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Serum levels of vitamins A, C, and E in persons with chronic spinal cord injury living in the community1
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Serum Levels of Vitamins A, C, and E in Persons With Chronic Spinal Cord Injury Living in the Community Robabeh M. Moussavi, PhD, Hector M. Garza, BS, Susan G. Eisele, BS, Gladys Rodriguez, PhD, Diana H. Rintala, PhD ABSTRACT. Moussavi RM, Garza HM, Eisele SG, Rodriguez G, Rintala DH. Serum levels of vitamins A, C, and E in persons with chronic spinal cord injury living in the community. Arch Phys Med Rehabil 2003;84:1061-7. Objectives: To determine serum levels of vitamins A, C, and E among individuals with spinal cord injury (SCI) living in the community, to compare these levels with general population norms, and to assess their association with demographic and injury-related data (age at onset, time since onset, level and completeness of injury), function, nutritional behaviors, and health status. Design: Descriptive and correlational. Setting: General community. Participants: A total of 110 adults (ⱖ18y) with traumatic SCI of at least 2 years in duration living within a 13-county area in Texas. Interventions: Not applicable. Main Outcome Measures: Demographic information, age at onset, time since onset, American Spinal Injury Association (ASIA) total motor index score, ASIA impairment score, assay of serum vitamins, FIM™ instrument motor items, HealthPromoting Lifestyle Profile nutrition subscale, Medical Outcomes Study 36-Item Short-Form Health Survey general health subscale, and pressure ulcer occurrence in past 12 months. Results: Many (16%–37%) of the participants had serum levels below the reference range for each vitamin. Being older at onset or less impaired was associated with higher serum vitamin A levels. Higher levels of serum vitamin A also were related to better function and health status and with not having a pressure ulcer within the past 12 months. Being older or older at onset was associated with higher serum levels of vitamin E. No relationships with vitamin C were found. Conclusions: Vitamin levels may be related to function, general health, and pressure ulcer incidence in persons with SCI. Further study is needed to determine effective interventions to improve vitamin levels and determine the effect of such improvements on overall health and rehabilitation outcomes. Key Words: Health behavior; Health status; Rehabilitation; Spinal cord injuries; Vitamins. © 2003 by the American Congress of Rehabilitation Medi-
From the Department of Physical Medicine and Rehabilitation, Baylor College of Medicine (Moussavi, Garza, Eisele, Rodriguez, Rintala), TIRR (Garza, Rintala), and Center of Excellence on Healthy Aging with Disabilities, Veterans Affairs Medical Center (Rintala), Houston, TX. Supported by the National Institutes of Health (grant no. 5-T32-HD-07465-05), and National Institute on Disability and Rehabilitation Research, Rehabilitation Research and Training Center on Community Integration for Individuals with Spinal Cord Injury (grant no. H133B40011-95). The opinions expressed in this article are those of the grantee and do not necessarily reflect those of the US Department of Education. Presented in part at the Second National Department of Veteran Affairs Rehabilitation Research and Development Conference, February 2000, Arlington, VA. Reprint requests to Diana H. Rintala, PhD, VAMC, 153, 2002 Holcombe Blvd, Houston, TX 77030, e-mail: [email protected]. 0003-9993/03/8407-7029$30.00/0 doi:10.1016/S0003-9993(03)00033-9
cine and the American Academy of Physical Medicine and Rehabilitation LTHOUGH THE IMPORTANT ROLE of vitamins on A both healthy and diseased individuals has been establittle is known about the nutritional status of persons lished, 1-10
with spinal cord injury (SCI). The present study concerns serum levels of vitamins A, C, and E and their association with demographic and health status in persons with chronic SCI. The antioxidant properties of vitamins A, C, and E in protecting against cancer, cardiovascular disease, and pressure ulcer development and the major sources of these nutrients have been investigated.2,5-11 Vitamin A, also called retinol, is found only in animal organisms. Carotenoids, found in plants, are converted into vitamin A in the liver. Vitamin A is important in fetal development, but little is known about the quantities used by various body tissues at different stages of development.12 Retinoids are very hydrophobic and are carried in the plasma attached to specific proteins and sometimes by nonspecific albumins or lipoproteins. Vitamin A is mainly involved in the metabolism of epithelial cells and in vision. Deficiency of vitamin A can lead to night blindness, dry flaky skin, failure to grow, cornea keratinosis, and increased susceptibility to infection. There is evidence11,13 supporting a negative association between vitamin A and cancer. Cigarette smokers have lower, but not deficient, serum levels of vitamin A. It has been theorized that some tissues might experience a deficiency of vitamin A within a normal systemic concentration of vitamin A.13 Plasma vitamin A concentration tends to remain within the normal range despite fluctuations in the daily intake of vitamin A. Some dietary sources of vitamin A are many vegetables such as carrots and broccoli, juices such as apricot nectar and tomato juice, butter, milk, eggs, and liver. Vitamin C, ascorbic acid, is an important catalyst for normal collagen metabolism. It also helps to maintain an acid pH in urine. Vitamin C is an antioxidant and epidemiologic studies suggest that its plasma concentration is inversely related to the incidence of coronary heart disease.5 Vitamin C is water soluble. Some dietary sources of vitamin C are citrus fruits, cruciferous vegetables such as broccoli and cauliflower, and cranberry and tomato juice. Vitamin E, alpha-tocopherol, is a fat-soluble antioxidant. One of its most important functions in the body may be its protection against lipid peroxidation. This is important for the functional integrity of all biologic membranes. Deficiency of vitamin E leads to pathologic changes in muscle and nervous systems. It has been reported that oral administration of vitamin E supplements increases the high-density lipoprotein– cholesterol ratio in humans.14 Some dietary sources of vitamin E are buttermilk, oatmeal, eggs, corn oil, tuna, tomato juice, cabbage, and peas. Vitamins A, C, and E play a major role in maintaining skin integrity, decreasing necrosis, and in promoting wound healing.15-22 However, there have been no controlled studies to assess the specific role of these nutrients and their association with demographic and health status in individuals with SCI. Arch Phys Med Rehabil Vol 84, July 2003
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VITAMINS AND SPINAL CORD INJURY, Moussavi Table 1: Characteristics of the Sample (Nⴝ110) Mean ⫾ SD
Age (y) Age at onset of SCI (y) Time since onset of SCI (y)
Gender Male Female Race and ethnicity White (non-Hispanic) African American Hispanic American Other Level and completeness of injury* Tetraplegia (ASIA class A, B, or C) Paraplegia (ASIA class A, B, or C) Tetraplegia or paraplegia (ASIA class D)
Range
44.1⫾13.2 22.4–81.9 29.7⫾11.8 9.7–58.9 14.3⫾9.6 2.3–46.9 n
%
79 31
71.8 28.2
63 27 19 1
57.3 24.5 17.3 0.9
46 43 21
41.8 39.1 19.1
Houston and Galveston, TX. Four additional men had been selected for the life status study because they had been injured a long time (23– 41y), and another 7 men had been selected because they had been injured over the age of 35 years (range, 36 – 68y). An additional 20 persons (17 men, 3 women) who
Abbreviation: SD, standard deviation *ASIA Impairment Scale.
Limited information is available on the nutritional status of persons with SCI, especially those who are living in the community.3,23-27 Most studies have been conducted during the acute phase of recovery, usually on a very small number of subjects.3,23-25,28 Levine et al26 examined the nutritional status of 33 persons with chronic SCI and reported that the intake of micronutrients, including vitamins A and E, was lower than the recommended dietary allowances. They concluded that nutritional intervention and education of persons with SCI were needed. Breslow29 reviewed the research information from 1943 to 1989 on the nutrition of individuals with pressure ulcers in the general population and concluded that they were malnourished. Several investigators4,30-36 have shown that inadequate serum vitamins C and E, together with poor nutritional intake, are among the major risk factors for developing pressure ulcers in persons with SCI. To our knowledge, no study has examined the association of these vitamins with ethnicity and health status in persons with SCI. The present report contains data about serum levels of vitamins A, C, and E and their relation to demographic information, health status, selected health-promoting behaviors, and pressure ulcer occurrence in persons with chronic SCI from various ethnic backgrounds. The results are compared with those of the recommended reference ranges for the general population. METHODS Participants This study was a component of the Rehabilitation Research and Training Center in Community Integration for Individuals with Spinal Cord Injury sponsored by the National Institute on Disability and Rehabilitation Research (1994 –2001). Complete serum vitamin data were provided by 110 individuals (table 1). Part of the sample consisted of 80 persons with chronic traumatic SCI (57 men, 23 women) who originally were recruited for an earlier study (1988 –1993) of the life status of persons with SCI. All 23 women and 46 of the men were randomly selected from a sampling frame of 661 adults (ⱖ18y) with traumatic SCI living within a 13-county area surrounding Arch Phys Med Rehabil Vol 84, July 2003
Fig 1. Distributions of age, age at onset, and time since onset.
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VITAMINS AND SPINAL CORD INJURY, Moussavi Table 2: Serum Levels of Vitamins A, C, and E (Nⴝ110) Vitamin
Mean ⫾ SD
Range
Reference Range*
% Below Reference Range
Serum vitamin A (g/dL) Serum vitamin C (mg/dL) Serum vitamin E (g/mL)
64.2⫾29.8 0.9⫾0.6 8.1⫾4.0
11.8–132.9 0.1–2.9 1.8–22.3
36–120 0.6–3.0 5.5–17
16.4 37.3 30.0
*The normal physiologic values were determined by Mayo Clinic.45
were injured more recently (2–7y) and 10 persons (5 men, 5 women) from Hispanic backgrounds were recruited from an updated sampling frame (1994 –1998) to supplement those persons with chronic SCI who had been in the earlier study. To participate, individuals had to be at least 18 years of age and have sustained a traumatic SCI at least 2 years before study entry. Participants had to be able to understand and respond to questions in either English or Spanish. Persons who were too cognitively impaired or who were too ill to participate were excluded. As can be seen in table 1 and figure 1, there were wide ranges for age (22– 82y), age at onset (10 –59y), and time since onset of SCI (2– 47y). Most of the participants were male and white; however, women and minorities were overrepresented compared with the general SCI population. There were nearly equal numbers of persons with tetraplegia and paraplegia. Procedures Recruitment was conducted by telephone. Persons interested in participating were sent a self-report packet and a consent form to complete. Research technicians were trained by the principal investigators to obtain the information from which the level and completeness of injury were later ascertained by a physician. They were also trained to perform venipunctures and to conduct structured interviews. The research technicians visited the participant’s residence to conduct an interview; to assess impairment status; and to collect the consent form, the self-report packet, and a blood sample. All procedures were in accordance with the standards of the Institutional Review Board for Human Subject Research for Baylor College of Medicine and Affiliated Hospitals. Measures Demographic data (age, gender, race and ethnicity), age at onset, and time since onset were collected by self-report for each participant. American Spinal Injury Association total motor index score. The American Spinal Injury Association37 (ASIA) total motor index score reflects the degree to which people with SCI have normal voluntary control of their musculature. This score is the sum of ratings for 10 key muscle segments on each side of the body. Each muscle segment is rated on a 6-point scale ranging from 0 (total paralysis) to 5 (normal). Total scores can range from 0 to 100 with normal motor function scored as 100 (50 for each side). Based on the ratings, participants were categorized as having tetraplegia (cervical level) or paraplegia (subcervical level). ASIA impairment score. The completeness of the injury was assessed with the ASIA impairment score,37 a 5-point scale with ASIA class A indicating no motor or sensory function in the sacral segments; class B indicating sensory but not motor function below the neurologic level, including the sacral segments; class C indicating motor function below the neurologic level and more than half of key muscles below the neurologic level having a muscle grade less than 3; class D indicating motor function below the neurologic level and at least half of
key muscles below that level having a muscle grade of 3 or more; and class E indicating normal motor and sensory function. Level and completeness of injury were combined to form 3 groups—tetraplegia (ASIA class A, B, or C), paraplegia (class A, B, or C), and tetraplegia or paraplegia (class D). Serum vitamins. After overnight fasting, blood was collected at the home of the participants and delivered in ice for biochemical assays. Serum levels of vitamins were measured by using standard high pressure liquid chromatography techniques.38,39 FIM™ instrument. The 13 motor items of the FIM instrument40 were administered as an interview during the home visit. These items assess the degree of assistance received to perform 13 activities of daily living (ADLs)— eating; bathing; grooming; dressing upper body; dressing lower body; toileting; bladder management; bowel management; transferring to bed, chair, or wheelchair, transferring to tub or shower; transferring to toilet; walking or using a wheelchair; and climbing stairs. Each item is rated on a 7-point scale ranging from 1 (completely dependent) to 7 (completely independent with no special equipment, extra time, or lack of safety). Scores on the 13 items are summed to obtain a total score. High concordance has been reported between self-reported motor FIM scores and scores based on independent observation.41,42 Health-Promoting Lifestyle Profile. The Health-Promoting Lifestyle Profile43 (HPLP) is comprised of 6 subscales— self-actualization, health responsibility, exercise, nutrition, interpersonal support, and stress management. It was completed as part of the self-report packet. For purposes of this study, only the nutrition subscale was used because it was hypothesized to be the most likely to be related to vitamin levels. The internal consistency of this 6-item subscale has been reported as .76. Each item is rated with regard to the regularity (1, never; 2, sometimes; 3, often; 4, routinely) with which the respondent engages in a particular health-promoting behavior (eg, eats breakfast, chooses foods without preservatives, plans or selects meals to include the “basic 4” food groups each day). An average score is calculated across the items for each subscale; thus, subscale scores can range from 1 to 4. Medical Outcomes Study 36-Item Short-Form Health Survey. The Medical Outcomes Study 36-Item Short-Form Health Survey44 (SF-36) is a questionnaire containing 36 items that assess 8 health concepts: physical functioning, bodily pain, role limitations due to physical health problems, role limitations due to personal or emotional problems, emotional wellbeing, social functioning, vitality (energy, fatigue), and general health perceptions including perceived change in health. It was completed as part of the self-report packet. For purposes of the present study, only the general health subscale was used because we hypothesized it to be the most likely to be related to vitamin levels. The internal consistency of this 5-item subscale has been reported as .78. One item asks respondents to rate their health as excellent, very good, good, fair, or poor. The response options for the remaining 4 items are definitely true, mostly true, do not know, mostly false, or definitely false. The Arch Phys Med Rehabil Vol 84, July 2003
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statements rated are “I seem to get sick a little easier than other people,” “I am as healthy as anybody I know,” “I expect my health to get worse,” and “My health is excellent.” Item responses are combined according to scoring procedures provided by the developers. Subscale scores can range from 0 to 100. Pressure ulcer incidence in past 12 months. As part of the self-report packet, participants were asked whether they had had in the past 12 months, a pressure ulcer that involved an open break in the skin (ie, at least a stage II). Statistical Analysis Descriptive statistics were obtained on all study variables (ie, means, standard deviations, [SDs], ranges, numbers, percentages). The percentage of participants whose serum level was below the minimum of the reference range45 for each of the 3 vitamins was calculated. Correlations were calculated between age, age at onset of SCI, and time since onset of SCI and each of the serum vitamin levels. To assess whether gender differences existed in serum vitamin levels, t tests were performed. Analyses of variance (ANOVAs) were performed to assess the relations between race-ethnicity and serum vitamin levels and between level and completeness of injury and serum vitamin levels. For ANOVAs, Bonferroni post hoc pairwise comparisons were performed when indicated. The relationships of the 3 serum vitamins with the FIM motor score, the HPLP nutrition subscale, and the SF-36 general health subscale were assessed with correlational analyses. The associations between the serum vitamins and having or not having a pressure ulcer that broke the skin in the past 12 months were assessed using t tests. To correct for multiple comparisons, a P value of .005 was selected to indicate significance. Analyses with P values less than .01 but greater than .005 were considered to approach significance. RESULTS Serum Vitamins Presented in table 2 are the descriptive statistics for the level of vitamins in the participants’ serum. There were wide ranges. The distributions for the serum vitamins are in figure 2. The reference range for each serum vitamin is listed and the percentage of participants who fell below the minimum is presented. A considerable proportion (16%–37%) of the sample had inadequate levels of each of these vitamins in their serum (table 2). Relations Between Serum Vitamins and Demographic and Injury-Related Data The relations between serum vitamins with demographic and injury-related variables are in table 3. Age was significantly related to vitamin E but only approached significance with vitamin A. Age at onset was significantly related to both vitamins A and E. Persons who were older or older at onset had higher levels of vitamins A and E. No relationship existed between time since onset of SCI, gender, or race and ethnicity and any of the 3 serum vitamins. Regarding level and completeness of injury, the more severe the impairment, the lower the level of serum vitamin A (F⫽11.00, P⬍.001). In pairwise comparisons, persons with tetraplegia or paraplegia with ASIA Impairment Scale scores of D had higher levels of serum vitamin A than persons with tetraplegia (ASIA class A, B, or C; P⬍.0001) and persons with paraplegia (class A, B, or C; P⬍.02). Furthermore, persons with paraplegia tended to have higher levels than persons with tetraplegia (P⬍.07). Arch Phys Med Rehabil Vol 84, July 2003
Fig 2. Distributions of serum vitamins A, C, and E.
Status Measures Descriptive statistics for the 13 motor items on the FIM, the HPLP nutrition subscale, the SF-36 general health subscale, and the occurrence of a pressure ulcer in the past 12 months are in table 4. Wide ranges existed for all of the continuous
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VITAMINS AND SPINAL CORD INJURY, Moussavi Table 3: Relation Between Serum Vitamins and Demographic and Injury-Related Data (Nⴝ110) Vitamin A
Vitamin C
Vitamin E
Pearson Correlations
Age Age at onset of SCI Time since onset of SCI
.24* .29† ⫺.03
⫺.07 .01 ⫺.11
.26† .30† ⫺.01
Mean Level of Vitamin ⫾ SD
Gender (t test) Female Male Race/ethnicity (ANOVA) White (non-Hispanic) African American Hispanic American Level and completeness of injury (ANOVA) Tetraplegia (ASIA class A, B, or C) Paraplegia (ASIA class A, B, or C) Tetraplegia or paraplegia (ASIA class D)
61.9⫾32.2 65.2⫾29.0
1.1⫾0.7 0.8⫾0.6
8.3⫾4.1 8.1⫾4.0
70.2⫾32.0 54.8⫾22.9 56.4⫾26.8
0.9⫾0.6 0.8⫾0.6 0.8⫾0.6
8.4⫾4.2 6.8⫾3.3 8.8⫾4.0
52.6⫾22.4‡ 66.0⫾32.7‡ 86.2⫾25.3‡
1.0⫾0.7 0.8⫾0.5 0.9⫾0.6
7.3⫾2.8 8.3⫾4.3 9.5⫾5.1
*P⬍.01. † P⬍.005. ‡ P⬍.001.
measures. More than one quarter of the participants had had a pressure ulcer in the past year that had broken the skin (ie, stage II or greater). Relation Between Serum Vitamins and Status Measures The relations between serum vitamin levels and various status measures are in table 5. The score on the 13 motor items of the FIM was moderately (r⫽.38) related to the level of serum vitamin A. Persons who were more independent in ADLs tended to have higher levels of vitamin A in their serum. The relation between the HPLP nutrition subscale and serum vitamin A approached significance (r⫽.26). Persons reporting better nutritional behaviors tended to have more vitamin A in their serum. The SF-36 general health subscale was weakly (r⫽.28) related to serum vitamin A. Persons reporting better health had higher levels of the vitamin. Persons who had not had a pressure ulcer of at least stage II severity in the past year had higher levels of serum vitamin A than did those with at least 1 pressure ulcer in the past year (t⫽3.79, P⬍.001). DISCUSSION Levels of vitamins A, C, and E were inadequate in the serum of a significant proportion (16%–37%) of the sample. Age, age at onset, and level of injury were each related to 1 or more serum vitamin levels. Persons who were older or older at onset Table 4: Functional Status, Health-Promoting Nutrition-Related Behaviors, Health Status, and Pressure Ulcer Incidence (Nⴝ110)
FIM motor items HPLP nutrition subscale SF-36 general health subscale
Pressure ulcer (at least stage II) in the past 12 months No Yes
Mean ⫾ SD
Range
62.7⫾23.4 2.4⫾0.6 65.5⫾19.7
13–91 1.2–4.0 15–100
n
%
80 30
72.7 27.3
had higher levels of serum vitamins A and E. Older persons may be more compliant with dietary recommendations and may be better educated or have a higher socioeconomic status, all of which may influence food choices. Regarding level and completeness of injury, the more severe the impairment, the lower the level of serum vitamin A. Consistent with this, a lower level of serum vitamin A was also associated with less functional independence in ADLs. Greater impairment and less functional independence may be related to comorbidities such as hypothyroidism. Many of the effects of vitamin A are mediated through specific nuclear receptors that are members of the steroid-thyroid hormone superfamily of receptors. A deficiency in the number of these receptors interferes with the optimal usage of the available vitamin A. These comorbidities may also affect the general perception of health status. The fact that lower levels of vitamin A were related to a greater likelihood of pressure ulcers may be related to the major role that vitamin A has in growth and differentiation of the epithelial cells, in maintaining skin integrity, and in promoting wound healing.15,16,46,47 It is possible that lower serum vitamin A disturbs the integrity of the skin by reducing the synthesis between skin collagen and the elastic fibers, thus predisposing the skin to develop pressure ulcers.17 This relationship needs to be confirmed by further study. Interventions, such as topical application of vitamin A to vulnerable areas of the skin and/or oral intake of a vitamin A supplement, must also be evaluated. The effect of these treatments on the development of pressure ulcers must be determined. A limitation of the study is that, although the total number of participants was respectable, the small size of certain subsamples such as women, minorities, and less impaired persons (ie, those with ASIA class D scores) may have affected some of the findings. CONCLUSIONS The present study is an important contribution to the sparse literature on vitamin levels in persons who have SCI and live in the community. Women and minorities were represented. Unlike the participants in other studies, the sample was well beyond the time of injury and, therefore, likely to have wellestablished nutritional patterns and lifestyles. The findings sugArch Phys Med Rehabil Vol 84, July 2003
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Table 5: Relation Between Serum Vitamins and Functional Status, Health-Promoting Nutrition-Related Behaviors, Health Status, and Pressure Ulcer Occurrence in Past Year (Nⴝ110) Vitamin A
Vitamin C
Vitamin E
Pearson Correlations
FIM motor items HPLP nutrition subscale SF-36 general health subscale
.38‡ .26* .28†
⫺.05 .16 ⫺.03
.07 .23 .02
Mean Level of Vitamin ⫾ SD
Pressure ulcer (at least stage II) in past 12 months (t tests) No Yes
70.5⫾29.0‡ 47.7⫾25.6‡
0.96⫾0.61 0.71⫾0.60
8.40⫾4.0 7.35⫾4.1
*P⬍.01. † P⬍.005. ‡ P⬍.001.
gest that vitamin levels may be related to function, general health, and pressure ulcer incidence. Clearly, a need exists for studies that evaluate innovative interventions such as adding vitamin-fortified grains and cereals or calcium-added orange juice to the diet of persons with SCI both to improve their nutritional status and to determine the effect of such improvement on various functional and health status measures. Fortified grains or cereals would make it easier for them to increase their vitamin intake because, based on the findings, they are more likely to eat bread than they are to increase their consumption of vegetables and fruits. A more direct approach would be to increase nutrition knowledge among persons with SCI. Rodriguez et al,18 in a study parallel to ours, sent nutrition information to persons with SCI who had evinced their interest in receiving nutritionrelated information. Once a month, these persons were sent information on a specific topic such as calcium, fats, fiber, and iron. The information consisted of (1) a relatively simple explanation of the role played by the specific nutrient in the body’s function, (2) a list of foods rich in the nutrient in question, and (3) some simple recipes incorporating the featured item. The recipes were chosen for their limited number of ingredients and uncomplicated cooking methods to facilitate use by persons with SCI. The information was compiled into fact sheets that are available from the Education Department of TIRR. Persons with SCI receive some nutrition counseling before their discharge from their first rehabilitation hospitalization. At that time, however, they are receiving so much information that nutrition is probably not high on their list of important information. It might be helpful if nutrition information and individual counseling were made part of subsequent rehabilitation admissions and annual check-ups. An educational approach in a rehabilitation setting or independent living agency may encourage some improvement in the diet of some persons with SCI. The success of these interventions depends on patient education that motivates the patients to take responsibility.48 Teaching strategies should include setting short- and long-term objectives, using simple understandable language, and evaluating the extent to which the learning objectives are achieved.48 The importance of gearing the intervention to the patient’s literacy level has also been emphasized in more recent publications.49,50 Innovative approaches have included use of the Internet, other computerbased interventions, audiotapes, and videotapes.50,51 However, compliance with recommended practices may not be assured even within the most ideal conditions. Chapman et al52 recommended encouraging patient responsibility. According to these investigators, noncompliance results from patients not believArch Phys Med Rehabil Vol 84, July 2003
ing the recommendation will help the problem. They suggest that positive patient participation will increase if the treatment is individualized to the patient’s needs, if it is easy to follow, if positive reinforcement is provided, and if a support system is in place. Tailoring the information to the patient is effective.51,53 Furthermore, the success of health education programs depends on the degree to which the patients participate in the process, including defining their needs, setting their priorities, and evaluating their own progress.51,53-56 Acknowledgment: We thank Michael M. Priebe, MD, for his assistance in determining the level and completeness of injury, and Margaret Nosek, PhD, for critical review of an earlier version of the manuscript. References 1. Houda B. Evaluation of nutritional status in persons with spinal cord injury: a prerequisite for successful rehabilitation. SCI Nurs 1993;10(1):4-7. 2. Block G, Patterson B, Subar A. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr Cancer 1992;18:1-29. 3. Laven GT, Huang CT, DeVivo MJ, Stover SL, Kuhlemeier KV, Fine PR. Nutritional status during the acute stage of spinal cord injury. Arch Phys Med Rehabil 1989;70:277-81. 4. Pinchcofsky-Devin GD, Kaminski MV Jr. Correlation of pressure sores and nutritional status. J Am Geriatr Soc 1986;34:435-40. 5. Gey KF. On the antioxidant hypothesis with regard to arteriosclerosis. Bibl Nutr Dieta 1986;37:53-91. 6. Gey KF. Ten-year retrospective on the antioxidant hypothesis of arteriosclerosis: threshold plasma levels of antioxidant micronutrients related to minimum cardiovascular risk. J Nutr Biochem 1995;6:206-36. 7. Price JF, Fowkes FG. Antioxidant vitamins in the prevention of cardiovascular disease: the epidemiological evidence. Eur Heart J 1997;18:719-27. 8. Todd S, Woodward M, Tunstall-Pedoe H, Bolton-Smith C. Dietary antioxidant vitamins and fiber in the etiology of cardiovascular disease and all-causes mortality: results from the Scottish Heart Health Study. Am J Epidemiol 1999;150:1073-80. 9. Clarkson PM, Thompson HS. Antioxidants: what role do they play in physical activity and health? Am J Clin Nutr 2000;72:637S46S. 10. Hu G, Cassano PA. Antioxidant nutrients and pulmonary function: the Third National Health and Nutrition Examination Survey (NHANES III). Am J Epidemiol 2000;151:975-81. 11. Lupulescu A. The role of vitamins A, beta-carotene, E, and C in cancer cell biology. Int J Vitam Nutr Res 1993;63:3-14. 12. Blomhoff R, Green MH, Berg T, Norum KR. Transport and storage of vitamin A. Science 1990;250:399-404.
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13. Edes, TE, Kwan SK, Buckley CS, Thomton WH Jr. Tissue vitamin A repletion is impaired by carcinogen exposure. Int J Cancer 1992;50:99-102. 14. Hermann WJ Jr. The effect of vitamin E on lipoprotein cholesterol distribution. Ann N Y Acad Sci 1982;393:467-72. 15. Albina JE. Nutrition and wound healing. JPEN J Parenter Enteral Nutr 1994;18:367-76. 16. Keller KL, Fenske NA. Uses of vitamins A, C, and E and related compounds in dermatology: a review. J Am Acad Dermatol 1998; 39:611-25. 17. Personelle J, Bolivar de Souza PE, Ruiz RO. Injection of vitamin A acid, vitamin E, and vitamin C for treatment of tissue necrosis. Aesthetic Plast Surg 1998;22:58-64. 18. Rodriguez GP, Claus-Walker J, Kent MC, Garza HM. Collagen metabolite excretion as a predictor of bone- and skin-related complications in spinal cord injury. Arch Phys Med Rehabil 1989;70:442-4. 19. Phillips C, Pinnell SR. Effects of ascorbic acid on proliferation and collagen synthesis in relation to the donor age of human dermal fibroblasts. Soc Invest Dermatol 1994;103:228-32. 20. Pinnell SR, Murad S. Vitamin C and collagen metabolism. In: Kligman AM, Takase Y, editors. Cutaneous aging. Tokyo: Univ Tokyo Pr; 1988. p 275-92. 21. Geesin JC, Brown LJ, Gordon JS, Berg RA. Human dermal fibroblasts in contracted collagen gels by ascorbic acid, growth factors, and inhibitors of lipid peroxidation. Exp Cell Res 1993; 206:283-90. 22. Nachbar F, Korting HC. The role of vitamin E in normal and damaged skin. J Mol Med 1995;73:7-17. 23. Mitchell E. Nutritional care plan for SCI patients. SCI Nurs 1984;1(2):13. 24. Gines DJ, Holliday ME, Ervin K. Nutrition assessment during rehabilitation of the spinal cord injury patient. Top Clin Nutr 1987;2:39. 25. Huang CT, DeVivo MJ, Stover SL. Anemia in acute phase of spinal cord injury. Arch Phys Med Rehabil 1990;71:3-7. 26. Levine AM, Nash MS, Green BA, Shea JD, Aronica MJ. An examination of dietary intakes and nutritional status of chronic healthy spinal cord injured individuals. Paraplegia 1992;30:880-9. 27. Lagger L. Spinal cord injury: nutritional management. J Neurosurg Nurs 1983;15:310-2. 28. Blissitt PA. Nutrition in acute spinal cord injury. Crit Care Nurs Clin North Am 1990;2:375-84. 29. Breslow R. Nutritional status and dietary intake of patients with pressure ulcers: review of research literature 1943 to 1989. Decubitus 1991;4:16-21. 30. Taylor TV, Rimmer S, Day B, Butcher J, Dymock IW. Ascorbic acid supplementation in the treatment of pressure-sores. Lancet 1974;2:544-6. 31. Salzberg CA, Byrne DW, Cayten CG, et al. Predicting and preventing pressure ulcers in adults with paralysis. Adv Wound Care 1998;11:237-46. 32. Byrne DW, Salzberg CA. Major risk factors for pressure ulcers in the spinal cord disabled: a literature review. Spinal Cord 1996; 34:255-63. 33. Breslow RA, Bergstrom N. Nutritional prediction of pressure ulcers. J Am Diet Assoc 1994;94:1301-4. 34. Rochon PA, Beaudet MP, McGlinchey-Berroth R, et al. Risk assessment for pressure ulcers: an adaptation of the National Pressure Ulcer Advisory Panel risk factors to spinal cord injured patients. J Am Paraplegia Soc 1993;16:169-77. 35. Balch JF, Balch PA. Prescription for nutritional healing. Garden City Park: Avery; 1990. 36. Matthews LE. Pressure sores—nutrition care’s vital role. J Nutr Elder 1989;8:107-12.
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37. American Spinal Injury Association. International standard for neurological and functional classification of spinal cord injury. Chicago: ASIA; 1992. 38. Driskell WJ, Neese JW, Bryant CC, Bashor MM. Measurement of vitamin A and vitamin E in human serum by high-performance liquid chromatography. J Chromatogr 1982;231:439-44. 39. Irache JM, Expeleta I, Vega FA. Determination of antioxidant synergists and ascorbic acid in some fatty pharmaceuticals, cosmetics, and food. Chromatographia 1993;3/4:232-6. 40. Smith P, Hamilton BB, Granger CV. Functional independence measure decision tree: the FONE FIM. Buffalo: Research Foundation of the State Univ New York; 1989. 41. Chang WC, Slaughter S, Cartwright D, Chan C. Evaluating the FONE FIM: Part I. Construct validity. J Outcome Meas 1997;1: 192-218. 42. Chang WC, Chan C, Slaughter SE, Cartwright D. Evaluating the FONE FIM: Part II. Concurrent validity & influencing factors. J Outcome Meas 1997;1:259-85. 43. Walker SN, Sechrist KR, Pender NJ. The Health-Promoting Lifestyle Profile: development and psychometric characteristics. Nurs Res 1987;36:76-81. 44. McHorney CA, Ware JE Jr, Lu JF, Sherbourne CD. The MOS 36-item Short-Form Health Survey (SF-36): III. Tests of data quality, scaling assumptions, and reliability across diverse patient groups. Med Care 1994;32:40-66. 45. Nelson JK, Moxness KE, Jensen MD, Gastineau CF. Mayo Clinic diet manual: a handbook of nutrition practices. St. Louis: Mosby; 1994. 46. Ellis CN, Weiss JS, Hamilton TA, Headington JT, Zelickson AS, Voorhees JJ. Sustained improvement with prolonged topical tretinoin (retinoic acid) for photoaged skin. J Am Acad Dermatol 1990;23:629-37. 47. Kligman AM, Grove GL, Hirose R, Leyden JJ. Topical tretinoin for photoaged skin. J Am Acad Dermatol 1986;15:836-59. 48. Rottkamp BC. An experimental nursing study: a behavior modification approach to nursing therapeutics in body positioning of spinal cord-injured patients. Nurs Res 1976;25:181-6. 49. Howard-Pitney B, Winkleby MA, Albright CL, Bruce B, Fortmann SP. The Stanford Nutrition Action Program: a dietary fat intervention for low-literacy adults. Am J Public Health 1997;87: 1971-6. 50. TenHave TR, Van Horn B, Kumanyika S, Askov E, Matthews Y, Adams-Campbell LL. Literacy assessment in a cardiovascular nutrition education setting. Patient Educ Couns 1997;31:139-50. 51. Anderson ES, Winett RA, Wojcik JR, Winett SG, Bowden T. A computerized social cognitive intervention for nutrition behavior: direct and mediated effects on fat, fiber, fruits, and vegetables, self-efficacy, and outcome expectations among food shoppers. Ann Behav Med 2001;23:88-100. 52. Chapman K, McGinnis-Rake C, O’Halloran W, Paul S, Virden JA. Convincing the non-compliant patient to change his behavior. Ostomy Wound Manage 1991;35:45-6, 48, 50-1. 53. Williamson AR, Hunt AE, Pope JF, Tolman NM. Recommendations of dietitians for overcoming barriers to dietary adherence in individuals with diabetes. Diabetes Educ 2000;26:272-9. 54. Green LW. The theory of participation: a quantitative study. Adv Health Promot Dis Prev 1986;1:211-66. 55. Cullen KW, Baranowski T, Smith SP. Using goal setting as a strategy for dietary behavior change. J Am Diet Assoc 2001;101: 562-6. 56. Schnoll R, Zimmerman BJ. Self-regulation training enhances dietary self-efficacy and dietary fiber consumption. J Am Diet Assoc 2001;101:1006-11.
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Serum Levels of Vitamins A, C, and E in Persons With Chronic Spinal Cord Injury Living in the Community Robabeh M. Moussavi, PhD, Hector M. Garza, BS, Susan G. Eisele, BS, Gladys Rodriguez, PhD, Diana H. Rintala, PhD ABSTRACT. Moussavi RM, Garza HM, Eisele SG, Rodriguez G, Rintala DH. Serum levels of vitamins A, C, and E in persons with chronic spinal cord injury living in the community. Arch Phys Med Rehabil 2003;84:1061-7. Objectives: To determine serum levels of vitamins A, C, and E among individuals with spinal cord injury (SCI) living in the community, to compare these levels with general population norms, and to assess their association with demographic and injury-related data (age at onset, time since onset, level and completeness of injury), function, nutritional behaviors, and health status. Design: Descriptive and correlational. Setting: General community. Participants: A total of 110 adults (ⱖ18y) with traumatic SCI of at least 2 years in duration living within a 13-county area in Texas. Interventions: Not applicable. Main Outcome Measures: Demographic information, age at onset, time since onset, American Spinal Injury Association (ASIA) total motor index score, ASIA impairment score, assay of serum vitamins, FIM™ instrument motor items, HealthPromoting Lifestyle Profile nutrition subscale, Medical Outcomes Study 36-Item Short-Form Health Survey general health subscale, and pressure ulcer occurrence in past 12 months. Results: Many (16%–37%) of the participants had serum levels below the reference range for each vitamin. Being older at onset or less impaired was associated with higher serum vitamin A levels. Higher levels of serum vitamin A also were related to better function and health status and with not having a pressure ulcer within the past 12 months. Being older or older at onset was associated with higher serum levels of vitamin E. No relationships with vitamin C were found. Conclusions: Vitamin levels may be related to function, general health, and pressure ulcer incidence in persons with SCI. Further study is needed to determine effective interventions to improve vitamin levels and determine the effect of such improvements on overall health and rehabilitation outcomes. Key Words: Health behavior; Health status; Rehabilitation; Spinal cord injuries; Vitamins. © 2003 by the American Congress of Rehabilitation Medi-
From the Department of Physical Medicine and Rehabilitation, Baylor College of Medicine (Moussavi, Garza, Eisele, Rodriguez, Rintala), TIRR (Garza, Rintala), and Center of Excellence on Healthy Aging with Disabilities, Veterans Affairs Medical Center (Rintala), Houston, TX. Supported by the National Institutes of Health (grant no. 5-T32-HD-07465-05), and National Institute on Disability and Rehabilitation Research, Rehabilitation Research and Training Center on Community Integration for Individuals with Spinal Cord Injury (grant no. H133B40011-95). The opinions expressed in this article are those of the grantee and do not necessarily reflect those of the US Department of Education. Presented in part at the Second National Department of Veteran Affairs Rehabilitation Research and Development Conference, February 2000, Arlington, VA. Reprint requests to Diana H. Rintala, PhD, VAMC, 153, 2002 Holcombe Blvd, Houston, TX 77030, e-mail: [email protected]. 0003-9993/03/8407-7029$30.00/0 doi:10.1016/S0003-9993(03)00033-9
cine and the American Academy of Physical Medicine and Rehabilitation LTHOUGH THE IMPORTANT ROLE of vitamins on A both healthy and diseased individuals has been establittle is known about the nutritional status of persons lished, 1-10
with spinal cord injury (SCI). The present study concerns serum levels of vitamins A, C, and E and their association with demographic and health status in persons with chronic SCI. The antioxidant properties of vitamins A, C, and E in protecting against cancer, cardiovascular disease, and pressure ulcer development and the major sources of these nutrients have been investigated.2,5-11 Vitamin A, also called retinol, is found only in animal organisms. Carotenoids, found in plants, are converted into vitamin A in the liver. Vitamin A is important in fetal development, but little is known about the quantities used by various body tissues at different stages of development.12 Retinoids are very hydrophobic and are carried in the plasma attached to specific proteins and sometimes by nonspecific albumins or lipoproteins. Vitamin A is mainly involved in the metabolism of epithelial cells and in vision. Deficiency of vitamin A can lead to night blindness, dry flaky skin, failure to grow, cornea keratinosis, and increased susceptibility to infection. There is evidence11,13 supporting a negative association between vitamin A and cancer. Cigarette smokers have lower, but not deficient, serum levels of vitamin A. It has been theorized that some tissues might experience a deficiency of vitamin A within a normal systemic concentration of vitamin A.13 Plasma vitamin A concentration tends to remain within the normal range despite fluctuations in the daily intake of vitamin A. Some dietary sources of vitamin A are many vegetables such as carrots and broccoli, juices such as apricot nectar and tomato juice, butter, milk, eggs, and liver. Vitamin C, ascorbic acid, is an important catalyst for normal collagen metabolism. It also helps to maintain an acid pH in urine. Vitamin C is an antioxidant and epidemiologic studies suggest that its plasma concentration is inversely related to the incidence of coronary heart disease.5 Vitamin C is water soluble. Some dietary sources of vitamin C are citrus fruits, cruciferous vegetables such as broccoli and cauliflower, and cranberry and tomato juice. Vitamin E, alpha-tocopherol, is a fat-soluble antioxidant. One of its most important functions in the body may be its protection against lipid peroxidation. This is important for the functional integrity of all biologic membranes. Deficiency of vitamin E leads to pathologic changes in muscle and nervous systems. It has been reported that oral administration of vitamin E supplements increases the high-density lipoprotein– cholesterol ratio in humans.14 Some dietary sources of vitamin E are buttermilk, oatmeal, eggs, corn oil, tuna, tomato juice, cabbage, and peas. Vitamins A, C, and E play a major role in maintaining skin integrity, decreasing necrosis, and in promoting wound healing.15-22 However, there have been no controlled studies to assess the specific role of these nutrients and their association with demographic and health status in individuals with SCI. Arch Phys Med Rehabil Vol 84, July 2003
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VITAMINS AND SPINAL CORD INJURY, Moussavi Table 1: Characteristics of the Sample (Nⴝ110) Mean ⫾ SD
Age (y) Age at onset of SCI (y) Time since onset of SCI (y)
Gender Male Female Race and ethnicity White (non-Hispanic) African American Hispanic American Other Level and completeness of injury* Tetraplegia (ASIA class A, B, or C) Paraplegia (ASIA class A, B, or C) Tetraplegia or paraplegia (ASIA class D)
Range
44.1⫾13.2 22.4–81.9 29.7⫾11.8 9.7–58.9 14.3⫾9.6 2.3–46.9 n
%
79 31
71.8 28.2
63 27 19 1
57.3 24.5 17.3 0.9
46 43 21
41.8 39.1 19.1
Houston and Galveston, TX. Four additional men had been selected for the life status study because they had been injured a long time (23– 41y), and another 7 men had been selected because they had been injured over the age of 35 years (range, 36 – 68y). An additional 20 persons (17 men, 3 women) who
Abbreviation: SD, standard deviation *ASIA Impairment Scale.
Limited information is available on the nutritional status of persons with SCI, especially those who are living in the community.3,23-27 Most studies have been conducted during the acute phase of recovery, usually on a very small number of subjects.3,23-25,28 Levine et al26 examined the nutritional status of 33 persons with chronic SCI and reported that the intake of micronutrients, including vitamins A and E, was lower than the recommended dietary allowances. They concluded that nutritional intervention and education of persons with SCI were needed. Breslow29 reviewed the research information from 1943 to 1989 on the nutrition of individuals with pressure ulcers in the general population and concluded that they were malnourished. Several investigators4,30-36 have shown that inadequate serum vitamins C and E, together with poor nutritional intake, are among the major risk factors for developing pressure ulcers in persons with SCI. To our knowledge, no study has examined the association of these vitamins with ethnicity and health status in persons with SCI. The present report contains data about serum levels of vitamins A, C, and E and their relation to demographic information, health status, selected health-promoting behaviors, and pressure ulcer occurrence in persons with chronic SCI from various ethnic backgrounds. The results are compared with those of the recommended reference ranges for the general population. METHODS Participants This study was a component of the Rehabilitation Research and Training Center in Community Integration for Individuals with Spinal Cord Injury sponsored by the National Institute on Disability and Rehabilitation Research (1994 –2001). Complete serum vitamin data were provided by 110 individuals (table 1). Part of the sample consisted of 80 persons with chronic traumatic SCI (57 men, 23 women) who originally were recruited for an earlier study (1988 –1993) of the life status of persons with SCI. All 23 women and 46 of the men were randomly selected from a sampling frame of 661 adults (ⱖ18y) with traumatic SCI living within a 13-county area surrounding Arch Phys Med Rehabil Vol 84, July 2003
Fig 1. Distributions of age, age at onset, and time since onset.
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VITAMINS AND SPINAL CORD INJURY, Moussavi Table 2: Serum Levels of Vitamins A, C, and E (Nⴝ110) Vitamin
Mean ⫾ SD
Range
Reference Range*
% Below Reference Range
Serum vitamin A (g/dL) Serum vitamin C (mg/dL) Serum vitamin E (g/mL)
64.2⫾29.8 0.9⫾0.6 8.1⫾4.0
11.8–132.9 0.1–2.9 1.8–22.3
36–120 0.6–3.0 5.5–17
16.4 37.3 30.0
*The normal physiologic values were determined by Mayo Clinic.45
were injured more recently (2–7y) and 10 persons (5 men, 5 women) from Hispanic backgrounds were recruited from an updated sampling frame (1994 –1998) to supplement those persons with chronic SCI who had been in the earlier study. To participate, individuals had to be at least 18 years of age and have sustained a traumatic SCI at least 2 years before study entry. Participants had to be able to understand and respond to questions in either English or Spanish. Persons who were too cognitively impaired or who were too ill to participate were excluded. As can be seen in table 1 and figure 1, there were wide ranges for age (22– 82y), age at onset (10 –59y), and time since onset of SCI (2– 47y). Most of the participants were male and white; however, women and minorities were overrepresented compared with the general SCI population. There were nearly equal numbers of persons with tetraplegia and paraplegia. Procedures Recruitment was conducted by telephone. Persons interested in participating were sent a self-report packet and a consent form to complete. Research technicians were trained by the principal investigators to obtain the information from which the level and completeness of injury were later ascertained by a physician. They were also trained to perform venipunctures and to conduct structured interviews. The research technicians visited the participant’s residence to conduct an interview; to assess impairment status; and to collect the consent form, the self-report packet, and a blood sample. All procedures were in accordance with the standards of the Institutional Review Board for Human Subject Research for Baylor College of Medicine and Affiliated Hospitals. Measures Demographic data (age, gender, race and ethnicity), age at onset, and time since onset were collected by self-report for each participant. American Spinal Injury Association total motor index score. The American Spinal Injury Association37 (ASIA) total motor index score reflects the degree to which people with SCI have normal voluntary control of their musculature. This score is the sum of ratings for 10 key muscle segments on each side of the body. Each muscle segment is rated on a 6-point scale ranging from 0 (total paralysis) to 5 (normal). Total scores can range from 0 to 100 with normal motor function scored as 100 (50 for each side). Based on the ratings, participants were categorized as having tetraplegia (cervical level) or paraplegia (subcervical level). ASIA impairment score. The completeness of the injury was assessed with the ASIA impairment score,37 a 5-point scale with ASIA class A indicating no motor or sensory function in the sacral segments; class B indicating sensory but not motor function below the neurologic level, including the sacral segments; class C indicating motor function below the neurologic level and more than half of key muscles below the neurologic level having a muscle grade less than 3; class D indicating motor function below the neurologic level and at least half of
key muscles below that level having a muscle grade of 3 or more; and class E indicating normal motor and sensory function. Level and completeness of injury were combined to form 3 groups—tetraplegia (ASIA class A, B, or C), paraplegia (class A, B, or C), and tetraplegia or paraplegia (class D). Serum vitamins. After overnight fasting, blood was collected at the home of the participants and delivered in ice for biochemical assays. Serum levels of vitamins were measured by using standard high pressure liquid chromatography techniques.38,39 FIM™ instrument. The 13 motor items of the FIM instrument40 were administered as an interview during the home visit. These items assess the degree of assistance received to perform 13 activities of daily living (ADLs)— eating; bathing; grooming; dressing upper body; dressing lower body; toileting; bladder management; bowel management; transferring to bed, chair, or wheelchair, transferring to tub or shower; transferring to toilet; walking or using a wheelchair; and climbing stairs. Each item is rated on a 7-point scale ranging from 1 (completely dependent) to 7 (completely independent with no special equipment, extra time, or lack of safety). Scores on the 13 items are summed to obtain a total score. High concordance has been reported between self-reported motor FIM scores and scores based on independent observation.41,42 Health-Promoting Lifestyle Profile. The Health-Promoting Lifestyle Profile43 (HPLP) is comprised of 6 subscales— self-actualization, health responsibility, exercise, nutrition, interpersonal support, and stress management. It was completed as part of the self-report packet. For purposes of this study, only the nutrition subscale was used because it was hypothesized to be the most likely to be related to vitamin levels. The internal consistency of this 6-item subscale has been reported as .76. Each item is rated with regard to the regularity (1, never; 2, sometimes; 3, often; 4, routinely) with which the respondent engages in a particular health-promoting behavior (eg, eats breakfast, chooses foods without preservatives, plans or selects meals to include the “basic 4” food groups each day). An average score is calculated across the items for each subscale; thus, subscale scores can range from 1 to 4. Medical Outcomes Study 36-Item Short-Form Health Survey. The Medical Outcomes Study 36-Item Short-Form Health Survey44 (SF-36) is a questionnaire containing 36 items that assess 8 health concepts: physical functioning, bodily pain, role limitations due to physical health problems, role limitations due to personal or emotional problems, emotional wellbeing, social functioning, vitality (energy, fatigue), and general health perceptions including perceived change in health. It was completed as part of the self-report packet. For purposes of the present study, only the general health subscale was used because we hypothesized it to be the most likely to be related to vitamin levels. The internal consistency of this 5-item subscale has been reported as .78. One item asks respondents to rate their health as excellent, very good, good, fair, or poor. The response options for the remaining 4 items are definitely true, mostly true, do not know, mostly false, or definitely false. The Arch Phys Med Rehabil Vol 84, July 2003
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VITAMINS AND SPINAL CORD INJURY, Moussavi
statements rated are “I seem to get sick a little easier than other people,” “I am as healthy as anybody I know,” “I expect my health to get worse,” and “My health is excellent.” Item responses are combined according to scoring procedures provided by the developers. Subscale scores can range from 0 to 100. Pressure ulcer incidence in past 12 months. As part of the self-report packet, participants were asked whether they had had in the past 12 months, a pressure ulcer that involved an open break in the skin (ie, at least a stage II). Statistical Analysis Descriptive statistics were obtained on all study variables (ie, means, standard deviations, [SDs], ranges, numbers, percentages). The percentage of participants whose serum level was below the minimum of the reference range45 for each of the 3 vitamins was calculated. Correlations were calculated between age, age at onset of SCI, and time since onset of SCI and each of the serum vitamin levels. To assess whether gender differences existed in serum vitamin levels, t tests were performed. Analyses of variance (ANOVAs) were performed to assess the relations between race-ethnicity and serum vitamin levels and between level and completeness of injury and serum vitamin levels. For ANOVAs, Bonferroni post hoc pairwise comparisons were performed when indicated. The relationships of the 3 serum vitamins with the FIM motor score, the HPLP nutrition subscale, and the SF-36 general health subscale were assessed with correlational analyses. The associations between the serum vitamins and having or not having a pressure ulcer that broke the skin in the past 12 months were assessed using t tests. To correct for multiple comparisons, a P value of .005 was selected to indicate significance. Analyses with P values less than .01 but greater than .005 were considered to approach significance. RESULTS Serum Vitamins Presented in table 2 are the descriptive statistics for the level of vitamins in the participants’ serum. There were wide ranges. The distributions for the serum vitamins are in figure 2. The reference range for each serum vitamin is listed and the percentage of participants who fell below the minimum is presented. A considerable proportion (16%–37%) of the sample had inadequate levels of each of these vitamins in their serum (table 2). Relations Between Serum Vitamins and Demographic and Injury-Related Data The relations between serum vitamins with demographic and injury-related variables are in table 3. Age was significantly related to vitamin E but only approached significance with vitamin A. Age at onset was significantly related to both vitamins A and E. Persons who were older or older at onset had higher levels of vitamins A and E. No relationship existed between time since onset of SCI, gender, or race and ethnicity and any of the 3 serum vitamins. Regarding level and completeness of injury, the more severe the impairment, the lower the level of serum vitamin A (F⫽11.00, P⬍.001). In pairwise comparisons, persons with tetraplegia or paraplegia with ASIA Impairment Scale scores of D had higher levels of serum vitamin A than persons with tetraplegia (ASIA class A, B, or C; P⬍.0001) and persons with paraplegia (class A, B, or C; P⬍.02). Furthermore, persons with paraplegia tended to have higher levels than persons with tetraplegia (P⬍.07). Arch Phys Med Rehabil Vol 84, July 2003
Fig 2. Distributions of serum vitamins A, C, and E.
Status Measures Descriptive statistics for the 13 motor items on the FIM, the HPLP nutrition subscale, the SF-36 general health subscale, and the occurrence of a pressure ulcer in the past 12 months are in table 4. Wide ranges existed for all of the continuous
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VITAMINS AND SPINAL CORD INJURY, Moussavi Table 3: Relation Between Serum Vitamins and Demographic and Injury-Related Data (Nⴝ110) Vitamin A
Vitamin C
Vitamin E
Pearson Correlations
Age Age at onset of SCI Time since onset of SCI
.24* .29† ⫺.03
⫺.07 .01 ⫺.11
.26† .30† ⫺.01
Mean Level of Vitamin ⫾ SD
Gender (t test) Female Male Race/ethnicity (ANOVA) White (non-Hispanic) African American Hispanic American Level and completeness of injury (ANOVA) Tetraplegia (ASIA class A, B, or C) Paraplegia (ASIA class A, B, or C) Tetraplegia or paraplegia (ASIA class D)
61.9⫾32.2 65.2⫾29.0
1.1⫾0.7 0.8⫾0.6
8.3⫾4.1 8.1⫾4.0
70.2⫾32.0 54.8⫾22.9 56.4⫾26.8
0.9⫾0.6 0.8⫾0.6 0.8⫾0.6
8.4⫾4.2 6.8⫾3.3 8.8⫾4.0
52.6⫾22.4‡ 66.0⫾32.7‡ 86.2⫾25.3‡
1.0⫾0.7 0.8⫾0.5 0.9⫾0.6
7.3⫾2.8 8.3⫾4.3 9.5⫾5.1
*P⬍.01. † P⬍.005. ‡ P⬍.001.
measures. More than one quarter of the participants had had a pressure ulcer in the past year that had broken the skin (ie, stage II or greater). Relation Between Serum Vitamins and Status Measures The relations between serum vitamin levels and various status measures are in table 5. The score on the 13 motor items of the FIM was moderately (r⫽.38) related to the level of serum vitamin A. Persons who were more independent in ADLs tended to have higher levels of vitamin A in their serum. The relation between the HPLP nutrition subscale and serum vitamin A approached significance (r⫽.26). Persons reporting better nutritional behaviors tended to have more vitamin A in their serum. The SF-36 general health subscale was weakly (r⫽.28) related to serum vitamin A. Persons reporting better health had higher levels of the vitamin. Persons who had not had a pressure ulcer of at least stage II severity in the past year had higher levels of serum vitamin A than did those with at least 1 pressure ulcer in the past year (t⫽3.79, P⬍.001). DISCUSSION Levels of vitamins A, C, and E were inadequate in the serum of a significant proportion (16%–37%) of the sample. Age, age at onset, and level of injury were each related to 1 or more serum vitamin levels. Persons who were older or older at onset Table 4: Functional Status, Health-Promoting Nutrition-Related Behaviors, Health Status, and Pressure Ulcer Incidence (Nⴝ110)
FIM motor items HPLP nutrition subscale SF-36 general health subscale
Pressure ulcer (at least stage II) in the past 12 months No Yes
Mean ⫾ SD
Range
62.7⫾23.4 2.4⫾0.6 65.5⫾19.7
13–91 1.2–4.0 15–100
n
%
80 30
72.7 27.3
had higher levels of serum vitamins A and E. Older persons may be more compliant with dietary recommendations and may be better educated or have a higher socioeconomic status, all of which may influence food choices. Regarding level and completeness of injury, the more severe the impairment, the lower the level of serum vitamin A. Consistent with this, a lower level of serum vitamin A was also associated with less functional independence in ADLs. Greater impairment and less functional independence may be related to comorbidities such as hypothyroidism. Many of the effects of vitamin A are mediated through specific nuclear receptors that are members of the steroid-thyroid hormone superfamily of receptors. A deficiency in the number of these receptors interferes with the optimal usage of the available vitamin A. These comorbidities may also affect the general perception of health status. The fact that lower levels of vitamin A were related to a greater likelihood of pressure ulcers may be related to the major role that vitamin A has in growth and differentiation of the epithelial cells, in maintaining skin integrity, and in promoting wound healing.15,16,46,47 It is possible that lower serum vitamin A disturbs the integrity of the skin by reducing the synthesis between skin collagen and the elastic fibers, thus predisposing the skin to develop pressure ulcers.17 This relationship needs to be confirmed by further study. Interventions, such as topical application of vitamin A to vulnerable areas of the skin and/or oral intake of a vitamin A supplement, must also be evaluated. The effect of these treatments on the development of pressure ulcers must be determined. A limitation of the study is that, although the total number of participants was respectable, the small size of certain subsamples such as women, minorities, and less impaired persons (ie, those with ASIA class D scores) may have affected some of the findings. CONCLUSIONS The present study is an important contribution to the sparse literature on vitamin levels in persons who have SCI and live in the community. Women and minorities were represented. Unlike the participants in other studies, the sample was well beyond the time of injury and, therefore, likely to have wellestablished nutritional patterns and lifestyles. The findings sugArch Phys Med Rehabil Vol 84, July 2003
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VITAMINS AND SPINAL CORD INJURY, Moussavi
Table 5: Relation Between Serum Vitamins and Functional Status, Health-Promoting Nutrition-Related Behaviors, Health Status, and Pressure Ulcer Occurrence in Past Year (Nⴝ110) Vitamin A
Vitamin C
Vitamin E
Pearson Correlations
FIM motor items HPLP nutrition subscale SF-36 general health subscale
.38‡ .26* .28†
⫺.05 .16 ⫺.03
.07 .23 .02
Mean Level of Vitamin ⫾ SD
Pressure ulcer (at least stage II) in past 12 months (t tests) No Yes
70.5⫾29.0‡ 47.7⫾25.6‡
0.96⫾0.61 0.71⫾0.60
8.40⫾4.0 7.35⫾4.1
*P⬍.01. † P⬍.005. ‡ P⬍.001.
gest that vitamin levels may be related to function, general health, and pressure ulcer incidence. Clearly, a need exists for studies that evaluate innovative interventions such as adding vitamin-fortified grains and cereals or calcium-added orange juice to the diet of persons with SCI both to improve their nutritional status and to determine the effect of such improvement on various functional and health status measures. Fortified grains or cereals would make it easier for them to increase their vitamin intake because, based on the findings, they are more likely to eat bread than they are to increase their consumption of vegetables and fruits. A more direct approach would be to increase nutrition knowledge among persons with SCI. Rodriguez et al,18 in a study parallel to ours, sent nutrition information to persons with SCI who had evinced their interest in receiving nutritionrelated information. Once a month, these persons were sent information on a specific topic such as calcium, fats, fiber, and iron. The information consisted of (1) a relatively simple explanation of the role played by the specific nutrient in the body’s function, (2) a list of foods rich in the nutrient in question, and (3) some simple recipes incorporating the featured item. The recipes were chosen for their limited number of ingredients and uncomplicated cooking methods to facilitate use by persons with SCI. The information was compiled into fact sheets that are available from the Education Department of TIRR. Persons with SCI receive some nutrition counseling before their discharge from their first rehabilitation hospitalization. At that time, however, they are receiving so much information that nutrition is probably not high on their list of important information. It might be helpful if nutrition information and individual counseling were made part of subsequent rehabilitation admissions and annual check-ups. An educational approach in a rehabilitation setting or independent living agency may encourage some improvement in the diet of some persons with SCI. The success of these interventions depends on patient education that motivates the patients to take responsibility.48 Teaching strategies should include setting short- and long-term objectives, using simple understandable language, and evaluating the extent to which the learning objectives are achieved.48 The importance of gearing the intervention to the patient’s literacy level has also been emphasized in more recent publications.49,50 Innovative approaches have included use of the Internet, other computerbased interventions, audiotapes, and videotapes.50,51 However, compliance with recommended practices may not be assured even within the most ideal conditions. Chapman et al52 recommended encouraging patient responsibility. According to these investigators, noncompliance results from patients not believArch Phys Med Rehabil Vol 84, July 2003
ing the recommendation will help the problem. They suggest that positive patient participation will increase if the treatment is individualized to the patient’s needs, if it is easy to follow, if positive reinforcement is provided, and if a support system is in place. Tailoring the information to the patient is effective.51,53 Furthermore, the success of health education programs depends on the degree to which the patients participate in the process, including defining their needs, setting their priorities, and evaluating their own progress.51,53-56 Acknowledgment: We thank Michael M. Priebe, MD, for his assistance in determining the level and completeness of injury, and Margaret Nosek, PhD, for critical review of an earlier version of the manuscript. References 1. Houda B. Evaluation of nutritional status in persons with spinal cord injury: a prerequisite for successful rehabilitation. SCI Nurs 1993;10(1):4-7. 2. Block G, Patterson B, Subar A. Fruit, vegetables, and cancer prevention: a review of the epidemiological evidence. Nutr Cancer 1992;18:1-29. 3. Laven GT, Huang CT, DeVivo MJ, Stover SL, Kuhlemeier KV, Fine PR. Nutritional status during the acute stage of spinal cord injury. Arch Phys Med Rehabil 1989;70:277-81. 4. Pinchcofsky-Devin GD, Kaminski MV Jr. Correlation of pressure sores and nutritional status. J Am Geriatr Soc 1986;34:435-40. 5. Gey KF. On the antioxidant hypothesis with regard to arteriosclerosis. Bibl Nutr Dieta 1986;37:53-91. 6. Gey KF. Ten-year retrospective on the antioxidant hypothesis of arteriosclerosis: threshold plasma levels of antioxidant micronutrients related to minimum cardiovascular risk. J Nutr Biochem 1995;6:206-36. 7. Price JF, Fowkes FG. Antioxidant vitamins in the prevention of cardiovascular disease: the epidemiological evidence. Eur Heart J 1997;18:719-27. 8. Todd S, Woodward M, Tunstall-Pedoe H, Bolton-Smith C. Dietary antioxidant vitamins and fiber in the etiology of cardiovascular disease and all-causes mortality: results from the Scottish Heart Health Study. Am J Epidemiol 1999;150:1073-80. 9. Clarkson PM, Thompson HS. Antioxidants: what role do they play in physical activity and health? Am J Clin Nutr 2000;72:637S46S. 10. Hu G, Cassano PA. Antioxidant nutrients and pulmonary function: the Third National Health and Nutrition Examination Survey (NHANES III). Am J Epidemiol 2000;151:975-81. 11. Lupulescu A. The role of vitamins A, beta-carotene, E, and C in cancer cell biology. Int J Vitam Nutr Res 1993;63:3-14. 12. Blomhoff R, Green MH, Berg T, Norum KR. Transport and storage of vitamin A. Science 1990;250:399-404.
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