Prevalence of anemia and malnutrition and their association

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1 DOI /s ORIGINAL ARTICLE Prevalence of anemia and malnutrition and their association in elderly nursing home residents Sevnaz Sahin 1 Pinar Tosun Tasar 1 Hatice Simsek 2 Zeynep Çicek 3 Hulya Eskiizmirli 4 Fisun Senuzun Aykar 5 Fahri Sahin 6 Fehmi Akcicek 1 Received: 27 August 2015 / Accepted: 27 October 2015 Springer International Publishing Switzerland 2015 Abstract Purpose Malnutrition is one of the most important geriatric syndromes in the elderly. The aim of this study was to investigate the association between anemia and malnutrition in elderly nursing home residents. Materials and methods Local nursing home residents over 60 years old in the Izmir were included in the study. Blood samples were taken from study participants for hemogram, iron, ferritin, total iron-binding capacity, vitamin B12 and folic acid analysis. WHO criteria were used to define anemia. Causes of anemia were classified as iron deficiency, vitamin B12 or folic acid deficiency, anemia of chronic disease or other hematologic causes. Anemia was defined as the dependent variable and malnutrition was defined as the independent variable. Correlation between MNA scores and Hb levels was determined using Pearson correlation analysis. The slope of causality between malnutrition and anemia was determined using the v 2 test and logistic regression analysis. & Pinar Tosun Tasar pinar.tosun@gmail.com Division of Geriatrics, Department of Internal Medicine, Ege University Hospital, Izmir, Turkey Department of Healthcare, Dokuz Eylul University Hospital, Izmir, Turkey Department of Nursing, School of Health Sciences, Istanbul Arel University, Istanbul, Turkey Department of Internal Medicine, Ege University Hospital, Izmir, Turkey Faculty of Nursing, Ege University Hospital, Izmir, Turkey Division of Hematology, Department of Internal Medicine, Ege University Hospital, Izmir, Turkey Results The study included 257 elderly nursing home residents with a mean age of 78.5 ± 7.8 years. The overall prevalence of anemia was 54.9 %; 35.8 % of the study participants were at risk of malnutrition and 8.2 % were malnourished. Anemia risk was 2.12-fold higher in participants at risk of malnutrition and 5.05-fold higher in those with malnutrition. In the participants with malnutrition or malnutrition risk, the most common cause of anemia was anemia of chronic disease (57.1 and 46.5 %, respectively). Conclusion The prevalence of anemia among elderly nursing home residents is high in Turkey. Malnutrition and malnutrition risk increase the incidence of anemia. Keywords Introduction Anemia Malnutrition Elderly Geriatrics The prevalence of anemia increases with age. According to data from the World Health Organization (WHO), anemia is defined as hemoglobin (Hb) value under 12 g/dl in women and 13 g/dl in men [1]. In community-dwelling elderly individuals, anemia increases fatigue, dementia and falls and decreases mobility and life quality, while in hospitalized elderly patients it increases the incidence of delirium and thereby morbidity; in both the communitydwelling elderly and those residing in nursing homes, anemia results in higher mortality rates by exacerbating existing diseases such as heart and kidney failure [2 4]. The reported prevalence of anemia among the elderly varies between 2.9 and 61 % depending on the study population [1]. Malnutrition is one of the geriatric syndromes and is a serious problem among the elderly; it often refers to

2 insufficient nutrition. The prevalence of malnutrition is 5 10 % in elderly individuals living independently and % in elderly inpatients; this rate increases to up to 85 % in nursing home residents [5 8]. Despite the many studies in the literature that show malnutrition as a cause of anemia in children [9], studies regarding the malnutrition-anemia association in the elderly are limited [10, 11]. The aim of this study was to investigate the association between anemia and malnutrition in elderly nursing home residents of Izmir, Turkey s third largest city. Materials and methods This cross-sectional study was conducted between July and August 2012 and included residents of 7 governmental and 4 privately owned nursing homes in the Izmir metropolitan area. A total of 257 elderly individuals met the inclusion criteria and participated in the study. Criteria for inclusion were that individuals were over 60 years old, had sufficient cognitive function to complete the written informed consent form and were residents of a nursing home in the Izmir area. Exclusion criteria were age under 60 years, acute infection, active malignancy, inability to provide written informed consent due to advanced dementia, and immobility preventing the measurement of height and weight. Data regarding the study participants age, gender, duration of nursing home residency, medications used, and type and number of chronic diseases were analyzed. Participants malnutrition status was assessed using the Full Mini Nutritional Assessment (MNA). The Full MNA consists of 18 items covering the following: Anthropometric measurements (4 items concerning height, weight, body mass index (BMI), mid-arm circumference and calf circumference) Dietary habits (6 items concerning fluid and food intake, whether assistance is required for eating, etc.) Global assessment (6 items concerning level of independence, medications used, mobility, mental status, skin changes, presence of acute stressors during the previous 3 months) Subjective assessment (items concerning patient s opinions about their health and nutrition) The Full MNA yields a score between 0 and 30. Individuals with a score of 24 or over is considered to have normal nutritional status (well-nourished), scores of indicate malnutrition risk, and individuals with scores under 17 are considered malnourished [12]. Venous blood samples (1 ml from the antecubital vein) were obtained from all study participants after at least 8 h of fasting. Samples were used for hemogram (using the CELL-DYN Ruby hematology system, Abbott Laboratories, Illinois, USA), serum iron (by ferene method using the ARCHITECT c16000 clinical chemistry analyzer, Abbott Laboratories, Illinois, USA) total iron-binding capacity (by ferrozine method using the ARCHITECT c16000 analyzer), vitamin serum ferritin, vitamin B12 and folic acid level analyses (by chemiluminescent microparticle immunoassay using the ARCHITECT i200 immunoassay analyzer). The WHO criteria (Hb level under 13 g/dl for men and 12 g/dl for women) were used to diagnose anemia [1]. Causes of anemia were classified as iron deficiency, vitamin B12 or folic acid deficiency, anemia of chronic disease or other hematologic causes. For serum iron, a lower limit of 12 mg/l was used; iron deficiency was defined as transferrin saturation under 20 % and ferritin value under 45 ng/ml [13]. Lower limits for vitamin B12 and folic acid were 200 pmol/l and 4 nmol/l, respectively [14]. Anemia of chronic disease was defined as ferritin level over 100 ng/ml and transferrin saturation over 20 % [15]. Statistical analyses Data were analyzed using SPSS version 16 (IBM, New York, USA) software. Numerical variables are shown as mean ± standard deviation; categorical variables are shown as percentage and were analyzed using the v 2 test. Anemia was defined as the dependent variable and malnutrition was defined as the independent variable. Possible confounding factors were age, gender, chronic disease and medication numbers, duration of nursing home residency and education level (with or without diploma). Correlation between points earned in the Mini Nutritional Assessment (MNA) and Hb levels was determined using Pearson correlation analysis. The slope of causality between malnutrition and anemia was determined using the v 2 test and logistic regression analysis. p values B0.05 were accepted as statistically significant. According to 2012 data, there were a total of 3 nursing home residents over 60 years old living in 28 private nursing homes in Izmir. The minimum sample size required for study efficacy was 1.5 %, corresponding to a minimum of 241 nursing home residents. Ethical regulations The study was conducted in accordance with the ethical guidelines of the Helsinki Declaration and was approved by the Ege University Ethics Committee (Date and Committee Number: 12/09/2011, 11-7/63). Biochemical supplies were financed with support from the Ege University Faculty of Medicine Research Projects Sub-Commission

3 for Scientific Research Projects (BAP) (2012, Medicine 27). During the study, all participants signed a written informed consent form. Results The findings of a total of 257 elderly nursing home residents are presented. Mean age of the study group was 78.5 ± 7.8 years; 46.7 % were old old and 29.2 % were young old; 61.9 % were women. The mean duration of nursing home residency was 51.9 ± 47.2 months. Education level was primary school for 36.5 %, middle school for 17.9 % and high school diploma for 17.9 % of the participants. Mean number of chronic diseases was 2.0 ± 1.3; 88.7 % of participants had at least one chronic disease. The most common chronic disease was hypertension (HT), present in 55.6 % of participants. Mean number of medications used daily was 4.1 ± 2.8; only 8.6 % of the participants used no medications, whereas 67.3 % used three or more. Demographic data of the nursing home residents are shown in Table 1. Overall prevalence of anemia in the nursing home residents included in the study was 54.9 %. Cause of anemia was anemia of chronic disease in 57.6 %, iron deficiency in 37.8 %, hematological pathology in 12.1 %, folic acid deficiency in 7.1 % and vitamin B12 deficiency in 6.1 % of anemic participants (Table 2). By gender, 58.3 % (n = 74) of female and 50 % (n = 44) of male patients were found to be anemic, though there was no statistically significant difference in prevalence between the genders (p [ 0.05). According to age group, 41.2 % (n = 28) of young old, 56.6 % (n = 56) of old old, and 70.8 % of oldest old participants were anemic. There was a statistically significant rise in the prevalence of anemia with increasing age (p = 0.006). The prevalence of malnutrition among the study participants was 8.2 and 35.8 % were found at risk of malnutrition. By age group, the rate of malnutrition and malnutrition risk were 2.7 % (n = 2) and 32 % (n = 24) in the young old group; 8.3 % (n = 10) and 46.7 % (n = 56) in the old group; and 14.5 % (n = 9) and 53.2 % (n = 33), respectively, in the oldest old group. The increase in malnutrition and risk of malnutrition with advancing age was statistically significant (p = and p = 0.03, respectively, in the logistic regression test). Participants at risk of malnutrition had a 2.12-fold greater risk of anemia, while malnourished participants had a 5.05-fold greater anemia risk (Table 3). The most common cause of anemia in participants with malnutrition or at risk of malnutrition was anemia of chronic disease, with 57.1 and 46.5 %, respectively; the second most common cause was iron deficiency, with 28.6 and 31.8 %, respectively; there was no Table 1 Demographic characteristics of the elderly nursing home residents Parameter Result Mean age (years) 78.5 ± 7.8 Gender Female 159 (61.9 %) Male 98 (38.1 %) Age group Young old (65 74 years) 75 (29.2 %) Old old (75 84 years) 120 (46.7 %) Oldest old (C85 years) 62 (24.1 %) Education level Illiterate 29 (11.3 %) Literate 20 (7.8 %) Elementary school 94 (36.5 %) Middle school 46 (17.9 %) High school 46 (17.9 %) University 22 (8.6 %) Mean duration of nursing home residency (months) 51.9 ± 47.2 Presence of chronic disease No 29 (11.3 %) Yes 228 (88.7 %) Mean number of chronic diseases 2.0 ± 1.3 Chronic diseases HT 143 (55.6 %) Alzheimer 60 (23.3 %) DM 44 (17.1 %) COPD 22 (8.6 %) CHF 19 (7.4 %) Parkinson 12 (4.7 %) Depression 11 (4.3 %) CKF 1 (0.4 %) Malignancy 1 (0.4 %) CAD 1 (0.4 %) Medication use None 22 (8.6 %) (24.1 %) C3 173 (67.3 %) Mean number of medications used daily 4.1 ± 2.8 HT hypertension, DM diabetes mellitus, COPD chronic obstructive pulmonary disease, CHF congestive heart failure, CKF chronic kidney failure, CAD coronary heart disease Table 2 Causes of anemia Pathology n (%) Anemia of chronic disease 68 (57.6) Iron deficiency anemia 45 (37.8) Hematological pathologies 15 (12.1) Folic acid deficiency 15 (7.1) B12 deficiency 13 (6.1)

4 Table 3 Presence of malnutrition and anemia Presence of anemia Crude OR (95 % CI) p Adjusted OR (95 % CI) p No malnutrition Risk of malnutrition 2.68 ( ) ( ) Malnutrition ( ) ( ) Adjusted for age, number of chronic diseases, number of medications, gender, and education level statistically significant difference according to nutritional status (p [ 0.05). Adjustments for age, number of chronic diseases, number of medications, gender, and education level were made during analysis. Discussion The prevalence of anemia was found to be 54.9 % among the elderly nursing home residents in this study. Anemia of chronic disease was the most common cause of anemia (57.6 %). Overall, 8.2 % of the study participants were determined to be malnourished, while 35.8 % were assessed as at risk of malnutrition. The risk of anemia was fold higher in participants at risk of malnutrition and fold higher in those with malnutrition. The most frequent causes of anemia in those at risk of malnutrition and those with malnutrition were anemia of chronic disease and iron deficiency anemia. Anemia prevalence varies depending on environmental factors and the population and location being studied. The prevalence of anemia was found to be 18.6 % in a study of community-dwelling elderly in Brazil [16], 11.8 % in Italy [17], 10.6 % in a study conducted in the United States [18], 4.3 % in Germany [19], and 7.3 % in Turkey [20]. In the literature, reports of anemia prevalence in the nursing home residents of Brazil, the United States and Italy were 29, 57 and 63 %, respectively [21 23]. Similar to the results of Reardon et al., the overall anemia prevalence in our study was 54.9 %. The higher rate of anemia in nursing home residents compared to the community-dwelling elderly population has been explained by the overall poorer condition and more frequent comorbidities of nursing home residents. In the present study, anemia prevalence increased with age, reaching 70 % in the oldest old group. Several mechanisms have been implicated in the age-related increase in anemia prevalence. Despite increased need for erythropoietin in old age, serum erythropoietin levels decrease with advancing age; pro-inflammatory cytokines increase with age, leading to erythropoietin resistance; and levels of hepcidin increase secondary to inflammation, inhibiting erythrocyte production [24]. The results of our study are consistent with those reported in the literature [18, 25]. There are contradictory studies in the literature regarding the effect of gender on anemia. Some studies have shown a higher prevalence of anemia in older men. Other proposed explanations for the higher anemia prevalence in males include decreases in testosterone levels in males and the lack of menstruation-related decreases in hemoglobin level in postmenopausal females [26, 27]. However, Guralnik et al. found no significant association between gender and anemia prevalence [28]. Similarly, the results of our study indicated no significant association between anemia prevalence and gender. It is reported in the literature that the rate of anemia rises with increasing age [28]. Consistent with these findings, we found that anemia prevalence increased with age. In the current study, the most common cause of anemia was anemia of chronic disease (ACD), occurring at a rate of 57.6 %. In the literature, the prevalence of ACD has been reported as 19.7 % in a NHANES III study of community-dwelling individuals [29], 17.4 % in a study of elderly nursing home residents in Italy [30], 9.8 % in community-dwelling elderly in the USA [31], 24.4 % in community-dwelling individuals in Italy [32], and 62.1 % among elderly outpatient clinic applicants and hospitalized patients in Australia [33]. The pathogenesis of ACD is multifactorial; the release of cytokines such as TNF-alpha, IL-6, IL-1, and macrophage migration inhibitory factor (MIF) during chronic disease stimulates hepcidin production and reduces iron absorption by the intestines and iron recycling by macrophages [34]. Our study has importance in terms of determining the anemia subtypes found in Turkey. Similar to the results of Bach et al. s Australian study [33], we found the prevalence of ACD quite high. Our findings may be attributable to the high number of chronic diseases among our study participants. The reported prevalence of iron deficiency anemia (IDA) in older people varies between 2.5 and 30 %. IDA can be caused by blood loss, malignancy, or decreases in iron intake or iron absorption. [35, 36]. In a Turkish study including 1388 elderly people conducted by Coban et al., anemia was found in 25 % of the participants and IDA accounted for one-third of the anemia cases [37]. In Turkey, the IDA prevalence in community-dwelling elderly residents of Ankara was reported to be 7.1 % [20], while a study of community-dwelling elderly in the western Black

5 Sea region indicated a prevalence of 40.5 % [38]. Our finding in the current study of a 37.8 % IDA prevalence is consistent with that of Yildizhan et al. However, we did not investigate the sources of the IDA in our population, which is one of the limitations of our study. In the literature, the rate of bone marrow dysplasia in the elderly ranges from 5 to 15 % [39, 40]. Consistent with the literature, in this study we found hematological pathology in 12 % of our subjects. Unexplained anemia is among the causes of anemia found in the literature. The pathogenesis of unexplained anemia involves age-related increases in pro-inflammatory cytokines levels, myelodysplasia, decreased androgen levels, and lower bone marrow proliferative capacity [18, 32]. Contrary to the literature, unexplained anemia was not among the anemia causes found in the current study; this is because a peripheral blood smear was conducted, and abnormalities in the smear were diagnosed as myelodysplastic syndrome by an experienced hematologist. Vitamin B12 deficiency increases with aging [41]; depending on the cut-off values used for vitamin B12 level, the prevalence of deficiency ranges from 5 to 40 % [41 44]. Prevalence of vitamin B12 deficiency is 5 15 % with a cut-off value of 200 pmol/l [43 45]; this rate increases to 40.5 % using a cut-off value of 350 pmol/l and analyzing methylmalonic acid and homocysteine levels [41, 42]. In the current study, the cut-off value was 200 pmol/l and the rate of vitamin B12 deficiency was 6.1 %, similar to other studies [43]. However, one of the limitations of our study was not analyzing serum methylmalonic acid and homocysteine levels. In the current study, we found folic acid deficiency at a rate of 7.1 %. Other studies in the literature report folic acid deficiency at 21 % [46, 47]. Guralnik et al. classified anemia caused by vitamin B12 and folic acid deficiency together as nutrient deficiency anemia, which they found at a rate of 14 % [18]. In a Turkish study, Yildirim et al. found the prevalence of folic acid deficiency to be 1 % [20]. The reason for the differences between the results may be associated with the use of different diagnostic criteria. Malnutrition, one of the geriatric syndromes, is common among nursing home residents; the prevalence of malnutrition varies greatly according to the population and nutritional status screening method used. Recent studies of elderly nursing home residents have found malnutrition frequencies of 19.2 % in the Czech Republic [48], 17.7 % in Switzerland [49], and 11.9 % in a Turkish study including a total of 14 centers from 3 provinces [44]. Similar to the study conducted by Cankurtaran et al., we detected malnutrition at a rate of 8.2 % in the elderly nursing home residents in this study. Studies have shown that anemia occurs more frequently in malnourished children [50]; however, there are few studies demonstrating the relationship between malnutrition and anemia in the elderly, which adds value to the current study. We found that the frequency of anemia increased 5.05-fold in the presence of malnutrition and 2.12-fold in those at risk of malnutrition. Earlier studies showed a link between low albumin levels and anemia. It has also been shown that malnutrition results in decreased albumin synthesis in the liver and lower levels of serum proteins like hemoglobin [10, 11]. An experimental study comparing malnourished rats to those with normal nutrition showed that insufficient erythropoiesis may cause anemia in malnourished rats, without iron or erythropoietin deficiency [51]. A limitation of this study is that we were unable to investigate albumin, prealbumin and lipids levels; evaluation of these determinants of malnutrition is necessary to establish causation between anemia and malnutrition. Another limitation is that homocysteine and methylmalonic acid levels were not assessed in cases of vitamin B12 and folic acid deficiency. One of the other limitations of our study is that serum TSH and vitamin B6 levels, which may also lead to anemia, were not evaluated. The strengths of this study are that it is one of the only studies investigating the prevalence and causes of anemia in Turkey, and it is the first study to demonstrate the anemia-malnutrition association in Turkish nursing home residents. In conclusion, the prevalence of anemia among nursing home residents is high. Malnutrition and malnutrition risk increase the incidence of anemia. Similar studies are needed to expand our data regarding anemia in the elderly population of Turkey. 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