat, restrict fats weight loss contradictorily occurs after 60 years old. A fur- intake, and lost weight (Sharma & Tandon, 2012). However, ther increase in fat mass with the main distribution in the we did not find any statistical significance between malnutri- abdominal area is followed by a decrease in fat-free mass tion at admission and gallstones (p = .05). among elderly (Sheehan et al., 2003). Our study has advantages and limitations. The advantage Our study discovered that marital status was related to of using BMI to assess nutritional status in this study is prac- undernutrition at admission. Unmarried patients had an tical and objective in nature. However, the use of BMI to increased risk of 6.3× in experiencing undernutrition at determine the nutritional status yields lesser research partici- admission. A previous study found that people who were pants due to the exclusion of patients with edema. Lately, married had heavier weight (Sobal & Rauschenbach, there are several validated tools that can address this limita- 2003). Another study had found that marital status was tion such as NRS-2002, MNA-SF, MUST, or SGA (Schueren associated with 3.3× the risk of weight gain in men within et al., 2014). This cross-sectional study design we used is not 10 years (Kahn & Williamson, 1990). This might be able to show the causal relationship between undernutrition because marital status is related to improved individual at admission and its associated factors. well-being. In addition, there is an increase in energy intake in married couples due to change of diet and eating Conclusion and Recommendations habits (Hanson et al., 2007). Malignancy is a type of comorbidity that affects the The study revealed that the prevalence of undernutrition at occurrence of undernutrition at admission in this study. admission among Internal Medicine ward patients was Undernutrition in patients with malignancy occurs due to 26.7%. Factors associated with an increased prevalence of increased metabolic needs due to the presence of malignant undernutrition at admission were age <40 years, unmarried cells, decrease in nutrient reserve in the body, as well as status, and malignancy. Malignancy is an independent factor severe decrease of appetite. This unmet nutritional need associated with undernutrition at admission among Internal results in a decreased energy intake, impaired nutrient Medicine ward patients. absorption, and increased nutrient loss due to the presence of The authors recommend that nutritional screening should malignant cells. In addition, tumor cells can release com- be done in all patients upon admission to the hospital. pounds that cause increased protein catabolism, increased Specific population that need special attention regarding gluconeogenesis, and increased acute phase protein synthe- nutritional monitoring are young patients (age <40 years), sis. When this condition continues untreated, patients with unmarried patients, and patients with malignancy. Further Bunawan et al. 5 research must be done in multiple sites so that the findings Departments. Journal of Human Nutrition & Food Science, 3(5), 1–5. could be used widely. Correia, M. I. T. D., & Waitzberg, L. (2003). The impact of mal- nutrition on morbidity, mortality, length of hospital stay, and Author Contributions costs evaluated through a multivariate model analysis. Clinical N.C.B. conceived the study question and contributed to the study Nutrition, 22(3), 235–239. design, undertook data collection, data analysis and interpretation, Dwiyanti, D., Hadi, H., & Susetyowati. (2004). Pengaruh asupan and writing the manuscript. D.S. contributed to the study design, makanan terhadap kejadian malnutrisi di rumah sakit [Effect of undertook data collection and data analysis, and contributed to data food intake on the incidence of hospital malnutrition]. Jurnal interpretation, and supervised the manuscript writing. D.H.S.D. Gizi Klinik Indonesia, 1(1), 1–7. conceived the study question, and contributed to the study design, FOOD Trial Collaboration. (2003). Poor nutritional status on supervised data collection, data analysis and interpretation, and admission predicts poor outcomes after stroke. Stroke, 34, writing the manuscript. I.R. conceived the study question, and con- 1450–1456. tributed to the study design, supervised data collection, data analy- Fruchtenicht, A. V. G., Poziomyck, A. K., Reis, A. M. D., Galia, C. sis and interpretation, and supervised the manuscript writing. D.P. R., Kabke, G. B., & Moreira, L. F. (2018). Inflammatory and conceived the study question, and contributed to the study design, nutritional statuses of patients submitted to resection of gastro- supervised data collection, data analysis and interpretation, and intestinal tumors. Revista do Colégio Brasileiro de Cirurgiões, supervised the manuscript writing. 45(2), e1614. Ginting, H., Naring, G., Veld, V. W. M., Srisayekti, W., & Becker, Declaration of Conflicting Interests E. S. (2013). Validating the Beck-Depression Inventory-II The author(s) declared no potential conflicts of interest with respect in Indonesia’s general population and coronary heart dis- to the research, authorship, and/or publication of this article. ease patient. International Journal of Clinical and Health Psychology, 13, 235–242. Funding Hanson, K. L., Sobal, J., & Frongilo, E. A. (2007). Gender and marital status clarify associations between food insecurity and The author(s) received no financial support for the research, body weight. Journal of Nutrition, 137(6), 1460–1465. authorship, and/or publication of this article. Huong, P. T. T., Lam, N. V., Thu, N. N., Quyen, T. C., Lien, D. T. K., Anh, N. D. Q., . . . Lenders, C. (2014). Prevalence of Ethical Approval malnutrition in patients admitted to a major urban tertiary care The study protocol has been approved by Ethics and Research hospital in Hanoi, Vietnam. 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Risk Factors for Undernutrition at Admission Among Adult Hospitalized Patients at a Referral Hospital in Indonesia:

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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 grade the severity of malnutrition. The screening process can Introduction be conducted using any validated screening tool, such as Hospital malnutrition remains a global problem, with reported Nutritional Risk Screening-2002 (NRS-2002), Mini prevalence rates varying between 20.0% and 65.5% (Barker Nutritional Assessment-Short Form (MNA-SF), Malnutrition et al., 2011; Syam et al., 2018). Malnutrition is an imbalance Universal Screening Tool (MUST), and Subjective Global of nutritional state, encompassing overnutrition and undernu- Assessment (SGA) depending on the population (Cederholm trition (Barker et al., 2011). Global Leadership Initiative on et al., 2019). American Society for Parenteral and Enteral Malnutrition (GLIM) defines malnutrition as a combination Nutrition (ASPEN) recommends nutritional status screening of one phenotypic criteria (non-volitional weight loss, low within 24 hr upon admission. A patient with a risk of malnu- body mass index [BMI], or reduced muscle mass) and one etiologic criteria (reduced food intake or inflammation/dis- Universitas Indonesia-Dr Cipto Mangunkusumo National General ease burden) (Cederholm et al., 2019). This condition is Hospital, Jakarta, Indonesia related to an increased number of morbidity and mortality, Southeast Asian Minister of Education Organization Regional Centre for prolonged hospitalization, and an increased cost of care; Food and Nutrition (SEAMEO RECFON), Jakarta, Indonesia therefore, early identification of nutritional status is important Corresponding Author: for all hospitalized patients (Correia & Waitzberg, 2003). Dyah Purnamasari, Endocrinologist, Department of Internal Medicine, GLIM introduced two-step approach for diagnosing mal- Faculty of Medicine, Universitas Indonesia-Dr. Cipto Mangunkusumo nutrition in clinical practice, which is screening to identify National General Hospital, Jl. Salemba Raya no. 6, Jakarta 10430, Indonesia. population at risk followed by assessment to diagnose and Email: dyah_p_irawan@yahoo.com Creative Commons CC BY: This article is distributed under the terms of the Creative Commons Attribution 4.0 License (https://creativecommons.org/licenses/by/4.0/) which permits any use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage). 2 SAGE Open trition should be referred to a clinical nutritionist for treat- Results ment to prevent further deterioration (White et al., 2012). A total of 60 patients participated in the study between July The nutritional status at admission can affect the inci- and September 2019, with a median age of 42 (min–max: dence of worsening nutritional status during hospitalization 18–59) years. Table 1 shows subject’s characteristics. More (Zhu et al., 2017). In 2003, Feed Or Ordinary Diet (FOOD) than half of subjects were men and mostly married. Nearly study conducted a study in 18 countries and found several half of subjects were hospitalized due to acute gastrointestinal increased complications among undernourished patients at diseases such as hematemesis, melena, cholangitis, cholecys- admission, such as gastrointestinal bleeding, pneumonia, and titis, and obstructive jaundice. The mean BMI was 22.3 ± 4.7 other infectious diseases (FOOD Trial Collaboration, 2003). kg/m , and nearly a third of subjects were undernourished at To date, Indonesia has still limited data on factors related admission. Most subjects had CCI score <5. We found as to undernutrition at admission (Syam et al., 2018; Syamsiatun many as one third of subjects suffered from depression as et al., 2004). This study aims to assess the prevalence of indicated by BDI, and half of the subjects had NLR score ≥5. undernutrition at admission among Internal Medicine patients The most common comorbidity was gallstones (25%), fol- in Indonesia and its association with age, sex, marital status, lowed by hypertension (20%) and malignancy (15%). type of comorbidity, depression, Charlson Comorbidity Index Factors associated with undernutrition at admission on (CCI), and neutrophil–lymphocyte ratio (NLR). bivariate analysis were unmarried status, age ≥40 years, and malignancy as shown in Table 2. The independent variable Materials and Methods with p value <.25 from the results of bivariate analysis were unmarried status (p = .006), men gender (p = .152), CCI A cross-sectional study using consecutive sampling method score ≥ 5 (p = .074), age ≥ 40 years (p = .028), gallstones was carried out in the Internal Medicine ward at Cipto (p = .050), malignancy (p = .008), and chronic liver disease Mangunkusumo National General Hospital, Jakarta, Indonesia, (p = .192). Adjusted multivariate analysis showed that between July and September 2019. We selected patients aged malignancy was an independent predictor of undernutrition between 18 and 59 years old who were fully conscious. upon hospital admission (p = .040; odds ratio [OR] = 11.8, Pregnant patients, edema, history of diuretics use, psychiatric 95% confidence interval [CI] = [1.1, 125.7]). patients, and patients admitted for elective intervention were not included in the study. As we use NLR to assess the occur- rence of inflammation in this study, patients with a history of Discussion steroid and immunosuppressant use prior to hospitalization, HIV-AIDS, hematologic malignancies, febrile neutropenia, Hospital malnutrition remains a global problem. The preva- and post-chemoradiation patients were also not included. lence of hospital malnutrition ranged between 20.0% and Study subjects underwent a series of assessments includ- 65.5% globally (Barker et al., 2011; Syam et al., 2018), while ing demographic data, medical interviews to look for in Indonesia it is estimated that the prevalence of hospital patient’s diseases, Beck Depression Inventory (BDI)-II malnutrition accounts for 13.0% to 65.5% (Barker et al., Indonesia to detect depression (Ginting et al., 2013), BMI to 2011; Budiningsari & Hadi, 2004; Dwiyanti & Hadi, 2004; determine nutritional status, CCI to know the existence of Kusumayanti & Hadi, 2004; Syamsiatun et al., 2004). These comorbidity, and NLR. different prevalence rates might be due to various population Body weight measurements were carried out using of the subjects and the diversity of diagnostic tools used in Electronic Bed Scale Sung Sim® E543-040 series with the the studies. Malnutrition at hospital admission is related to precision of 0.1 kg. Height was determined using a conver- prolonged hospital stay and increased morbidity and mortal- sion formula of knee-height according to Paramita (2012). ity, which can lead to increased cost of care (Chermesh et al., 2 2 BMI was obtained by dividing weight (kg) by height (m ), 2015). Undernourished patients at hospital admission also and BMI <18.5 kg/m was considered as undernutrition have a higher risk of declining nutritional status during hos- according to WHO (World Health Organization, 1995). pitalization (Susetyowati et al., 2010). Therefore, it is very ® ® Statistical analysis was performed using IBM SPSS important to identify this group of patients and associated Statistics version 20. Bivariate analyses for categorical factors to prevent further deterioration of nutritional status variables were performed with chi-square test or Fisher during hospitalization. exact test as applicable. Multivariate analysis with logistic This study was conducted in Internal Medicine ward at regression backward method was performed on variables Cipto Mangunkusumo National General Hospital, which is a with p <.25 on the bivariate analysis. Statistical signifi- national referral hospital in Indonesia. This study observed cance was at p < .05. The study protocol has been approved 26.7% prevalence of undernourished subjects, which was by Ethics and Research Committee of the Faculty of similar to the results of a study conducted by Syam et al. Medicine, University of Indonesia (approval letter KET- (2018) in the same hospital, which was 22.7%. Subjects in 389/UN2.F1/ETIK/PPM.00.02/2019). our study had relatively stable medical conditions, which Bunawan et al. 3 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. Table 2. Analysis of Factors Associated With Undernutrition at Admission. Undernourished Yes No Variables n (%) n (%) 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. was different from Syam et al.’s study. This was observable In our study, factors associated with malnutrition at from the low percentage of subjects with CCI score ≥ 5 admission based on the bivariate analysis were age, marital (11.7%). The prevalence of comorbidity in our subjects was status, and malignancy. Gender was found unrelated to low (11.7%–25.0%), with gallstones as the most common undernutrition at admission. Although this is consistent comorbidity. Another study from developing countries con- with the findings of Syam et al.’s (2018) study, other stud- ducted by Huong et al. (2014) obtained the prevalence of ies reported different results (Banks et al., 2007; Chermesh undernutrition at admission as 33.3%. This might be due to et al., 2015). This indicates that the role of gender in under- the older population (52.8 ± 16.9 years) with varying degrees nutrition remains controversial upon hospital admission. of disease severity when compared to our study. We did not find any association between depression and 4 SAGE Open undernutrition at admission, which was in contrast with a malignancy would suffer from cachexia (Wulandari, 2015). study by Prasetyo et al. (2015). This study was performed Malnutrition at admission in these malignant patients could among geriatric population in a psychiatric center, there- be worsened by a decrease in nutritional status during hospi- fore leading to higher prevalence of depressive patients. talization, together with all of its outcomes. Based on a study This study found that CCI scores were not associated with conducted by Nourissat et al. (2008) as much as 8.6% of can- undernutrition at admission while Chermesh et al. (2015) cer patients were undernourished and 21.9% of these under- found that patients with CCI scores ≥ 5 were associated with nourished patients lost weight after 2 weeks. According to a 1.3 times the incidence of malnutrition at admission. This study by Susetyowati et al. (2010) using Patient Generated difference might be due to the lesser comorbidities experi- Subjective Global Assessment (PG-SGA), 86% of patients enced in our subjects, as observable from the low percentage with malignancy and malnutrition at admission suffered of patients with CCI ≥ 5 (11.7%) in our study. NLR scores from weight loss during hospitalization. Approximately one were not associated with undernutrition at admission. This is fifth of patients with malignancy died from undernutrition consistent with the results by Fruchtenicht et al. (2018) in complications when compared to the mortality by the malig- Brazil. We hypothesize that this insignificant result could be nancy itself (Wulandari, 2015). This emphasizes the needs due to the duration of the inflammatory changes which was for special attention to hospitalized patients with malignancy, not long enough to cause significant changes in nutritional especially those who have experienced undernutrition upon status. The low comorbidities status found among most of hospital admission. our subjects also contributed to a less systemic inflammation Our study showed that subjects with gallstones had lower (Miller et al., 2013). tendency to suffer from malnutrition at admission. This is in Age ≥ 40 years was associated with 80% reduction risk conformity with the risk factors for gallstones, which are of undernutrition at admission in our study. This might be female, age ≥40 years, multiparity, and obesity. The forma- due to the alteration of body composition that is associated tion of gallstones is due to the presence of certain substances with aging. Aging causes an increase in body weight with a that caused supersaturated bile. This eventually forms crys- doubled increase in fat mass in men and women during mid- tals that trap in the mucus of the gallbladder to form biliary dle age (Kuczmarski et al., 1994; Sheehan et al., 2003). This sludge, resulting in gallstones. Because 80% of gallstones increase in body weight could be influenced by reduced are cholesterol stones, these patients are strongly advised to physical activity in older age (Jakicic, 2002). However, consume diet low in cholesterol and saturated fat, restrict fats weight loss contradictorily occurs after 60 years old. A fur- intake, and lost weight (Sharma & Tandon, 2012). However, ther increase in fat mass with the main distribution in the we did not find any statistical significance between malnutri- abdominal area is followed by a decrease in fat-free mass tion at admission and gallstones (p = .05). among elderly (Sheehan et al., 2003). Our study has advantages and limitations. The advantage Our study discovered that marital status was related to of using BMI to assess nutritional status in this study is prac- undernutrition at admission. Unmarried patients had an tical and objective in nature. However, the use of BMI to increased risk of 6.3× in experiencing undernutrition at determine the nutritional status yields lesser research partici- admission. A previous study found that people who were pants due to the exclusion of patients with edema. Lately, married had heavier weight (Sobal & Rauschenbach, there are several validated tools that can address this limita- 2003). Another study had found that marital status was tion such as NRS-2002, MNA-SF, MUST, or SGA (Schueren associated with 3.3× the risk of weight gain in men within et al., 2014). This cross-sectional study design we used is not 10 years (Kahn & Williamson, 1990). This might be able to show the causal relationship between undernutrition because marital status is related to improved individual at admission and its associated factors. well-being. In addition, there is an increase in energy intake in married couples due to change of diet and eating Conclusion and Recommendations habits (Hanson et al., 2007). Malignancy is a type of comorbidity that affects the The study revealed that the prevalence of undernutrition at occurrence of undernutrition at admission in this study. admission among Internal Medicine ward patients was Undernutrition in patients with malignancy occurs due to 26.7%. Factors associated with an increased prevalence of increased metabolic needs due to the presence of malignant undernutrition at admission were age <40 years, unmarried cells, decrease in nutrient reserve in the body, as well as status, and malignancy. Malignancy is an independent factor severe decrease of appetite. This unmet nutritional need associated with undernutrition at admission among Internal results in a decreased energy intake, impaired nutrient Medicine ward patients. absorption, and increased nutrient loss due to the presence of The authors recommend that nutritional screening should malignant cells. In addition, tumor cells can release com- be done in all patients upon admission to the hospital. pounds that cause increased protein catabolism, increased Specific population that need special attention regarding gluconeogenesis, and increased acute phase protein synthe- nutritional monitoring are young patients (age <40 years), sis. When this condition continues untreated, patients with unmarried patients, and patients with malignancy. Further Bunawan et al. 5 research must be done in multiple sites so that the findings Departments. Journal of Human Nutrition & Food Science, 3(5), 1–5. could be used widely. Correia, M. I. T. D., & Waitzberg, L. (2003). The impact of mal- nutrition on morbidity, mortality, length of hospital stay, and Author Contributions costs evaluated through a multivariate model analysis. Clinical N.C.B. conceived the study question and contributed to the study Nutrition, 22(3), 235–239. design, undertook data collection, data analysis and interpretation, Dwiyanti, D., Hadi, H., & Susetyowati. (2004). Pengaruh asupan and writing the manuscript. D.S. contributed to the study design, makanan terhadap kejadian malnutrisi di rumah sakit [Effect of undertook data collection and data analysis, and contributed to data food intake on the incidence of hospital malnutrition]. Jurnal interpretation, and supervised the manuscript writing. D.H.S.D. Gizi Klinik Indonesia, 1(1), 1–7. conceived the study question, and contributed to the study design, FOOD Trial Collaboration. (2003). Poor nutritional status on supervised data collection, data analysis and interpretation, and admission predicts poor outcomes after stroke. Stroke, 34, writing the manuscript. I.R. conceived the study question, and con- 1450–1456. tributed to the study design, supervised data collection, data analy- Fruchtenicht, A. V. G., Poziomyck, A. K., Reis, A. M. D., Galia, C. sis and interpretation, and supervised the manuscript writing. D.P. R., Kabke, G. B., & Moreira, L. F. (2018). Inflammatory and conceived the study question, and contributed to the study design, nutritional statuses of patients submitted to resection of gastro- supervised data collection, data analysis and interpretation, and intestinal tumors. Revista do Colégio Brasileiro de Cirurgiões, supervised the manuscript writing. 45(2), e1614. Ginting, H., Naring, G., Veld, V. W. M., Srisayekti, W., & Becker, Declaration of Conflicting Interests E. S. (2013). 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Published: Jan 6, 2021

Keywords: BMI; hospital; Indonesia; internal medicine; undernutrition at admission

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