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Archives of Gynecology and Obstetrics

https://doi.org/10.1007/s00404-020-05561-y

MATERNAL-FETAL MEDICINE

Does vegan diet influence umbilical cord vitamin B12, folate,


and ferritin levels?
Tomer Avnon1,2   · Ronit Anbar3,4 · Inbar Lavie2 · Tali Ben‑Mayor Bashi1 · Efrat Paz Dubinsky3 · Sivan Shaham3 ·
Yariv Yogev1,2

Received: 2 March 2020 / Accepted: 20 April 2020


© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract
Purpose  To determine the influence of maternal diets on maternal and umbilical cord blood levels of vitamin B12, folic
acid, ferritin, and hemoglobin.
Methods  A prospective observational study on women who maintained the same diet for at least 3 months prior to, and
throughout current pregnancy. Women were divided according to their diet. Diet questionnaires were filled in during the 3rd
trimester. Blood samples for complete blood counts and levels of ferritin, vitamin B12, folate, and albumin were taken from
the women prior to delivery and from the umbilical cord immediately after delivery.
Results  The 273 enrolled women included 112 omnivores, 37 pescatarians, 64 vegetarians, and 60 vegans. There were no
significant differences in the maternal B12 levels between the study groups (P = 0.426). Vegans had lower maternal fer-
ritin levels compared to pescatarians (27 ± 17 vs 60 ± 74 ng/ml, respectively, P = 0.034), but not compared to vegetarians
(P = 0.597), or omnivores (P = 1.000). There were no significant differences in the umbilical cord B12, folate, ferritin, and
hemoglobin levels between the study groups. A sub-analysis that compared women who consumed multivitamins, B12
and iron supplements during pregnancy to women who did not, revealed differences in the levels of umbilical-cord B12
(1002 ± 608 vs 442 ± 151 pg/ml, respectively, P = 0.000) and maternal blood B12 (388 ± 209 vs 219 ± 95 pg/ml, respectively,
P = 0.030) only among vegans, but not among omnivores.
Conclusion  Vegan diet does not change the umbilical cord levels of B12, folic acid, ferritin, and hemoglobin. Vegans who
do not take any vitamin supplementation are at greater risk for B12 deficiency than omnivores.

Keywords  Anemia · B12 · Folic acid · Micronutrient · Plant-based food · Vitamin deficiency

Introduction
The findings were presented at the 40th annual pregnancy meeting
of the Society for Maternal Fetal Medicine, Grapevine, Texas, US,
The prevalence of people who choose to maintain a vegan
February 3–8, 2020.
and a vegetarian diet and abstain from any animal-based
* Tomer Avnon food has been steadily increasing [1]. A vegan diet is distin-
Tomer.avnon@gmail.com guished from a vegetarian diet by being strictly limited to
1 plant-based products and free of all dairy products and eggs
Department of Obstetrics and Gynecology, Lis Maternity
and Women’s Hospital, Tel‑Aviv Sourasky Medical Center, [2]. A vegan diet may lead to potential nutritional deficits,
Affiliated to the Sackler Faculty of Medicine, Tel-Aviv including vitamins B12 [1–7], B2 [4], and D [1, 5, 6], as
University, 6 Weizmann Street, 6423906 Tel‑Aviv, Israel well as calcium [1, 2, 6], iron, zinc [6], and even iodine [7].
2
Sackler Faculty of Medicine, Tel-Aviv University, Tel‑Aviv, The maternal diet during pregnancy reportedly could
Israel have an effect on the newborn bone mass later in life [8],
3
Nutrition and Dietetic Unit, Tel‑Aviv Sourasky Medical on insulin resistance, and on changes in lipid ratio in the
Center, Affiliated to the Sackler Faculty of Medicine, umbilical cord [9]. Few studies have examined the effect of
Tel-Aviv University, Tel‑Aviv, Israel a vegan diet on pregnancy outcome and on potential related
4
The Robert H Smith Faculty of Agriculture, Food complications [10–12], though, those studies focused on
and Environmental Quality Sciences, School of Nutritional vegetarians or on women in the general population, and not
Sciences, Hebrew University, Jerusalem, Israel

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on women who followed the stringent regulations of a vegan Maternal blood tests were taken prior to delivery for com-
diet. Vegans have been found to be at increased risk for defi- plete blood count and levels of ferritin, vitamin B12, folic
ciencies in vitamin levels, such as B12 and D, and in micro- acid and albumin. Umbilical cord blood tests were taken
nutrients, such as iron, zinc, iodine, and calcium [1–7]. As a immediately after delivery for levels of hemoglobin, ferritin,
result, it was considered that the newborns of those women vitamin B12, and folic acid. Data were extracted from the
may suffer from similar deficiencies [10, 11]. Most of our real-time computerized database and from the filled-in ques-
knowledge about the influence of low B12 levels in infancy tionnaires whose items included eating habits and length
is based upon maternal depletion [13]. Specifically, low lev- of following a specific diet, maternal age, gravidity, parity,
els of maternal B12 may cause failure to thrive, irritability, background medical information, data regarding vitamins
and reduced cerebral growth. They may also be associated and supplementations taken throughout pregnancy, body
with increased risk for neural tube defects and low verbal mass index (BMI) at the time of conception, weight gain
performance [13, 14]. Since there is no reliable plant-based during pregnancy, and mode of conception (either spontane-
food source for B12, several guidelines recommend vegan ous or artificial reproductive techniques).
women to receive adequate B12 supplementation and nutri-
tional counselling [15, 16]. Biochemical analysis
The purpose of our study was to prospectively deter-
mine the influence of vegan, vegetarian, pescatarian, and Vitamin B12, folic-acid and ferritin levels were measured
omnivore maternal diets on maternal blood levels and on in blood plasma using a commercial immunoassay (ADVIA
umbilical cord levels of vitamin B12, folic acid, ferritin and Centaur, Siemens Healthcare GmbH, Germany). Iron levels
hemoglobin. were measured in blood plasma (ADVIA, Siemens Health-
care GmbH, Germany). Albumin levels were measured by
BCG dye binding (ADVIA, Siemens Healthcare GmbH,
Germany). Hemoglobin concentrations were measured by
Methods DxH 800 Hematology Analyzer (Beckman Coulter, CA,
US). Umbilical cord folate values < 3 ng/ml [17], vitamin
Study design B12 concentrations < 200 pg/ml [1, 17], and ferritin con-
centrations < 76 ng/ml [18] were classified as insufficient.
The study was approved by the local institutional review Neonatal anemia was defined as umbilical cord hemoglobin
board (0715-17-TLV) and all women provided written levels < 13 g/dL [19].
informed consent. This was a prospective observational
study of women who gave birth in a tertiary, university- Data analysis
affiliated medical center between May 2018 and June 2019.
Eligibility was limited to women aged 18 years or more Descriptive statistics of demographic and laboratory results
with a singleton pregnancy. Only women who maintained were generated by the type of diet. Differences between the
the same diet for at least 3 months prior to and through- selected parameters were evaluated by one-way ANOVA,
out current pregnancy were enrolled. The exclusion criteria chi-squared, and Fisher’s exact test. A sub-analysis was
were women with medical indications for a specific restric- performed to evaluate a possible influence of vitamin sup-
tive diet, such as pre-gestational diabetes mellitus, celiac, plementation: women who consumed multivitamins, iron,
lactose intolerance, and inflammatory bowel disease, and and/or B12 supplementation were compared to women who
women after bariatric procedures or other bowel resections. did not consume any supplementation. Differences between
The participants were divided into 4 groups according to the selected parameters were evaluated by t tests. A P value
their diet: vegans who consume only plant-based products, of 0.05 was considered statistically significant. Statistical
vegetarians who consume mainly a plant-based diet but also analysis was performed with IBM SPSS statistics version
include dairy products and eggs, pescatarians who consume 26 (Chicago, IL, USA).
fish products in their vegetarian diet, and omnivores who
consume animal-based and plant-based products. All women
were asked to fill eating questionnaires during their 3rd tri- Results
mester of pregnancy.
Sample size analysis: Our main hypothesis was that During the study period, 273 women were enrolled and met
vegans will have lower maternal and umbilical B12 levels. the inclusion criteria, which included 112 (41.03%) omni-
We calculated a sample size of 32 women in each group vores, 37 (13.55%) pescatarians, 64 (23.44%) vegetarians,
with a power of 80%, based on past studies’ B12 difference and 60 (21.98%) vegans. The participants’ demographical
of 23–56% between vegans to omnivores [4–6]. characteristics are provided in Table 1. Vegan women were

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Archives of Gynecology and Obstetrics

older and had a significantly lower mean pre-gestational differences in B12, folic acid, ferritin, or hemoglobin lev-
BMI compared to the other groups (Table 1). els between the study groups (Table 2). There were no diet
Maternal and umbilical cord blood tests measurements group differences in the rates of maternal anemia, neonatal
are summarized in Table 2. For the maternal blood meas- anemia, or in the rates of low umbilical B12, ferritin or folic
urements, only ferritin levels were significantly different acid levels (Table 3).
between the groups (P = 0.029). Vegans had lower mater- During pregnancy, 30 women received nutritional con-
nal ferritin levels compared only to pescatarians (27 ± 17 vs sultation (vegans 13.33%, vegetarians 6.25%, pescatarians
60 ± 74 ng/ml, respectively, 95% CI − 62.776 to − 1.524, 10.81% and omnivores 12.50%). We did not find any influ-
P = 0.034), but not compared to vegetarians (44 ± 73 ng/ ence for nutritional consultation during pregnancy on the
ml, 95% CI − 43.564 to 10.165, P = 0.597) or omnivores measured outcomes.
(34 ± 45 ng/ml, 95% CI − 29.279 to 16.191, P = 1.000). We performed a sub-analysis comparing women who con-
For the umbilical cord blood tests, there were no significant sumed multivitamins, B12, and/or iron supplements during

Table 1  Maternal demographics according to diet


Vegan Vegetarian Pescatarian Omnivore P value
n = 60 n = 64 n = 37 n = 112 (α = 5%)

Age (years) 34.97 ± 3.85 33.56 ± 4.13 32.62 ± 3.63 32.56 ± 4.02 0.010
 BMI 21.41 ± 2.63 23.51 ± 3.42 21.82 ± 2.93 22.56 ± 3.32 0.020
 Parity [n (%)]
  Nullipara 29 48.33% 35 54.69% 24 64.86% 66 58.93% 0.374
  Para 1–2 28 46.67% 24 37.50% 11 29.73% 42 37.50% 0.400
  Para 3 +  3 5.00% 5 7.81% 2 5.40% 4 3.57% 0.637
Use of ART, n (%) 12 20.00% 11 17.19% 4 10.81% 10 8.93% 0.162

BMI body mass index at pregnancy onset, ART​artificial reproductive techniques

Table 2  Maternal and umbilical Vegan Vegetarian Pescatarian Omnivore P value


cord blood measurements
according to diet n = 60 n = 64 n = 37 n = 112 (α = 5%)

Maternal
 Hemoglobin (g/dL) 12.24 ± 1.04 12.22 ± 0.90 12.07 ± 1.30 12.39 ± 1.08 0.406
 Ferritin (ng/ml) 27.71 ± 17.37 44.41 ± 72.53 59.86 ± 73.70 34.26 ± 44.97 0.029
 B12 (pg/ml) 361.37 ± 204.76 378.94 ± 282.85 375.78 ± 301.33 325.84 ± 151.53 0.426
 Folic acid (ng/ml) 15.55 ± 7.57 15.51 ± 6.12 14.10 ± 5.12 14.33 ± 6.37 0.536
 Albumin (g/L) 35.49 ± 3.32 36.55 ± 1.93 35.54 ± 2.66 36.52 ± 2.47 0.080
Umbilical
 Hemoglobin (g/dL) 15.56 ± 2.21 15.98 ± 1.99 15.49 ± 1.76 15.76 ± 2.23 0.703
 Ferritin (ng/ml) 199.02 ± 120.87 200.86 ± 142.46 257.98 ± 144.72 233.26 ± 216.80 0.453
 B12 (pg/ml) 902.05 ± 586.60 832.21 ± 469.80 778.89 ± 481.94 778.57 ± 402.04 0.573
 Folic acid (ng/ml) 20.51 ± 4.66 20.45 ± 4.10 18.73 ± 4.01 20.61 ± 5.01 0.677

Table 3  Deficiencies in Characteristic Vegan Vegetarian Pescatarian Omnivore P value


maternal and umbilical cord
blood levels according to diet (α = 5%)

Maternal anemia 10.00% 6/60 9.37% 6/64 8.11% 3/37 8.04% 9/112 0.969
Maternal B12 deficiency 17.54% 10/57 12.25% 6/49 18.75% 6/32 9.26% 10/108 0.347
Umbilical anemia 8.33% 4/48 0.00% 0/52 3.45% 1/29 5.10% 5/98 0.167
Umbilical ferritin deficiency 7.32% 3/41 11.36% 5/44 4.35% 1/23 14.12% 12/85 0.561
Umbilical B12 deficiency 5.00% 2/40 0.00% 0/39 0.00% 0/19 1.23% 1/81 0.504
Umbilical folic acid deficiency 0.00% 0/20 0.00% 0/23 0.00% 0/11 1.67% 1/60 1.000

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pregnancy to women who did not consume any supplements It is possible that such differences disappear as a result of
(Table 4). There was a significant difference between vegans the commonplace use of vitamin supplementation among
who consumed to vegans who did not consume any sup- pregnant women compared to nonpregnant women. Inter-
plements, in the levels of umbilical cord B12 (1002 ± 608 estingly, only the ferritin level was lower among our vegan
vs 442 ± 151 pg/ml, respectively, 95% CI 312.986–807.121, group and only in comparison to pescatarians. Though, we
P < 0.001) and in the level of maternal blood B12 (388 ± 209 do not think this difference has any clinical implication
vs 219 ± 95 pg/ml, respectively, 95% CI 16.708–320.625, since its levels were within normal range and no differences
P = 0.030). There was no significant difference in the lev- were found in all other measurements. As far as we know,
els of maternal B12 levels (95% CI − 61.512 to 137.546, no study mentioned ferritin levels among pregnant vegan
P = 0.450) or umbilical cord B12 levels (95% CI − 91.887 women, although the review of Piccoli et al. [10] did men-
to 563.835, P = 0.156) between the omnivores who did or tion lower ferritin levels among pregnant vegetarians with a
did not consume any supplements. Since only 2 vegetarians higher incidence of anemia.
and 2 pescatarians did not consume any supplements, we We did not find any effect of the maternal diet on umbili-
could not compare the influence of supplement use for those cal cord laboratory measurements. As far as we know, the
groups (Table 4). question of a vegan diet’s effect on umbilical hemoglobin,
B12, or folic acid levels has not been addressed before. The
fact that we did not find any difference in the maternal-blood
Discussion groups for most of the measurements, is in the concordance
of this finding.
In this study, we aimed to examine the influence of 4 types of Our findings of similar rate of anemia and B12 defi-
maternal diets on maternal and umbilical cord blood levels ciency among different maternal diets are supported by sev-
of vitamin B12, folic acid, ferritin and hemoglobin, with eral studies that did not demonstrate a higher prevalence of
emphasis on the specific comparable effect of the vegan anemia among pregnant [1] and non-pregnant [6] vegans.
diet. Our main findings were fourfold. (1) Vegan diet did Additionally, Chebaya et al. [20] reported a similar rate of
not affect maternal blood levels of B12, folic acid, albu- maternal B12 deficiency among women who consumed vita-
min, or hemoglobin, and only the ferritin level was lower mins and those who did not. Unlike earlier reports, however,
among vegans in comparison to pescatarians. (2) Vegan diet the rate of maternal B12 deficiency (< 200 pg/ml) in our
did not affect umbilical cord blood levels of B12, ferritin, vegan group was much lower (18%) than the rate reported
folic-acid, or hemoglobin. (3) There was no difference in by others (38%) [1].
the rate of maternal or neonatal anemia or in the rate of low Since the source of B12 is mainly in animal-based food,
umbilical B12, ferritin, or folic acid levels between any of some vegetarians or vegans are at increased risk for B12
the 4 diet groups. (4) Only the vegan women who did not deficiency, such as women with intestinal diseases and
take any supplements during pregnancy had lower maternal decreased B12 absorption. The transport of B12 to the fetus
and umbilical B12 levels in comparison to vegans who con- is diminished in women with low levels of B12 [14], where-
sumed supplements. upon their children may have B12 deficiency [10, 11]. Those
Overall, the vegan women in our study cohort did not studies support our findings of there being a direct relation
differ in their B12 or folic acid levels from the other 3 diet between maternal B12 levels and umbilical cord B12 levels,
groups. This finding is in opposition to the findings of oth- and the contention that vegans who do not consume sup-
ers [4–6], which demonstrated lower B12 and higher folic plements have lower maternal and umbilical blood levels.
acid [4] levels among vegans compared to omnivores. Those Although the levels of our study vegans were still inside
studies, however, compared vegans and omnivores in the the lower-normal range (> 200 pg/ml). In contrast to our
general population and did not focus on pregnant women. findings, several studies demonstrated higher maternal B12

Table 4  B12 measurements Multivitamins + iron sup- No multivitamins or iron P value (α = 5%)


according to oral plementation supplementation
supplementation
Vegan n = 51 n = 8
 Maternal B12 (pg/ml) 388.29 ± 209.54 219.63 ± 95.26 0.030
 Umbilical B12 (pg/ml) 1002.63 ± 608.56 442.57 ± 151.30  < 0.001
Omnivore n = 91 n = 11
 Maternal B12 (pg/ml) 330.47 ± 163.16 292.45 ± 82.22 0.450
 Umbilical B12 (pg/ml) 794.55 ± 423.69 558.57 ± 282.96 0.156

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levels in the general pregnant population who consume B12 Compliance with ethical standards 
supplementation during pregnancy [20, 21] and postpartum
[22]. Importantly, those studies enrolled women in India Conflict of interest  All the authors report no conflicts of interest.
[21], Cambodia [20], and Bangladesh [22], and they did
Ethical approval  All procedures performed in studies involving human
not relate specifically to vegan or vegetarian populations, participants were in accordance with the ethical standards of the insti-
even though many of those countries’ populations consume tutional and/or national research committee and with the 1964 Hel-
mainly plant-based diets. sinki declaration and its later amendments or comparable ethical stand-
Newborns with B12 deficiency may sustain several seque- ards. Informed consent was obtained from all individual participants
included in the study.
lae such as failure to thrive, irritability, reduced cerebral
growth, apathy, and future interference with verbal perfor- Informed consent  This article does not contain any studies with ani-
mance [6, 13, 14]. Since maternal B12 depletion may be the mals performed by any of the authors.
reason for many of those cases [13], several guidelines are
in place that recommend vegan women receive nutritional
counselling and to check regularly for critical B12 levels and
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