Dietary source of vitamin B12 intake and vitamin B12 status in female elderly Koreans aged 85 and older living in rural area

Chung Shil Kwak; Mee Sook Lee; Hae Jeung Lee; Jin Yong Whang; Sang Chul Park

doi:10.4162/nrp.2010.4.3.229

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Kwak, Lee, Lee, Whang, and Park: Dietary source of vitamin B12 intake and vitamin B12 status in female elderly Koreans aged 85 and older living in rural area

Original Article

Nutrition Research and Practice

Nutrition Research and Practice 2010; 4(3): 229-234.

Published online: 29 June 2010

DOI: https://doi.org/10.4162/nrp.2010.4.3.229

Dietary source of vitamin B₁₂ intake and vitamin B₁₂ status in female elderly Koreans aged 85 and older living in rural area

Chung Shil Kwak¹, Mee Sook Lee², Hae Jeung Lee³, Jin Yong Whang¹, Sang Chul Park^1,⁴

¹Institute on Aging, Seoul National University, 199-1 Dongsoong-dong, Jongno-gu, Seoul 110-810, Korea.

²Department of Food and Nutrition, Hannam University, Daejeon 305-811, Korea.

³Center for Nutrition Policy and Promotion, Korea Health Industry Development Institute, Seoul 156-800, Korea.

⁴The Aging and Apoptosis Research Center, Seoul National University, Seoul 110-810, Korea.

Corresponding Author: Chung Shil Kwak, Tel. 82-2-740-8506, Fax. 82-2-742-0626, kwakcs@snu.ac.kr

Received 24 February 2010 Revised 12 May 2010 Accepted 22 May 2010

(open-access):

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Recently, we found and analyzed vitamin B₁₂ in some Korean traditional plant foods which had not reported, yet. This study was to investigate vitamin B₁₂ intake and its dietary sources and the vitamin B₁₂ status in the very old elderly Koreans. We measured serum vitamin B₁₂ level and estimated the amounts of vitamin B₁₂ intake from different dietary sources in female elderly Koreans aged 85 and over who had consumed a relatively low animal traditional diet for the whole life. The average age of the subjects (n = 127) was 98.0 years (85-108 years). The assessment on energy and nutrient intake involved a one-day 24-hour recall, and serum vitamin B₁₂ concentration was measured by radioimmunoassay. Overall diet pattern was not different between the 85-99 yr-old group and centenarians, except centenarians were taking more dairy product. The average ratio of plant food to animal food consumption was 87.5:12.5 in weight. The average vitamin B₁₂ intake of our subjects was 3.2 µg/day, and 52.7% of subjects consumed under estimated average requirement, 2.0 µg/day. On dietary source, 67.3% of dietary vitamin B₁₂ was from meat, eggs and fishes and 30.6% was from plant foods, such as soybean-fermented foods, seaweeds, and kimchi. The average serum vitamin B₁₂ concentration was 450.5 pg/mL, and low serum vitamin B₁₂ (< 200 pg/mL) was found in 9.6% of subjects. Dietary vitamin B₁₂ intake was significantly lower in subjects with low serum vitamin B₁₂ (0.79 µg/day) than those with normal serum vitamin B₁₂ (3.47 µg/day). There were no significant difference in vitamin B₁₂ intake and its dietary sources and serum vitamin B₁₂ level between the 85-99 yr-old group and centenarians. In conclusion, several plant-origin foods including seaweed, soybean-fermented foods, and kimchi, may contribute significantly to good vitamin B₁₂ status in very old elderly Koreans.

Keywords: Female elderly, dietary source of vitamin B₁₂, serum vitamin B₁₂ level

Introduction

The prevalence of vitamin B₁₂ deficiency was underestimated in the past for several reasons, including the erroneous belief that deficiency is unlikely except in strict vegetarians or patients with pernicious anemia, and that it usually takes ~20 y for stores of the vitamin to become depleted [1].

Numerous reports have indicated the increasing prevalence of low vitamin B₁₂ levels among different segments of the general population [2-5]. Poor vitamin B₁₂ status is associated with neurological problems [6,7], hematological disorders [6,8], and other health-related conditions, including poor cognition and Alzheimer's disease [9,10], depression [11], hearing loss [12], cancer [13], and poor bone health [14,15]. Recently, the rapid aging of many populations has increased attention to vitamin B₁₂.

It is known that more vegetarians or elderly people suffer from vitamin B₁₂ deficiency compared to omnivores or younger adults. Because natural sources of vitamin B₁₂ in human diets have known to be restricted to animal-origin food, it has been believed that those people with low animal food diets are more susceptible to cobalamin deficiency [16]. However, vitamin B₁₂ also exists in soybean-fermented foods, seaweeds, and tea leaves [17-19]. Recently, we reported that doenjang, a Korean soybean-fermented paste, contained 0.04-1.85 µg cobalamin/100 g, and that dried laver contained 66.76 µg/100 g (laver is normally consumed in dried form); these figures are surprisingly high compared to those of 0.9-1.2 µg/100 g for eggs [20], and also 1.33 µg per one sheet of dried laver (2 g) was higher than 0.45-0.6 µg per one egg (50 g) when calculated B₁₂ content per one serving size.

In terms of the relationship between vitamin B₁₂ and aging, it has been reported that atrophic gastritis increases with aging, thereby inducing decreased production of the gastric acid and digestive enzymes that are needed to cleave protein-bound vitamin B₁₂ from the natural chemical form of vitamin B₁₂ found in foods. Therefore, Americans aged over 50 years have been advised to consume vitamin B₁₂ in the crystalline form [6].

Historically, Koreans have consumed a plant-based diet including steamed rice, staple food. Even today, the elderly, especially those living in rural areas, adhere to this traditional diet, even though young people have moved toward Western dietary patterns. There has been concern that vitamin B₁₂ status among the elderly is poor. However, data are not available on vitamin B₁₂ status and intake among elderly Koreans, and only a few reports have been published regarding vitamin B₁₂ intake or serum vitamin B₁₂ level among young adults [21,22] and pregnant women [23]. Moreover, the vitamin B₁₂ intake in extant reports are considered to represent underestimates because the Korean national database on vitamin B₁₂ content in foods does not contain data on plant-origin foods. Recently, we analyzed some plant-origin foods widely consumed in Korea [20], and updated this database accordingly.

In this study, we first assessed the vitamin B₁₂ status and intake pattern among very old elderly female Koreans living in rural areas by measuring serum vitamin B₁₂ level and estimating daily vitamin B₁₂ intake. Especially, we were interested in how much some unique plant-origin foods consumed by Koreans, such as soybean-fermented foods, seaweeds and kimchi, contribute to their vitamin B₁₂ intake.

Subjects and Methods

Subjects

Females aged 85 years and older were recruited in rural areas in Korea during summer of 2003 to 2005. Candidates were randomly selected based on birth records, and those living in facilities were excluded. Our research team including dietician, nurse, medical doctor and students visited each home after getting the consent. We kept the ethical and standard of institutional review board of author's institute and the Helsinki Declaration during this study. For recruiting subjects, we explained about the purpose and process of this study to Government officer and village leaders, and also explained and took the consent from every candidate or her/his family member. Finally, 127 subjects, including 70 centenarians, participated in our study. The age of the subjects ranged from 85 to 108 years, and the average age was 98.0 ± 5.7 years. The age distribution of subjects is shown in Table 1.

Food and nutrient intake including vitamin B₁₂

Well-trained interviewer wrote down one-day diet history of each subject by 24-h recall and weighing method with the help of her/his family members. The intake of dairy product, meat and eggs, fish and shellfish, cereals, potatoes and starch, sweets, legumes and tofu, vegetables and seaweeds, fruits, and soybean-fermented foods, as well as total food intake were calculated. The energy and nutrient intake of subjects were calculated using a computer software package, CAN-Pro 2.0, developed by the Korean Nutrition Society. In particular, we calculated daily vitamin B₁₂ intake and the proportions of vitamin B₁₂ from plant-origin foods such as soybean-fermented foods, seaweeds, kimchi and etc.

Blood test

Blood samples were drawn and delivered the same day to the laboratory in a cold iced box. Serum vitamin B₁₂ level was assessed by radioimmunoassay using a SimulTRAC-SNB Radioassay kit (ICN, New York, USA).

Statistical analysis

Analyses were performed using SAS version 9.2 software (SAS Institute, Inc., Cary, NC). All data were expressed as means and standard deviations, frequencies, or percentages. Statistically significant differences between groups were determined by t-test or Chi-square test.

Results

Food intake

The food intake pattern is shown in Table 2. The average total food intake of subjects was 761.1 g/day. Meals were comprised primarily of plant foods (87.5% of total) such as cereals, legumes and their products, vegetables, fruits, and so on. The average intake of cereals was 232.6 g/day, and almost of this consumption derived from rice, a staple food for Koreans. The subjects consumed 26.3 g/day of legumes, nuts, and tofu, a representative soybean product consumed in Korea. They consumed 216.1 g/day of vegetables and seaweeds, including 82.2 g/day of kimchi, the most popular vegetable-fermented food in Korea, and large portion of vegetable intake was derived from various blanched vegetables (namul in Korean). They also consumed 23.1 g/day of soybean-fermented foods, such as doenjang, chungkookjang, gochujang, and ganjang. The average fruit intake was 71.0 g/day. On the other hand, subjects consumed 95.5 g/day of animal foods (12.5% of total), including 52.7 g of meat, poultry, and eggs; 30.9 g of fish and shellfish; and 10.8 g of dairy products.

On comparing the food intake patterns between the 85-99 yr-old group and centenarians, centenarians consumed significantly more dairy products (P < 0.05) and sweets (P < 0.001) than the 85-99 yr-old group did, because some centenarians enjoyed candy and consumed yogurt. However, no significant differences in the consumption of the other food groups or in the ratio of animal to plant food intake were found.

Energy intake and vitamin B₁₂ Intakes

Daily energy and protein, fat, carbohydrate and vitamin B₁₂ intake of subjects are shown in Table 3. The average energy intake was 1,229 ± 457 kcal/day which is 76.8% of the estimated energy requirement (EER) for Korean women aged 75 and over, 1,600 kcal/day [24]. The average energy intakes in the 85-99 yr-old group and centenarians were not significantly different; 1286 ± 510 kcal/day in the 85-99 yr-old group, and 1,186 ± 418 kcal/day in centenarians. The subjects consumed 49.3 g of protein/day, 109.6% of the recommended intake (RI) of protein, 45 g/day [24], even though they consumed less animal foods. As shown in Fig. 1, 70.6% of energy was from carbohydrates (220.5 g/day); 15.5% from protein and 13.9% from fat, and these proportions were not significantly different between the two age groups.

In terms of vitamin B₁₂, our subjects consumed 3.17 ± 4.77 µg/day of vitamin B₁₂, which is about 132% of RI for Korean adults, 2.4 µg/day [24]. There was no significant difference in daily mean vitamin B₁₂ intake between the two age groups (2.48 ± 3.00 µg/day in the 85-99 yr-old group and 3.73 ± 5.79 µg/day in centenarians). In total subjects, 52.7% consumed less than 2.0 µg/day, estimated average requirement (EAR) for vitamin B₁₂ for Korean adults (Table 3).

Dietary source of vitamin B₁₂

Dietary sources of vitamin B₁₂ are listed in Table 4. The percentages of vitamin B₁₂ intake derived from animal food and plant food were 69.4% and 30.6% of total vitamin B₁₂ intake, respectively. The primary source of vitamin B₁₂ was clearly meat, eggs, and fish, which provided 2.45 ± 4.52 µg/day (67.3% of total intake); the secondary was soybean-fermented foods, providing 0.07 ± 0.13 µg/day (14.5%); the tertiary was seaweeds, providing 0.59 ± 1.58 µg/day (10.8%) (Table 4 & Fig. 2), and kimchi also provided 0.02 ± 0.03 µg/day (4.3%). The average intake of vitamin B₁₂ and the sources did not differ between the two age groups.

Serum vitamin B₁₂ concentration and association with dietary intake

The mean serum vitamin B₁₂ concentration was 450.5 ± 226.9 pg/mL; 477.1 ± 172.7 pg/mL in the 85-99 yr-old group and 441.5 ± 243.1 pg/mL in centenarians without significant difference between the two age groups (Table 5).

It has been widely accepted that adults with serum vitamin B₁₂ level under 200 pg/mL are highly likely to be vitamin B₁₂ deficient [25,26]. By the same criteria, 9.6% (4.8% of the 85-99 yr-old group and 11.3% of centenarians) were assessed to be vitamin B₁₂ deficient. The prevalence of low serum vitamin B₁₂ was not significantly different between the two age groups (Table 5).

It was not observed a significant correlation between serum vitamin B₁₂ concentration and dietary intake (P=0.4769). However, vitamin B₁₂ intake was significantly lower (P < 0.001) in the subjects with low serum vitamin B₁₂ (0.79 ± 0.79 µg/day) than those in normal subjects (3.47 ± 5.72 µg/day) (Table 6).

Discussion

It is well known that the metabolism of vitamin B₁₂, folate, and homocystein are associated in humans and play very important roles in preventing cognitive impairment in the elderly [27-29]. Risk factors for vitamin B₁₂ deficiency include low animal protein intake, malabsorption associated with atrophic gastritis or Helicobacter pylori infection, pancreatic or intestinal pathology, and gastric acid-reducing medications [6,30-32]. Malabsorption of vitamin B₁₂ from food is the main cause of deficiency in the elderly and explains why depletion occurs with aging. The condition is caused by atrophy of gastric mucosa and the gradual loss of gastric acid, which releases the vitamin from food. The low gastric pH that occurs as a result of gastric atrophy can also increase bacterial overgrowth in the upper intestine, which results in less absorption of protein-bound vitamin B₁₂. Approximately, 10-30% of older adults suffer from malabsorption of protein-bound vitamin B₁₂ [6].

Serum vitamin B₁₂ concentrations < 150 pmol/L (200 pg/mL) indicates frank vitamin B₁₂ deficiency, but there is no widely accepted biochemical cutoff for marginal or preclinical vitamin B₁₂ deficiency or vitamin B₁₂ adequacy [6]. The use of both serum vitamin B₁₂ and methylmalonic acid (MMA) or holotranscobalamin is more recommended to improve diagnosis of vitamin B₁₂ deficiency [25,26]. However, it is limitation s to use MMA level for simple screening of the vitamin B₁₂ status because MMA measurement needs mass spectrometry which is not easily available and needs trained labor and high cost.

It has been reported that, depending on the biochemical criteria for vitamin B₁₂ and/or MMA, approximately 5 - 20% of elderly individuals are deficient in vitamin B₁₂ in the Americans [1,6,30,33]. Pfeiffer et al. [34] reported that the prevalence of vitamin B₁₂ deficiency (serum concentration < 200 pg/mL) in US population varied by age group and affected ≤ 3% of those aged 20-39 y, ~4% of those aged 40-59 y and ~6% of persons aged ≥ 70 y, and plasma MMA concentration were markedly higher after > 60 y. The prevalence of vitamin B₁₂ deficiency increased substantially after 69 y in 3 UK surveys; it affected about 1 in 20 people aged 65-74 y and at least 1 in 10 of those aged ≥ 75 y [1].

Originally, we expected that vitamin B₁₂ deficiency would be more prevalent in our subjects than in subjects of Western countries because our cohort were included many centenarians and had been eating a greater proportion of plant foods. However, only 9.6% of our subjects showed low vitamin B₁₂ concentration (< 200 pg/mL), which was lower than those of Western cohorts. So far, there were very few reports on vitamin B₁₂ status or intake in subjects aged 85 and more. The mean serum vitamin B₁₂ concentration of our subjects, 450.5 pg/mL (337 pmol/L), was similar to 332 pmol/L of an elderly cohort (mean age 76.4 years) in the US [30], but lower than 358 pmol/L of 71-74 y-old female Norwegian cohort [35].

The relation between dietary intake and vitamin B₁₂ status has been investigated in different populations, with conflicting results. One study concluded that low vitamin B₁₂ status in the elderly was not related to inadequate intake [36], whereas other reports showed significant associations between intake of vitamin B₁₂ and plasma concentrations [37,38]. Recently, Vogiatzoglou et al. [35] reported that the association of plasma vitamin B₁₂ with food intake was weaker in older subjects than in younger subjects, and that plasma vitamin B₁₂ was associated with intakes of increasing amounts of vitamin B₁₂ from dairy products or fish but not with intakes of vitamin B₁₂ from meat or eggs. In the present study, it was not observed significant correlation between dietary intake and serum vitamin B₁₂ concentration (P=0.4769), however, the dietary intake of the subjects with low serum vitamin B₁₂ (< 200 pg/mL) was significantly lower (P=0.0005) than that of the subjects with normal serum normal serum vitamin B₁₂.

Our subjects consumed dietary vitamin B₁₂ (3.17 µg/day) less than that in female subjects aged 85 and older in Austria (3.9 µg/day) or the UK (4.3 µg/day) [39]. Interestingly, the dietary source of vitamin B₁₂ intake was totally different. Whereas our subjects were taking 30.6% of total vitamin B₁₂ intake from plant-origin foods, mainly soybean-fermented foods, seaweeds and kimchi, female Norwegian aged 71-74 y were taking 5.0 µg/day of vitamin B₁₂, which was entirely from animal foods; 52.7% from meat, fish and eggs and 47.3% from milk and dairy products [35].

Most of Koreans enjoy fermented foods, such as doenjang (soybean-fermented paste), ganjang (soy sauce) and gochujang (Red pepper, soybean & starch-fermented paste), and kimchi (vegetable-fermented foods) every day, and seaweeds very often. Therefore, it is considered that these foods are very helpful in protecting the elderly Koreans from vulnerability to vitamin B₁₂ deficiency. Some edible algae, including laver, have already been reported to contain large amounts of vitamin B₁₂ [20,40]. Takenaka et al. [41] have demonstrated that the vitamin B₁₂ in dried purple laver is bioavailable to mammals.

This study has some limitations. First and foremost, only a one-day diet record was collected. Second, serum data number was small in 85-99 yr-old group. Third, the updated food composition table on vitamin B₁₂ is still not large enough to cover all foods consumed by subjects. Fourth, the references of RI and EAR for nutrients for the elderly people aged 75 years and older were used, because those for very old people aged 85 years and older are not yet established. Nevertheless, this study is of value because it represents the first report on vitamin B₁₂ intake pattern and serum level in a very old elderly Korean cohort, including centenarians, and also because it elucidates the big contribution of Korean traditional foods to the dietary vitamin B₁₂ intake of this population.

Figures and Tables

Fig. 1

Percentage of energy composition of subjects

Fig. 2

The percentages of food sources in vitamin B₁₂ intake of the subjects

Table 1

Age distribution of subjects

¹⁾Mean ± SD

²⁾Range

Table 2

Daily food intake of subjects

¹⁾Mean ± SD

Significantly different at ^*P < 0.05 or ^**P < 0.01

Table 3

Daily energy, protein, fat, carbohydrate and vitamin B₁₂ intake of subjects

¹⁾Mean ± SD

²⁾EAR for vitamin B₁₂ for Korean adults

³⁾N (%)

Table 4

Dietary source of vitamin B₁₂

¹⁾Mean ± SD

Table 5

Serum vitamin B₁₂ concentration of subjects

¹⁾Mean ± SD

²⁾N (%)

Table 6

Relation between serum vitamin B₁₂ concentration and dietary intake

¹⁾Mean ± SD

^***Significantly different at P < 0.001

Notes

This research was supported by the grants from SRC program (The Aging and Apoptosis Research Center) of the Korea Science and Engineering Foundation (R11-2002-097-05001-0) and from Soonchang-Gun (2003).

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