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Nutrición Hospitalaria

versão On-line ISSN 1699-5198versão impressa ISSN 0212-1611

Nutr. Hosp. vol.29 no.4 Madrid Abr. 2014 

ORIGINAL / Alimentos funcionales


Estimation of antioxidants dietary intake in wet age-related macular degeneration patients

Estimación de la ingesta de antioxidantes en pacientes con degeneración macular asociada con la edad; variedad húmeda



María del Mar Bibiloni1, María Elisa Zapata1, Juan A. Aragón2, Antoni Pons1, José Luis Olea2 and Josep A. Tur1

1Research Group on Community Nutrition and Oxidative Stress. University of Balearic Islands, and CIBERobn (Physiopathology of Obesity and Nutrition). Palma de Mallorca. Spain.
2Ophthalmology Service. Son Espases Hospital. Palma de Mallorca. Spain.

The study was supported by the Balearic Islands Regional Ministry of Health (project DGAVAL PI 033/09; IB 1148/09), CIBERobn (CB12/03/30038), Grant of support to research groups no. 35/2011 (Balearic Islands Gov. and EU FEDER funds), Spanish Ministry of Education and Science (FPU Programme, PhD fellowship to Maria del Mar Bibiloni), Bank of Santander (PhD Programme Santander-Iberoamérica, PhD fellowship to Maria Elisa Zapata). The Research Group on Community Nutrition and Oxidative Stress, University of Balearic Islands belongs to the Centre Català de la Nutricio (IEC) and Exernet Network.





Aims: The aim of this study was to estimate the intake of antioxidant nutrients in wet age-related macular degeneration (AMD) patients, a degenerative and progressive disorder of the macula, which is the central part of the retina, associated with central vision loss.
Methods: A sample (n = 52, 78.9 ± 6.6 years old, 40.4% females and 59.6% males) of patients diagnosed of AMD was interviewed. Anthropometric measurements, two 24-h recalls, a semi-quantitative food frequency questionnaire and a general questionnaire incorporating questions related to socio-demographic and lifestyle variables were used.
Results: Most of wet AMD patients showed inadequate antioxidant nutrient intake (< 2/3 of Recommended Dietary Intake, RDI), and more than 60% of patients showed serious deficient intake (< 1/3 RDI) of lutein and zeaxanthin. Most consumed antioxidant rich foods only represented low contributions to antioxidant intake. Although adiposity is a factor risk for AMD progression; the fat and saturated fatty acids (SFA) intake of study participants were higher than the recommendations; the prevalence of overweight was 61.9% men and 58.1% in women; and 83% of patients (90.5% men and 77.4% women) showed fat mass over the cut-off limits.
Conclusions: The food pattern of wet AMD patients should be improved by means of an increase in the consumption of antioxidant rich foods, and a decrease in SFA rich foods.

Key words: Antioxidants. Wet age-related macular degeneration. Lutein. Zeaxanthin.


Objetivos: El objetivo de este estudio fue estimar la ingesta de nutrientes antioxidantes en pacientes con degeneración macular asociada a la edad (AMD) variedad húmeda, un trastorno degenerativo y progresivo de la mácula, la parte central de la retina, asociada con la pérdida de la visión central.
Métodos: En una muestra de pacientes diagnosticados de AMD (n = 52, 78,9 ± 6,6 años, 40,4% mujeres y 59,6% hombres) se registraron medidas antropométricas, dos recordatorios de 24 h, un cuestionario semicuantitativo de frecuencia de consumo de alimentos y cuestiones socio-demográficas y de estilo de vida.
Resultados: La mayoría de los pacientes con AMD húmeda mostraron una ingesta inadecuada de nutrientes antioxidantes (< 2/3 de las Ingestas Dietéticas Recomendadas, RDI) y más de 60% de los pacientes mostraron un déficit grave (< 1/3 RDI) de luteína y zeaxantina. Los alimentos ricos en antioxidantes más consumidos sólo aportaron bajas contribuciones a la ingesta de antioxidantes. Aunque la adiposidad es un factor de riesgo para la progresión de la AMD, el consumo de grasas y ácidos grasos saturados (SFA) de los pacientes fueron superiores a las recomendaciones; la prevalencia de sobrepeso fue del 61,9% hombres y 58.1% en las mujeres; y el 83% de los pacientes (90,5% hombres y 77,4% mujeres) mostró una masa grasa superior a los límites.
Conclusiones: El patrón alimentario de los pacientes con AMD debería mejorarse aumentando el consumo de alimentos ricos en antioxidantes y disminuyendo los alimentos ricos en SFA.

Palabras clave: Antioxidantes. Degeneración macular asociada a la edad. Luteína. Zeaxantina.

Non-standard abbreviations
AMD: Age-related macular degeneration
AREDS: Age-Related Eye Disease Study
OCT: optical coherence tomography
RAP: retinal angiomatous proliferation
PCV: polypoidal choroidal vasculopathy



Age-related macular degeneration (AMD) is a degenerative and progressive disorder of the macula, the central part of the retina, associated with central vision loss. It is the leading cause of visual impairment and blindness in people over the age of 60 years in industrialized countries1-4.

The population-based studies suggest that approximately 30% of people aged 75 years or older shows early signs of disease, and 7% shows an advanced stage5. The overall prevalence of AMD is 1% in 65-74 year old persons, 5% in 75-84 y-o, and 13% in ≥ 85 y-o5. The prevalence of late AMD is 0.8% in 60-69 y-o, 3.2% in 70-79 y-o and 19.7% in ≥ 80 y-o6. In Spain, AMD prevalence is 13% in people over age 65, and ranges from 0.5% at age 55, up 7% on ager over 757. Based on the Spanish population pyramid, it has been estimated that by 2015, 400.000 Spanish people will suffer AMD and more than 1 million people may be at risk8.

Risk factors associated with AMD include sex, iris color, heredity, cardiovascular health, nutrient status, body mass index, age and smoking9. Foods contain many nutrients that could interact on the risk for multifactorial diseases such as AMD10. It has been suggested that the condition of AMD may improve in people fed vitamins, antioxidants (carotenoids, vitamins C and E) and minerals (selenium and zinc) rich diets11. Age-Related Eye Disease Study (AREDS) recommended that to take an antioxidant supplementation (15 mg p-carotene, 500 mg vitamin C, 400 1U vitamin E and 80 mg zinc plus 2 mg copper) is successful in preventing the development of advanced AMD by 25%, and AREDS-2 included lutein, zeaxanthin and omega-3 fatty acids in the analysis of late AMD progression9.

AMD shows two clinics forms, an atrophic form that progresses slowly and represents 80-90% of cases, and a wet form characterized by the appearance of a choroidal membrane that promoted acute vision loss, represents 10-20%, and is responsible of 90% of blindness12. To our knowledge, no studies have been undertaken on antioxidant nutrient intake and the wet AMD.

The aim of the present study was to estimate the intake of antioxidant nutrients in wet AMD patients.


Subjects and methods

Selection of participants, recruitment and approval

Fifty-two patients (40.4% females and 59.6% males, and mean age 78.9 (SD 6.6) years old) diagnosed of wet age-related macular degeneration, living in the Balearic Islands, Spain, were selected. This study was conducted according to the guidelines laid down in the Declaration of Helsinki and all procedures involving human subjects/patients were approved by the Balearic Islands Ethics Committee. Written informed consent was obtained from all subjects.

Wet AMD diagnosis

Wet AMD was diagnosed from a baseline ophthalmic examination. Visual acuity (Snellen chart), slit lamp examination, intraocular pressure, fundus photographs (Canon 60 CFUD, Japan), fluorescein and indocyanine green angiography (HRA, Heidelberg Engineering), and optical coherence tomography, OCT (Cirrus™ HD-OCT, Carl Zeiss Meditec, Oberkochen, Germany) were taken. Wet AMD was defined by the presence of a subretinal neovascular membrane. Choroidal neovascularitation (CNV) was classified by location into 3 groups: subfoveal, juxta-foveal and extrafoveal, by type into 4: occult, classic, retinal angiomatous proliferation (RAP) and polypoidal choroidal vasculopathy (PCV). Ophthalmic characteristics of participants are summarized in table I.


Anthropometric measurements

Body weight was determined to the nearest 100 g using a digital scale (BAS 60, 00788, Básculas y Balanzas Año Sayol SL, Barcelona, Spain). Height was determined using the scale´s anthropometer (BAS 60, 00788, Básculas y Balanzas Año Sayol SL, Barcelona, Spain) to the nearest mm, with the subject´s head in the Frankfurt plane. The subjects were weighed and measured in light clothes and without shoes.

Waist circumference (WC, measured at the navel in men, and midway between the bottom of the ribs and the top of the hip bone in women) and hip circumference (HC, measured at the tip of the hip bone in men, and at the widest point between the hips and the buttocks in women) both were measured on light clothes. Mid-upper-arm circumference (MUAC, mid-acromiale-radiale distance of the right arm parallel to the long axis of the humerus when the subject was standing erect and the relaxed arm was hanging by the sides). WC, HC and MUAC were measured to the nearest 0.1 cm, using a non-stretchable measuring tape (KaWe, 43972; Kirchner & Wilhelm GmbH, Asperg, Germany). Triceps skin-fold thickness was measured in the right arm using a Holtain skinfold caliper (Tanner/Whitehouse, Crymych, UK), and the mean of three measurements (right arm) was used. Fat mass (FM) was estimated using validated digital bioimpedance (Omron Body Fat Monitor BF306, Omron Healthcare Europe B.V. Hoofddorp, The Netherlands)14, applying the following procedure: Stand with both feet slightly apart; hold the grip electrodes (wrap middle finger around the groove of the handle, place the palm of hand on the top and the bottom electrodes, and put thumbs up, resting on top of the unit); hold arms straight out, at a 90 degree angle to the body, not moving during the measurement; display the measure holding the electrodes. Blood pressure was measure in mmHg using automated machines (Omron No. RX3 Plus, Omron Healthcare Europe B.V., Hoofddorp, The Netherlands). All anthropometric measurements were performed by a well-trained observer in order to avoid the inter-observer coefficients of variation.

Body mass index (BMI, kg/m2), waist-to-hip ratio (WHR, cm = WC/HP), mid-upper arm area (MUAA, cm2 = MUAC2/4π), mid-upper arm muscle area (MUAMA, cm2 = MUAC2/4π), and mid-upper arm fat area (MUAFA, cm2 = MUAA-MUAMA) were also calculated15.

According to the anthropometric reference parameters for the Spanish elderly13 and the European Society for Clinical Nutrition and Metabolism guidelines for Nutrition Screening in the elderly16,17, the prevalence of underweight BMI < 22.0 kg/m2, normal weight 22.0 ≤ BMI < 27.0 kg/m2, and overweight/obesity BMI ≥ 27.0 were calculated.

Waist-hip ratio (WHR) cut-off limits for men and women described elsewhere (> 1 in men, and > 0.9 in women)18,19 were also considered. The prevalence of central obesity was calculated based on WC, using the following cut-off points20,21: > 94 cm in men and > 80 cm in women (moderate risk of cardiovascular diseases, CVD), and > 102 cm in men and > 88 cm in women (high risk of CVD). Fat mass (%) cut-off limits of obesity were > 25% in men and > 33% in women21. MUAMA and the MUAFA (cm2) were compared with the percentiles of reference for the Spanish elderly population13. Considered hypertension cut-off limits were DBP > 90 mmHg and/or SBP ≥ 140 mmHg21,22.


During the visit to the hospital, the participants underwent a standardized interview with a trained dietitian based on an overall questionnaire incorporating socio-demographic status and lifestyle factors, two 24-hour recalls and a validated semi-quantitative food frequency questionnaire23. Socio-demographic variables included (place of residence, place and date of birth, familiar family origin, sex, marital status, home-mates, work situation, and time to residence in Balearic Islands.

Food and nutrient intake

Conversion of food into nutrients was made using a self-made computerized program based on Spanish, European and American Food tables24-27. Composition Tables, and complemented food composition data available for Majorcan food items. Food composition data were specific for raw and cooked foods. Recommended Dietary Intake (RDI) for Spanish population age and gender specific compared the intake of antioxidants26, whereas lutein and zeaxanthin were compared with international references28.


Analyses were performed with Statistical Package for the Social Sciences version 21.0 (SPSS, Inc., Chicago, IL, USA). All tests were stratified by sex and age. Significant differences in prevalence were calculated by means of Χ2. Differences between groups' means were tested using ANOVA. Sequential Bonferroni´s test was applied to control type-I error29. The level was established for P values < 0.05.



Table II shows the anthropometric characteristics for participants, stratified by sex and age. Two age groups were made (< 80 and > 80 years old persons) according to the p50 distribution of the sample. No significant differences were observed between sex and age distribution, but also in anthropometric parameters between age group in men. Young women showed higher weight (kg), BMI (kg/m2), MUAC (cm) and MUAFA (cm2) than their old peers. Moreover, men showed higher weight (kg), height (cm), MUAMA (cm2) and WC (cm), whereas women showed higher MUAFA (cm2), WHR, and FM (%).

The prevalence of underweight was 4.8% men and 9.7% in women, and prevalence of overweight was 61.9% men and 58.1% in women. There were no differences between sexes, but older women showed higher proportions of underweight and lower overweight than their young peers. According to the FM (%) cut-offs around 83% of subjects (90.5% of men and 77.4% of women) were overweighed. Around 79% of participants (76.1% of men and 80.7% of women) showed a risk of CVD, and 42.3% of the studied population (38.1% of men and 45.2% of women) showed hypertension.

Estimation of energy, macro and micronutrient intake stratified by sexes are showed in table III. There were no differences between sexes, except for higher protein, phosphorus and alcohol intake observed in men. The fat and SFA intake of study participants were higher than recommendations for a healthy diet.

Table IV summarizes the estimation of antioxidant nutrient intake of participants. Men and women showed no different intakes, which did not cover recommendations for vitamin E, lutein and zeaxanthin, and zinc. Moreover, high proportion of participants showed inadequate antioxidant nutrient intake, which was more prevalent for lutein and zeaxanthin, zinc, vitamin E, vitamin A and vitamin C. Zinc deficient intake was more prevalent in men than in women.

The food source (%) of antioxidant nutrients of participants was also assessed (table V). The major foods contributors of antioxidants were green beans (vitamin E), carrots (α-carotenes), chard and spinach (lutein andzeaxanthin), cabbage, tomato and carrots (vitamin A), orange, cabbage, pepper and tomato (vitamin C), carrots, chard and spinach (β-carotenes), olive oil (linoleic acid), poultry (zinc), bread, fish and whole grain (selenium), and coffee/infusions (copper).

The percentage of consumers of antioxidant rich foods are shown in table VI. Milk, cheese, egg, carrots, and butter and margarine (vitamin A sources), cauliflower, cabbage, orange, pepper, and strawberry (vitamin C), butter & margarine (vitamin E), green beans, banana, carrots, and mandarin (α-carotenes), tomato, cabbage, and apricot (β-carotenes), tomato, cabbage, and lettuce (lutein and zeaxanthin), olive oil, and nuts (linoleic acid), meta & poultry, and cheese (zinc), legumes, fish, pasta, shellfish & squid, and tuna (selenium), and peas, and butter & margarine (copper) are consumed by at least half of the participants.



This estimation of antioxidant intake showed that most of wet AMD patients usually showed very low intake of lutein and zeaxanthin, zinc, vitamin A and vitamin E. Moreover, high proportion of patients also showed inadequate intake of vitamin C and selenium. The intake of other antioxidant nutrients widely achieved the recommendations. These results suggest that any intervention on wet AMD patients must to be carried out to enhance the antioxidant nutrient intake that were below the recommendations, which is in accordance with previous findings on AMD patients3,30.

It is important to emphasize that the highest nutrient deficiency was observed on lutein and zeaxanthin, since more than 60% of wet AMD patients showed serious deficient intake (< 1/3 RDI) of these nutrients. POLA study31 evaluated the diet of Mediterranean population and observed that the increase of lutein and zeaxanthin intake, by means of dietary modifications or nutritional supplements, had preventive effect of AMD and cataract. Previous findings pointed out the need to increase the knowledge on the relationship of lutein and zeaxanthin and the reduction of the risk of developing AMD or slow the progression to late-stage AMD28. Therefore, it would be useful to know the food source of these nutrients, and also if the diet of patients contained these foods.

A first analysis of the food source of antioxidant nutrients of participants showed the main dietary contributors of antioxidants. However, when the proportion of consumers of these foods among the participants in the study were analysed, we observed that most consumed antioxidant rich foods (tomatoes, carrots, spinaches, oranges, cabbages, cheese, pulses, green beans) only represented low contributions to antioxidant intake (i.e.: All the participants stated to consume tomato, but it only contributed 14.7% of vitamin A intake, 10.3% of vitamin C, 4.7% of vitamin E, 17.8% of α-carotenes, 9.0% of β-carotenes, 4.1% of lutein & zeaxanthin, and 3.5% of copper). Therefore, it would be desirable to increase the servings or the total amount of the antioxidant rich foods, enough to widely cover the recommendations.

Furthermore, the fat and SFA intake of study participants were higher than the recommended nutritional objectives for the Spanish population32. It has been pointed out that a high dietary intake of fat is associated with a higher prevalence or incidence of early or late AMD33. Moreover, a high proportion of the participants showed fat mass over the cut-off limits34, and it has been also pointed out that a relative lack of macular pigment is associated with adiposity, and may underlie the association between body fat and risk for AMD progression35. These results also agree our findings that most of participants showed a risk of CVD, and hypertension, which also support the general hypothesis that AMD shares multiple risk factors with cardiovascular disease36.

These results give an insight into the dietary habits of wet AMD patients in the Balearic Islands, who may be successful in meeting health nutritional recommendations, thereby also providing clues for the development of future food-base dietary guidelines (FBDG) that would be relevant to the health of this population. Realistic FBDG should be established on the basis of a given socio-economic context. They must be drawn from population-based epidemiological studies, and it will be essential to analyse prevalent food consumption patterns in order to be realistic for the population37. Dietary guidelines need to be based on an assessment of the available scientific information on diet and the maintenance of good health. This assessment needs to include an evaluation of the prevailing diet and nutrient intake compared to any recommended optimum. Therefore, a stepwise approach is needed to address large disparities between actual and ideal dietary habits38.

Finally, it is also necessary to consider that the study participants were elderly people (78.9 ± 6.6 y.o.) and observed antioxidants intakes deficiencies could be associated with physiological factors (partial or total loss of teeth, modifications in the senses of taste and smell, lack of appetite or a heightened feeling of satiety)39,40, physical factors that impede the acquisition or preparation of foods; depression and other psychological factors, often associated with a lack of appetite or the rejection of food41; and economic and social factors that limited the purchase of certain foods1.

In any case, the food pattern of wet AMD patients should be improved by means of an increase in the consumption of antioxidant rich foods, and a decrease in SFA rich foods, which is in accordance with a previous study that evidenced the overall diet quality, may play an important role in modulating the risk of AMD36. The promotion of this food pattern would constitute a good strategy to develop healthy FBDG among the Balearic Islands wet AMD patients.


Limitations of the study

The methodology of this study have some limitations, as for example the 24 h recalls provides information on food intake, and because the data collection occurs after consumption, this method does not affect an individual´s food choices on a given day42. At least two non-consecutive administrations are necessary to assess usual intakes, to reduce dependency on intake from the previous day and by household food avai-lability42. Accordingly, we applied two 24 h nonconsecutive recalls in this study. Although 24 h recalls collects data soon after intake, recalls have also limitations related to memory and bias42. Moreover, the sample size is small (n = 52); then, only an estimation of antioxidant intake can be considered. Finally, this study was a cross-sectional study, and it can be thought of as providing a "snapshot" of the frequency and characteristics of a disease in a population at a particular point in time, However, since exposure and disease status are measured at the same point in time, it may not be possible to distinguish whether the exposure proceeded or followed the disease, and thus cause and effect relationships are not certain.


Authors' contributions

JLO and JAT conceived, designed and devised the study, MEZ, MMB, JAA; AP, JLO and JAT collected and supervised the samples, and analyzed the data and wrote the manuscript. JLO and JAT supervised the study. JLO and JAT obtained funding.


Conflict of interest statement

The authors state that there are no conflicts of interest.



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Josep A. Tur.
Research Group on Community Nutrition and Oxidative Stress.
University of the Balearic Islands and CIBERobn.
Guillem Colom Bldg. Campus.
07122 Palma de Mallorca. Spain.

Recibido: 25-X-2013.
1.a Revisión: 1-XII-2013.
2.a Revisión: 13-I-2014.
Aceptado: 16-I-2014.

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