Red palm oil in the maternal diet improves the vitamin A status of lactating mothers and their infants

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1 Red palm oil in the maternal diet improves the vitamin A status of lactating mothers and their infants Abstract Improvement of the vitamin A status of lactating mothers and their nursing infants following maternal palm oil consumption was comparable to that following supplementation with purified β-carotene. Mothers who consumed β-carotene as red palm oil had 2.1- and 2.5-fold increases in their serum and milk β-carotene concentrations, respectively, and 2.8- and 3.2-fold increases in their serum and milk α-carotene concentrations, respectively. Infant serum retinol concentrations were significantly increased following maternal supplementation with red palm oil or β-carotene. Maternal intake of red palm oil or β-carotene supplements did not alter infant serum carotenoids, maternal serum retinol, or milk retinol. Because the local diet includes foods prepared with oil, the possibility that red palm oil could provide a significant source of provitamin A carotenoids for Honduran women and children should be further investigated. Introduction On the basis of meta-analysis of intervention trials conducted over the past decade, it is estimated that vitamin A supplementation can reduce childhood mortality in developing countries by as much as 30% [1]. However, in spite of widespread vitamin A supplementation programmes in these countries for more than two decades, vitamin A deficiency remains a major problem because of logistical and economic obstacles to their implementation [2]. It is estimated that in a single year, vitamin A deficiency still contributes to over one million childhood deaths and is responsible for blindness L. M. Canfield is affiliated with the Department of Biochemistry, University of Arizona, in Tucson, Arizona, USA. R. G. Kaminsky is affiliated with the Universidad Nacional Autónoma de Honduras in Tegucigalpa, Honduras. Mention of the names of firms and commercial products does not imply endorsement by the United Nations University. in about half a million children. In response to this problem, the World Bank has recommended fortification of common foods as an additional strategy [3]. A number of options are currently being investigated, including biscuits fortified with β-carotene [4], dietary palm oil [3, 5], and β-carotene-containing foods [6 9]. We have previously demonstrated [10, 11] that supplementation of mothers with β-carotene results in a substantial increase in serum carotenoids in maternal serum and milk. In addition, others have reported that vitamin A supplementation of mothers improves the vitamin A content of breastmilk and the vitamin A status of nursing infants [12]. Building on these results, we investigated the effect of supplementing lactating mothers who were low in vitamin A with β-carotene or red palm oil. Our hypothesis was that increasing the provitamin A intake of the mother with foods high in β- carotene or with β-carotene-fortified foods can increase the vitamin A content of maternal milk, thus improving the vitamin A status of the mother infant pair. Although they are not currently marketed in Honduras, red palms are grown commercially on the north coast of Honduras and therefore are potentially accessible to the Honduran population. Staples of the Honduran diet, such as plantains and black beans, are typically prepared with oil. Furthermore, in spite of early concerns about atherogenicity, it is now clear that red palm oil is no more atherogenic, and possibly less so, than other plant oils [13 15]. In addition, red palm oil is a rich source of energy and vitamin E as well as of α-carotene, which is also a provitamin A carotenoid. Therefore, we chose red palm oil as a vehicle for our studies with the hope that introduction of this oil into the diet of mothers could eventually contribute substantially to a sustainable solution to vitamin A deficiency in Honduras. Methods Studies were conducted from November 1993 through June 1997 in three colonias (urban districts) near 144 Food and Nutrition Bulletin, vol. 21, no , The United Nations University.

2 Red palm oil in the maternal diet Tegucigalpa: Via Cristina, Los Pinos, and Via Alemania. The methods of the first two studies have been described in detail elsewhere [16, 17]. The design of the Via Alemania study was similar to that of the other two, except that it was carried out over one month. The total amount of β-carotene supplement provided in each of the studies was 90 mg. Subjects Lactating mothers and their nursing infants (aged 1 24 months) were recruited from the marginal barrios of Tegucigalpa. Mothers provided informed consent in accordance with the regulations of the University of Arizona Human Subjects Committee. Mothers who smoked, were ill, had infants with chronic illnesses, or had infants less than one month old were excluded from the study. Immediately after their arrival in the clinic, health histories for mothers and infants and 24-hour dietary recalls were obtained from the mothers. Supplements were administered with a breakfast that provided about 8 g of fat. The meal consisted of tortillas, black beans, crema (a local sour cream product), and 250 ml of whole milk. The β-carotene supplements were provided as capsules (BASF), beadlets (Hoffmann LaRoche), or red palm oil. The β-carotene concentrations of the supplements were verified by high-performance liquid chromatography (HPLC). Milk was obtained from the mothers at mid-morning by manual expression. Blood samples were obtained from the mothers and infants by a trained, Spanish-speaking phlebotomist using venipuncture. Sample collection and handling The blood samples were transported to a clinical laboratory in Tegucigalpa where serum was prepared and stored at 20 C along with milk samples. The frozen milk and serum samples were hand-carried by air to the laboratory in Arizona by one of the research staff. On arrival in Tucson, the samples were stored at 70 C until they were analysed. Carotenoids and retinol were analysed in serum and milk by HPLC, as previously 145 described [11, 18]. The lipid content of the milk was determined as the percentage of the total volume by creamatocrit assay [19]. Dietary analyses Because the diets of the mothers contained very few foods high in carotenoids, and because only limited information on individual carotenoids was available for Honduran foods, a qualitative rather than a quantitative analysis of the diets was performed. Serving sizes were recorded by volume (e.g., ½ cup of vegetables, ½ cup of milk or ice cream), piece (e.g., one piece of fruit), or weight (e.g., 100 g of meat). Statistical analysis Standard descriptive statistics were performed using Microsoft Excel 5.0 or STATA (College Station, Tex., USA). Results and discussion The results of three studies from our laboratory designed to determine the effect of β-carotene supplementation of lactating mothers on the vitamin A status of the mother infant pair are shown in tables 1 to 3. Supplementation of lactating mothers with β-carotene or dietary red palm oil significantly increased their serum and milk β-carotene levels and the serum retinol levels of their nursing infants. The total dosage of β- carotene administered in all studies was 90 mg. Since the duration of the studies varied from 5 to 30 days (table 4), in a strict sense they cannot be directly compared. However, the results clearly demonstrate that the effectiveness of red palm oil is comparable to that of β-carotene supplements in improving the vitamin A status of lactating mothers and their infants. Maternal diets were monotonous, consisting mostly of beans and tortillas, with an occasional serving of meat and dairy products. The diets were extremely low in fruits and green vegetables. Dietary data for the Via Cristina and the Los Pinos studies have previously been TABLE 1. Changes in β-carotene concentration of mothers serum Study Supplement Initial Final Fold increase Via Cristina β-carotene beadlets 0.09 ± ± 0.39 a 9.7 Los Pinos BASF β-carotene 0.21 ± ± 0.02 b 1.2 Palm oil 0.32 ± ± 0.06 a 2.1 Via Alemania β-carotene beadlets 0.28 ± ± 0.35 a 2.7 a. p <.01 (paired, two-tailed t test). b. p <.05 (paired, two-tailed t test).

3 146 TABLE 2. Changes in β-carotene concentration of breastmilk Study Supplement Initial Final Fold increase Via Cristina β-carotene beadlets 17.0 ± ± 16.6 a 5.8 Los Pinos BASF β-carotene 38.9 ± ± 31.9 a 1.6 Palm oil 35.3 ± ± 37.7 a 2.5 Via Alemania β-carotene beadlets 23.9 ± ± 39.1 a 3.0 a. p <.001 (paired, two-tailed t test). TABLE 3. Changes in retinol concentration of infants serum Absolute Study Supplement Initial Final increase (µmol/l) Via Cristina β-carotene beadlets 0.88 ± ± 0.25 a 0.14 Los Pinos BASF β-carotene 0.71 ± ± Palm oil 0.64 ± ± 0.04 a 0.10 Via Alemania β-carotene beadlets 0.48 ± ± 0.13 a 0.07 a. p <.01 (paired, two-tailed t test). TABLE 4. Outline of study protocols Feature Via Cristina Los Pinos Via Alemania Supplement β-carotene beadlets a β-carotene capsules b β-carotene beadlets a Red palm oil c β-carotene dosage 3 30 mg 6 15 mg mg Treatment days 1, 3, 4 1, 3, 5, 7, 9, 10 1, 14 Sample collection days 1, 3, 5 1, 10 1, 14, 30 Duration of study (days) No. of subjects Mothers palm oil β-carotene Infants palm oil β-carotene a. The supplement was provided by Hoffmann LaRoche. b. A powdered preparation of β-carotene (BASF, 15 mg), dispersed in cornstarch and packaged in an opaque capsule. β-carotene concentrations in the BASF preparation were verified by HPLC. c. The red palm oil fraction (Palm Oil Research Institute of Malaysia) contained 0.55 mg of β-carotene and 0.25 mg of α-carotene per milliliter. We estimated that the effective amount of provitamin A carotenoid furnished by α-carotene in palm oil was < 2 mg (12.5% of the total dose); this amount was not considered in the calculations. described in detail [16, 17], and the diets in the Via Alemania study were similar to these. For example, in the Via Alemania study a third of the women reported consuming no fruits or vegetables in the 24 hours before completing the questionnaire. Further, although vitamin A consumption was very low, most of it, surprisingly, was in the form of retinol from animal sources or fortified foods, not in the form of provitamin A carotenoids. In Honduras the sugar supply has been fortified with vitamin A since 1993; however, the extent of industry compliance is unclear at present [20]. Although oil is used for cooking, lard is the most common fat used for cooking. However, foods prepared with oil are widely consumed. Oils containing carotenoids, such as red palm oil, are potentially effective vehicles for increasing vitamin A intake in this population of mothers and infants. Changes in maternal serum β-carotene concentrations following the various treatments are shown in

4 Red palm oil in the maternal diet table 1. The initial concentrations of serum carotenoids were substantially lower than those of mothers in the United States [10, 11, 18]. The largest changes were in response to β-carotene beadlets in the Via Cristina study, where the initial concentrations were lowest (approximately 10% of those of mothers in the United States). Since this study was conducted in winter and the others in spring, seasonal variation may have been responsible, at least in part, for the noticeably lower maternal serum and milk carotenoid concentrations. Interestingly, infant serum retinol concentrations were not lower than those in the other studies, suggesting that maternal carotenoid stores are mobilized to provide a vitamin A source for the infant. The smallest changes in serum carotenoids were in response to the powdered β-carotene preparation, apparently due to its lower bioavailability compared with that of water-miscible beadlets [21]. Notably, palm oil treatments compared favourably to beadlets when the starting serum concentrations were the same, despite the difference in duration of supplementation. In this regard, no further increase was seen after day 3 (60 mg dosage) in the Via Cristina study or day 14 (45 mg) in the Via Alemania study, suggesting that a maximum increase is reached within a few days. The other major carotenoids we analysed, α-carotene, β-cryptoxanthin, lycopene, and lutein/zeaxanthin, were unaffected by any of the β-carotene treatments. Similarly, the concentrations of β-cryptoxanthin, lycopene, and lutein/zeaxanthin were unaffected by palm oil treatments. However, serum α-carotene was increased almost threefold in mothers and 1.4-fold in infants [17]. Maternal serum retinol concentrations were not affected by any of the treatments. Changes in milk β-carotene are shown in table 2. As in the case of serum β-carotene, the β-carotene beadlets in the Via Cristina study produced the largest increases. Similarly, the initial milk carotenoid concentrations of mothers in the Via Cristina study were substantially lower than in the other two colonias. Notably, the response to palm oil treatment was comparable to treatment with beadlets in the Via Alemania and Los Pinos studies, where the initial concentrations were similar. The mothers in these colonias nurse frequently and on demand, so that full breast expression is not possible. Therefore, to control for changing lipid concentrations over the nursing episode, milk concentrations were normalized to lipid. Since normalization gave comparable results, there was no significant effect of changing lipid concentrations over the nursing episode. Milk retinol and other carotenoids were not significantly affected by any of the treatments. 147 Infant serum retinol was significantly increased by both maternal β-carotene supplementation and red palm oil consumption. As in the case of serum and milk carotenoids, the largest increases were in response to β-carotene beadlets in the Via Cristina study. However, the increases in response to palm oil supplementation were similar to those in response to β-carotene supplementation in the Via Alemania study. The powdered β-carotene preparation was less effective than the other treatments (table 3). The initial serum retinol concentrations of the infants ranged from 0.48 to 0.88 mmol/l. The average concentration in all studies was 0.63 mmol/l, which was less than the World Health Organization recommended value for developing countries (0.7 mmol/l). Our results are in agreement with a 1996 national survey of the Honduran Ministry of Health, which found that over 30% of all Honduran children 12 to 71 months of age had low levels of vitamin A (serum retinol between 0.35 and 0.70 mmol/l) and 10% were vitamin A deficient (serum retinol less than 0.35 mmol/l) [20, 22]. With the advent of Hurricane Mitch, unfortunately, the vitamin A status of Honduran children almost certainly has now worsened, increasing the urgency of finding a sustainable solution to the problem of vitamin A deficiency in this population. In summary, both β-carotene supplementation of mothers and red palm oil in the maternal diet improved the vitamin A status of the mother infant pair in Honduran colonias. Red palm oil is comparable in effectiveness to supplementation with β-carotene. Both treatments significantly increased serum and milk β-carotene and infant serum retinol. The initial vitamin A status of the infants was marginal-to-deficient, and the maternal diet was low in vitamin A. Because the local diet typically includes foods prepared with oil, the possibility that dietary red palm oil could provide a significant source of provitamin A carotenoids for Honduran women and children should be further investigated. Acknowledgements This work was supported by grants from the National Institutes of Health, the OMNI Research Program, and the Palm Oil Research Institute of Malaysia (PORIM). We thank Yun Liu, Manping Liu, and Herminia Valladores for technical support. Special thanks go to the mothers and children of Via Cristina, Via Alemania, and Los Pinos, without whose participation and cooperation the work would not have been possible.

5 148 References 1. Fawzi WW, Chalmers TC, Herrera MG, Mosteller F. Vitamin A supplementation and child mortality: a metaanalysis. JAMA 1993;269: Humphrey JH, West K Jr, Sommer A. Vitamin A deficiency and attributable mortality among under 5-year olds. Bull WHO 1992;70: Solomons NW. Plant sources of vitamin A and human nutrition: red palm oil does the job. Nutr Rev 1998; 56: van Stuijvenberg ME, Kvalsvig JD, Faber M, Kruger M, Kenoyer DG, Benadé AJ. Effect of iron-, iodine-, and β- carotene-fortified biscuits on the micronutrient status of primary school children: a randomized controlled trial. Am J Clin Nutr 1999;69: Manorama R, Brahmann GN, Rukmini C. Red palm oil as a source of β-carotene for combating vitamin A deficiency. Plant Foods Hum Nutr 1999;49: Bulux J, Quan de Serrano J, Giuliano A, Perez E, Lopez CY, Rivera C, Solomons NW, Canfield LM. Plasma response of children to short-term chronic β-carotene supplementation. Am J Clin Nutr 1994;59: Jalal F, Nesheim MC, Zulkarnain A, Sanjur D, Habicht JP. Serum retinol concentrations in children are affected by food sources of β-carotene, fat intake and anthelmintic drug treatment. Am J Clin Nutr 1998;68: Solomons NW, Bulux J. Identification and production of local carotene-rich foods to combat vitamin A malnutrition. Eur J Clin Nutr 1997;51:S Canfield LM, Bulux J, Quan de Serrano J, Rivera C, Lima AF, Lopez CY, Perez R, Khan LK, Harrison GG, Solomons NW. Plasma response to oral β-carotene in Guatemalan schoolchildren. Am J Clin Nutr 1991;54: Canfield LM, Giuliano A, Neilson E, Blashill B, Graver E, Yap H. Kinetics of the response of milk and serum β-carotene to daily β-carotene supplementation in healthy, lactating women. Am J Clin Nutr 1998;67: Canfield LM, Giuliano AR, Neilson EM, Yap HH, Cui HA, Blashill BM. β-carotene in breast milk and serum is increased following a single β-carotene dose. Am J Clin Nutr 1997;66: Stoltzfus RJ, Hakimi M, Miller KW, Rasmussen KM, Dawiesah S, Habicht JP, Dibley MJ. High dose vitamin A supplementation of breast-feeding Indonesian mothers: effects on the vitamin A status of mother and infant. J Nutr 1993;123: Choudhury N, Tan L, Truswell AS. Comparison of palmolein and olive oil: effects on plasma lipids and vitamin E in young adults. Am J Clin Nutr 1999;61: Ghafoorunissa, Reddy V, Sesikaran B. Palmolein and groundnut oil have comparable effects on blood lipids and platelet aggregation in healthy Indian subjects. Lipids 1999;30: Ghafoorunissa. Nutrition and health implications of palm oil in Indian diets. Indian J Med Res 1999;102: Canfield LM, DeKaminsky R, Taren DL, Mahal Z. Maternal β-carotene supplementation: a strategy for improving the vitamin A status of the mother infant dyad. J Nutr Biochem 1999;10: Canfield LM, Kaminsky RG, Shaw EH, Sander JK. Dietary palm oil improves the vitamin A status of the mother infant dyad. Am J Clin Nutr 1999 (in press). 18. Jackson JG, Lien EL, White SJ, Bruns NJ, Kuhlman CF. Major carotenoids in mature human milk: longitudinal and diurnal patterns. J Nutr Biochem 1998;9: Lucas A, Gibbs JAH, Lyster RLJ, Baum JD. Creamatocrit: simple clinical technique for estimating fat concentration and energy value of human milk. BMJ 1978;1: Nestel P, Melara A, Rosado J, Mora JO. Vitamin A deficiency and anemia among children months old in Honduras. Revista de Salud Publica 1999;6: Papas AM. Carotenoids and human health: current issues. Xerophthalmia Club Bull 1999;70: Secretaria de Salud, Tegucigalpa, Honduras. Encuesta nacional sobre micronutrientes (National Honduran micronutrient survey), Tegucigalpa: Secretaria de Salud, 1998:28 9.

Women by area: Urban F Women by area: Rural F

Women by area: Urban F Women by area: Rural F Vitamin and Mineral Nutrition Information System (VMNIS) WHO Global Database on Vitamin A Deficiency The Vitamin A Deficiency database includes data by country based on xerophthalmia and/or serum or plasma