e-spen, the European e-journal of Clinical Nutrition and Metabolism

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1 e-spen, the European e-journal of Clinical Nutrition and Metabolism 5 (2010) e272ee276 Contents lists available at ScienceDirect e-spen, the European e-journal of Clinical Nutrition and Metabolism journal homepage: Original Article Improvement in the nutritional status of very elderly stroke patients who received long-term complete tube feeding Hitoshi Obara a, *, Yasuka Tomite b, Mamoru Doi c a Department of Nutrition Management, National Hospital Organization, Yamagata National Hospital, Yamagata, Japan b Department of Nutrition Management, National Hospital Organization, Kamaishi National Hospital, Iwate, Japan c Department of Rehabilitation, National Hospital Organization, Kamaishi National Hospital, Iwate, Japan article info summary Article history: Received 4 February 2010 Accepted 23 September 2010 Keywords: Malnutrition Albumin Long-term complete tube feeding Stroke Very elderly patients Background & aims: Elderly patients who receive enteral nutrition after stroke are at a high risk of malnutrition. However, there are few investigations of the changes in the nutritional status of very elderly tube-fed patients in the long-term. We aimed to clarify the improvement in the nutritional status of very elderly patients who receive long-term complete tube feeding after stroke. Methods: Our subjects were 68 elderly bedridden patients who received complete enteral nutrition after stroke. All subjects had hypoalbuminemia and low body weight. The subjects were divided into the Elderly group (n ¼ 37) and the Very elderly group (n ¼ 31). Their nutritional indices were measured at the time of admission, and at 6 and 12 months after admission. Changes in the nutritional indices of each group were assessed. Results: In both groups, the albumin, prealbumin, total cholesterol, and hemoglobin levels and body mass index, mid-arm circumference, and triceps skinfold thickness after 12 months were significantly higher than baseline levels. There was no significant difference between the C-reactive protein level and midupper-arm muscle circumference at baseline and after 12 months. The raise in albumin and prealbumin levels were significantly higher in the Elderly group as compared with in the Very elderly group. However, there were no significant differences in the change in other biochemical and anthropometric parameters between the Elderly and Very elderly groups. The BMI in both groups improved to within the normal range. However, the serum albumin levels in both groups did not improve to within the normal range. Both groups showed a mild inflammatory response during the study period. Albumin and prealbumin levels were negatively associated with age. Conclusions: Long-term complete tube feeding after stroke is effective for improving the nutritional status of very elderly patients. Both in the elderly and in the very elderly patients, most of the biochemical parameters and anthropometric parameters improved. However, the change in albumin levels differed between elderly patients and very elderly patients, probably because albumin levels are influenced by aging. In addition, it was difficult to improve the low serum albumin levels of bedridden elderly patients who exhibited an inflammatory response to within the normal range. Especially, in the very elderly patients, serum albumin levels were hard to reflect improvement of malnutrition. Ó 2010 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved. 1. Introduction The nutritional status of stroke patients can worsen easily. 1e3 The reported prevalence of malnutrition after acute stroke is 26%e 49%. 4e6 In fact, in long-term care wards and nursing homes that house many stroke patients, the prevalence of malnutrition is 25%e 45%. 7e9 Malnutrition depresses immunity and increases the risk of * Corresponding author. Tel.: þ ; fax: þ address: hitoshi@yamagata.hosp.go.jp (H. Obara). infection. 10e12 Wound healing is also delayed. 13 In addition, malnutrition affects serum albumin levels, which are related to the outcomes of rehabilitation. 14,15 It has been reported that malnutrition is associated with increased mortality and complications. 16,17 Malnutrition also affects treatment outcomes and increases medical expenses. 18,19 Therefore, managing the nutritional status of stroke patients is extremely important. Malnutrition develops in stroke patients because of various causes, including dysphagia, tube feeding, bedridden state, aspiration pneumonia, longer duration of hospitalization, and /$36.00 Ó 2010 European Society for Clinical Nutrition and Metabolism. Published by Elsevier Ltd. All rights reserved. doi: /j.eclnm

2 H. Obara et al. / e-spen, the European e-journal of Clinical Nutrition and Metabolism 5 (2010) e272ee276 e273 aging. 7,9,20e22 Decline in the chewing and swallowing function by aging decreases dietary intake, and contributes to the development of malnutrition. 7 Dysphagia is a well-known risk factor for malnutrition in stroke patients. Aspiration pneumonia because of dysphagia worsens nutritional status. 22 Further, the nutritional status of stroke patients fed via a tube is poorer than that of stroke patients fed orally. 23,24 Malnutrition has been associated with longer duration of hospitalization and decrease in daily life activities. 21,22,25 Further since serum albumin levels decrease with age, the prevalence of hypoalbuminemia increases with age. 26,27 After a stroke, patients with severe dysphagia are provided complete enteral nutrition via a nasogastric tube or percutaneous endoscopic gastrostomy. There are several reports on the nutritional status of elderly patients who have received long-term tube feeding. The prevalence of malnutrition among tube-fed patients is higher than among orally-fed patients. 23 Although the body weight tube-fed patients is in the normal range, they have low serum albumin concentrations. 21,28 Many elderly patients who receive long-term tube feeding develop hypoalbuminemia despite being provided sufficient calories through an enteral formula. 23,29 However, enteral nutrition improves the nutritional indices of undernourished elderly patients. 30,31 Unfortunately, few studies have investigated the changes in the nutritional status of very elderly tube-fed patients in the long-term. We believe that there is inadequate information on the improvement in the nutritional status of very elderly patients receiving long-term enteral nutrition. Therefore, in this study, we assessed the changes in the nutritional indices of elderly and very elderly patients in order to clarify the improvements in their nutritional status following long-term complete tube feeding after stroke. 2. Methods 2.1. Subjects This was a prospective study with a 1-year follow-up period. Subjects were admitted to the geriatric stroke rehabilitation wards of Kamaishi National Hospital between January 2005 and December The study population comprised patients aged more than 65 years who had been bedridden, had hypoalbuminemia and low body weight, and had received enteral nutrition after stroke because of severe dysphagia. All subjects were provided complete enteral nutrition via a nasogastric tube. Throughout the study period, all subjects continued to receive complete enteral nutrition. Subjects were divided into the Elderly group (n ¼ 37) and the Very elderly group (n ¼ 31). The characteristics of the Elderly group and the Very elderly group are provided in Table 1. The Elderly group comprised 14 men and 23 women aged less than 85 years, with a mean age of years Table 1 Characteristics of the Elderly group and the Very elderly group. Elderly group (n ¼ 37) Very elderly group (n ¼ 31) Gender (%) Male Female Mean age (years) Mean period after stroke (months) Stroke types (%) Cerebral infarction Intracerebral hemorrhage Subarachnoid hemorrhage Mean SD or %. (mean standard deviation (SD)). The age range of this group was 65e84 years. The Very elderly group comprised 10 men and 21 women aged more than 85 years, with a mean age of years (mean SD). The age range of this group was 85e96 years. Patients diagnosed with renal dysfunction, liver dysfunction, edema, and dehydration were excluded from the study. In addition, patients who progressed to oral feeding (6 patients) or died (20 patients) before the 1-year follow-up was complete were excluded from the study. This study was conducted in compliance with the principles of the Declaration of Helsinki and approved by the ethics committee of Kamaishi National Hospital. Informed consent was obtained from the patients or their families Nutritional status assessment Nutritional indices were measured at the time of admission and at 6 and 12 months after admission. The rate of improvement in hypoalbuminemia and low body weight was determined at 6 and 12 months after admission. Nutritional indices were assessed on the basis of biochemical data, anthropometric data, and nutritional intake. Blood samples were drawn after an overnight fast. Fasting blood samples were obtained for determining albumin, prealbumin, C-reactive protein, total cholesterol, and hemoglobin levels. The albumin levels was measured using the bromocresol green method; the prealbumin levels was measured using nephelometry; the C-reactive protein levels was measured using the turbidimetric immunoassay; and the total cholesterol levels was measured using the enzymatic method. The hemoglobin levels was measured using an automated blood cell counter. Patients were diagnosed with hypoalbuminemia if they had an albumin level of less than 3.5 g/dl. 32 Height, body weight, mid-arm circumference (AC), and triceps skinfold thickness (TSF) were measured. AC was measured with a flexible tape measure, and TSF was measured with a skinfold caliper. AC and TSF were measured in triplicate. Body mass index (BMI) was calculated using height and weight data, and the mid-upper-arm muscle circumference (AMC) was calculated using AC and TSF data. Patients were diagnosed as being underweight if their BMI was less than 20 kg/m Daily nutritional intake was calculated based on the total nutrition intake over 5 days. Energy and protein intake were calculated from the amount of enteral formula received by each patient. Energy and protein intake were expressed in terms of kilocalories per kg and per day. In this study, one type of enteral formula was prescribed. The nutritional composition of the enteral formula per 1000 ml was as follows: 1000 kcal energy, 50 g protein, 22 g fat, and 147 g carbohydrate Statistical analysis Data were presented as mean SD and analyzed using SPSS (version 14.0J; SPSS Co. Tokyo, Japan). The unpaired t-test was used to compare nutritional indices at the time of admission between the Elderly and Very elderly groups. The paired t-test was used to compare nutritional indices of each group between the baseline and after 12 months. Two-way repeated measures ANOVA was used to compare the 2 groups (months group) in terms of change in all nutritional indices. Pearson s correlation coefficients were used to assess the relationship between age and nutritional indices after 12 months for all subjects. P < 0.05 was considered statistically significant. 3. Results A comparison of the nutritional indices at the time of admission is shown in Table 2. There was no significant difference in all biochemical parameters between the Elderly and Very elderly

3 e274 H. Obara et al. / e-spen, the European e-journal of Clinical Nutrition and Metabolism 5 (2010) e272ee276 Table 2 Comparison of the nutritional indices at the time of admission. Elderly group (n ¼ 37) Very elderly group (n ¼ 31) Albumin (g/dl) Prealbumin (mg/dl) Total cholesterol (mg/dl) Hemoglobin (g/dl) C-reactive protein (mg/dl) Height (cm) * Body weight (kg) ** BMI (kg/m 2 ) AC (cm) TSF (mm) AMC (cm) Mean SD. Unpaired t-test. *P < 0.05, **P < groups. Height and body weight in the Very elderly group were significantly lower than those in the Elderly group. However, there were no significant differences in BMI between the Elderly and Very elderly groups. Improvements in biochemical and anthropometric parameters are shown in Table 3and 4. Both in the Elderly and in the Very elderly group, most of the biochemical parameters (except CRP) and anthropometric parameters (except AMC) increased. Two-way repeated measures ANOVA was used to compare the 2 groups in terms of change in all nutritional indices; the comparison is shown in Table 5. The raise in albumin and prealbumin levels were significantly higher in the Elderly group as compared with in the Very elderly group (two-way repeated measures ANOVA, months group). There were no significant differences in the change in total cholesterol, hemoglobin, and C-reactive protein levels between the Elderly and Very elderly groups (two-way repeated measures ANOVA, months group). Similarly, there were no significant differences in the change in BMI, AC, TSF, and AMC between the Elderly and Very elderly groups (two-way repeated measures ANOVA, months group). Daily nutritional intake data are as follows. In the Elderly group, energy intake at baseline and after 12 months were kcal/ day ( kcal/kg/day), kcal/day ( kcal/ kg/day), respectively. Protein intake at baseline and after 12 months were g/day ( g/kg/day), g/day ( g/kg/day), respectively. In the Very elderly group, energy intake at baseline and after 12 months were kcal/day ( kcal/kg/day), kcal/day ( kcal/kg/ day), respectively. Protein intake at baseline and after 12 months Table 3 Improvements in biochemical parameters. Baseline 6 months 12 months Albumin (g/dl) Elderly group *** Very elderly group ** Prealbumin (mg/dl) Elderly group *** Very elderly group ** Total cholesterol (mg/dl) Elderly group ** Very elderly group ** Hemoglobin (g/dl) Elderly group *** Very elderly group * C-reactive protein (mg/dl) Elderly group Very elderly group Mean SD. Paired t-test (Baseline vs 12 months). *P < 0.05, **P < 0.01, ***P < Table 4 Improvements in anthropometric parameters. Baseline 6 months 12 months BMI (kg/m 2 ) Elderly group *** Very elderly group *** AC (cm) Elderly group *** Very elderly group *** TSF (mm) Elderly group *** Very elderly group *** AMC (cm) Elderly group Very elderly group Mean SD. Paired t-test (Baseline vs 12 months). ***P < were g/day ( g/kg/day), g/day ( g/kg/day), respectively. Both in the elderly and in the very elderly group, there were no significant differences in energy intake and protein intake at baseline and after 12 months. The relationships between age and nutritional indices after 12 months for all subjects are shown in Table 6. Albumin and prealbumin levels were negatively associated with age, and the correlation coefficients for these associations were 0.4 or less. 4. Discussion In this study, we assessed the changes in the nutritional indices of elderly and very elderly patients in order to clarify the improvement in the nutritional status of very elderly patients who receive long-term complete tube feeding after stroke. With regard to the improvement in the nutritional status of the Very elderly group, the albumin, prealbumin, total cholesterol, and hemoglobin levels and BMI, AC, and TSF after 12 months were significantly higher than baseline levels. In particular, the BMI improved to within the normal range. Thus, we conclude that long-term enteral nutrition improved the nutritional status of patients in the Very elderly group. The Elderly group had results similar to those of the Very elderly group. It is reported that the nutritional indices of undernourished elderly patients improve after enteral nutrition. 30,31 Further, the BMI of tube-fed patients is in the normal range. 24 Our study yielded similar results. Therefore, long-term complete enteral nutrition may be effective in improving the nutritional status of very elderly patients. In this study, the nutritional status of the Elderly and Very elderly groups improved after 1 year. However, the raise in albumin and Table 5 Two-way repeated measures ANOVA of comparison to 2 groups in terms of all nutritional indices. Nutritional indices p-value Albumin 0.011* Prealbumin 0.040* Total cholesterol Hemoglobin C-reactive protein BMI AC TSF AMC Mean SD. Two-way repeated measures ANOVA (months group). *P < 0.05.

4 H. Obara et al. / e-spen, the European e-journal of Clinical Nutrition and Metabolism 5 (2010) e272ee276 e275 Table 6 Relationships between age and nutritional indices after 12 months for all subjects. Age p-value Albumin <0.001*** Prealbumin <0.001*** Total cholesterol Hemoglobin * C-reactive protein BMI AC * TSF AMC Data are presented as the correlation coefficients. *P < 0.05, ***P < prealbumin levels were significantly higher in the Elderly group as compared with in the Very elderly group. Albumin is the most abundant serum protein synthesized in the liver, and prealbumin is a rapid turnover protein synthesized in the liver. Malnourished individuals have low levels of albumin and prealbumin. 34,35 In addition, in the elderly, the serum albumin level decreases with age. 27,36 Further, the serum albumin levels tend to decrease after 70 years of age. 37 In this study, albumin and prealbumin levels at 12 months after admission were negatively associated with age. It has been suggested that albumin and prealbumin levels were significantly different between the Elderly and Very elderly groups because the serum albumin levels are influenced by aging. The BMI of patients in both groups improved to within the normal range. However, their serum albumin levels did not improve to within the normal range. The serum albumin levels of healthy elderly persons, on the other hand, are within the normal range. 26 We believe that the albumin levels were low because of the following reason. In this study, all subjects were bedridden as a result of stroke and had low AMC levels. Therefore, skeletal muscle mass was decreasing in both the groups. Serum albumin levels are associated with skeletal muscle mass in the elderly. 38,39 Consequently, patients experiencing muscle loss have low albumin levels. 40 Further, the inflammatory response curbs the synthesis of albumin in the liver, and the serum albumin levels decrease in the presence of an inflammatory response. 41 The C- reactive protein is an acute-phase protein synthesized during inflammation and is used as an inflammation marker. 42 Both groups in this study showed a mild inflammatory response during the study period. It has been reported that patients with high levels of C-reactive protein have low levels of albumin. 28 In addition, the serum albumin level in the elderly decreases with age. 37 We believe that because of the bedridden status, inflammatory response and aging the serum albumin levels of our subjects did not improve to within the normal range. Especially, in the very elderly bedridden patients who received long-term complete tube feeding, serum albumin levels were hard to reflect improvement of malnutrition. In conclusion, long-term complete tube feeding after stroke is effective for improving the nutritional status of very elderly patients. Both in the elderly and in the very elderly patients, most of the biochemical parameters and anthropometric parameters improved. However, the change in albumin levels differed between elderly patients and very elderly patients, probably because albumin levels are influenced by aging. In addition, it was difficult to improve the low serum albumin levels of bedridden elderly patients who exhibited an inflammatory response to within the normal range. Especially, in the very elderly patients, serum albumin levels were hard to reflect improvement of malnutrition. Conflict of interest The authors have no conflict of interest. Statement of authorship All authors made significant contributions to the study s conception and design, acquisition of data, analysis of the data, and drafting of the manuscript. All authors have read and approved the final manuscript. Acknowledgments We appreciate the cooperation of the patients and their families. References 1. Chai J, Chu FC, Chow TW, Shum NC. Prevalence of malnutrition and its risk factors in stroke patients residing in an infirmary. Singapore Med J 2008;49: 290e6. 2. Hamidon BB, Nabil I, Raymond AA. Risk factors and outcome of dysphagia after an acute ischaemic stroke. Med J Malaysia 2006;61:553e7. 3. Axelsson K, Asplund K, Norberg A, Eriksson S. Eating problems and nutritional status during hospital stay of patients with severe stroke. J Am Diet Assoc 1989;89:1092e6. 4. Brynningsen PK, Damsgaard EM, Husted SE. Improved nutritional status in elderly patients 6 months after stroke. J Nutr Health Aging 2007;11:75e9. 5. Dávalos A, Ricart W, Gonzalez-Huix F, Soler S, Marrugat J, Molins A, et al. Effect of malnutrition after acute stroke on clinical outcome. Stroke 1996;27: 1028e Finestone HM, Greene-Finestone LS, Wilson ES, Teasell RW. Malnutrition in stroke patients on the rehabilitation service and at follow-up: prevalence and predictors. Arch Phys Med Rehabil 1995;76:310e6. 7. Suominen M, Muurinen S, Routasalo P, Soini H, Suur-Uski I, Peiponen A, et al. Malnutrition and associated factors among aged residents in all nursing homes in Helsinki. Eur J Clin Nutr 2005;59:578e Compan B, di Castri A, Plaze JM, Arnaud-Battandier F. Epidemiological study of malnutrition in elderly patients in acute, sub-acute and long-term care using the MNA. J Nutr Health Aging 1999;3:146e Keller HH. Malnutrition in institutionalized elderly: how and why? J Am Geriatr Soc 1993;41:1212e Paillaud E, Herbaud S, Caillet P, Lejonc JL, Campillo B, Bories PN. Relations between undernutrition and nosocomial infections in elderly patients. Age Ageing 2005;34:619e Brundtland GH. Nutrition and infection: malnutrition and mortality in public health. Nutr Rev 2000;58:S1e Woodward B. Protein, calories, and immune defenses. Nutr Rev 1998;56:S84e Mathus-Vliegen EM. Old age, malnutrition, and pressure sores: an ill-fated alliance. J Gerontol A Biol Sci Med Sci 2004;59:355e Finestone HM, Greene-Finestone LS, Wilson ES, Teasell RW. Prolonged length of stay and reduced functional improvement rate in malnourished stroke rehabilitation patients. Arch Phys Med Rehabil 1996;77:340e Aptaker RL, Roth EJ, Reichhardt G, Duerden ME, Levy CE. Serum albumin level as a predictor of geriatric stroke rehabilitation outcome. Arch Phys Med Rehabil 1994;75:80e Martineau J, Bauer JD, Isenring E, Cohen S. Malnutrition determined by the patient-generated subjective global assessment is associated with poor outcomes in acute stroke patients. Clin Nutr 2005;24:1073e Gariballa SE, Sinclair AJ. Assessment and treatment of nutritional status in stroke patients. Postgrad Med J 1998;74:395e Reilly Jr JJ, Hull SF, Albert N, Waller A, Bringardener S. Economic impact of malnutrition: a model system for hospitalized patients. JPEN 1988;12:371e Gallagher-Allred CR, Voss AC, Finn SC, McCamish MA. Malnutrition and clinical outcomes: the case for medical nutrition therapy. J Am Diet Assoc 1996;96: 361e Sullivan DH, Walls RC. Impact of nutritional status on morbidity in a population of geriatric rehabilitation patients. J Am Geriatr Soc 1994;42:471e Challa S, Sharkey JR, Chen M, Phillips CD. Association of resident, facility, and geographic characteristics with chronic undernutrition in a nationally represented sample of older residents in U.S. nursing homes. J Nutr Health Aging 2007;11:179e Lugger KE. Dysphagia in the elderly stroke patient. J Neurosci Nurs 1994;26:78e Okada K, Yamagami H, Sawada S, Nakanishi M, Tamaki M, Ohnaka M, et al. The nutritional status of elderly bed-ridden patients receiving tube feeding. J Nutr Sci Vitaminol 2001;47:236e Leibovitz A, Sela BA, Habot B, Gavendo S, Lansky R, Avni Y, et al. Homocysteine blood level in long-term care residents with oropharyngeal dysphagia: comparison of hand-oral and tube-enteral-fed patients. JPEN 2002;26:94e Van Nes MC, Herrmann FR, Gold G, Michel JP, Rizzoli R. Does the mini nutritional assessment predict hospitalization outcomes in older people? Age Ageing 2001;30:221e6.

5 e276 H. Obara et al. / e-spen, the European e-journal of Clinical Nutrition and Metabolism 5 (2010) e272ee Gom I, Fukushima H, Shiraki M, Miwa Y, Ando T, Takai K, et al. Relationship between serum albumin level and aging in community-dwelling self-supported elderly population. J Nutr Sci Vitaminol 2007;53:37e Greenblatt DJ. Reduced serum albumin concentration in the elderly: a report from the Boston Collaborative Drug Surveillance Program. J Am Geriatr Soc 1979;27:20e Obara H, Tomite Y, Doi M. Serum trace elements in tube-fed neurological dysphagia patients correlate with nutritional indices but do not correlate with trace element intakes: case of patients receiving enough trace elements intake. Clin Nutr 2008;27:587e Leibovitz A, Sharon-Guidetti A, Segal R, Blavat L, Peller S, Habot B. CD4 lymphocyte count and CD4/CD8 ratio in elderly long-term care patients with oropharyngeal dysphagia: comparison between oral and tube enteral feeding. Dysphagia 2004;19:83e Abitbol V, Selinger-Leneman H, Gallais Y, Piette F, Bouchon JP, Piera JB, et al. Percutaneous endoscopic gastrostomy in elderly patients. A prospective study in a geriatric hospital. Gastroenterol Clin Biol 2002;26:448e Vetta F, Gianni W, Ronzoni S, Donini LM, Palleschi L, Peppe T, et al. Role of aging in malnutrition and in restitution of nutritional parameters by tube feeding. Arch Gerontol Geriatr 1996;22:599e Shimetani N. Plasma protein. Nippon Rinsho 2004;62:203e Volkert D, Berner YN, Berry E, Cederholm T, Coti Bertrand P, Milne A, et al. ESPEN guidelines on enteral nutrition: geriatrics. Clin Nutr 2006;25:330e Yanai M. Transthyretin (prealbumin. Nippon Rinsho 2004;62:209e Lefèvre P, Badetti C. Metabolism of albumin. Ann Fr Anesth Reanim 1996;15: 464e Salive ME, Cornoni-Huntley J, Phillips CL, Guralnik JM, Cohen HJ, Ostfeld AM, et al. Serum albumin in older persons: relationship with age and health status. J Clin Epidemiol 1992;45:213e Cooper JK, Gardner C. Effect of aging on serum albumin. J Am Geriatr Soc 1989;37:1039e Nakamura H, Fukushima H, Miwa Y, Shiraki M, Gomi I, Saito M, et al. A longitudinal study on the nutritional state of elderly women at a nursing home in Japan. Intern Med 2006;45:1113e Visser M, Kritchevsky SB, Newman AB, Goodpaster BH, Tylavsky FA, Nevitt MC, et al. Lower serum albumin concentration and change in muscle mass: the health, aging and body composition study. Am J Clin Nutr 2005;82:531e Baumgartner RN, Koehler KM, Romero L, Garry PJ. Serum albumin is associated with skeletal muscle in elderly men and women. Am J Clin Nutr 1996;64:552e Rothschild MA, Oratz M, Schreiber SS. Serum albumin. Hepatology 1988;8: 385e Shimetani N. C-reactive protein. Nippon Rinsho 2004;62:212e6.

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