Vegetarianism during pregnancy: Risks and benefits

Accepted Manuscript Vegetarianism during pregnancy: Risks and benefits J. Costa-Rodrigues, Rute Sá-Azevedo, João Balinha, Graça Ferro

PII:

S0924-2244(18)30091-8

DOI:

10.1016/j.tifs.2018.06.014

Reference:

TIFS 2255

To appear in:

Trends in Food Science & Technology

Received Date: 8 February 2018 Revised Date:

14 June 2018

Accepted Date: 27 June 2018

Please cite this article as: Costa-Rodrigues, J., Sá-Azevedo, R., Balinha, J., Ferro, G., Vegetarianism during pregnancy: Risks and benefits, Trends in Food Science & Technology (2018), doi: 10.1016/ j.tifs.2018.06.014. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT 1

Vegetarianism during pregnancy: risks and benefits

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Costa-Rodrigues J.a,b,c,d,*, Rute Sá-Azevedoe, João Balinhae, Graça Ferroe

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a

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U. Porto, Portugal; cInstituto Politécnico de Viana do Castelo, Escola Superior de

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Saúde, Portugal; ei3S, Instituto de Inovação e Investigação em Saúde, Universidade do

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Porto, Portugal; eServiço Nutrição e Alimentação da Unidade Local de Saúde do Alto

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ESS – Escola Superior de Saúde, P. Porto, Portugal; bFaculdade de Medicina Dentária,

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Minho, EPE

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Short title: Vegetarianism and pregnancy

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* Corresponding author

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Escola Superior de Saúde do Porto

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Instituto Politécnico do Porto

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Rua Dr. António Bernardino de Almeida, 400

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4200-072 Porto

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Portugal

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Telephone: +351 222 061 000

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Fax: +351 222 061 001

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E-mail address: [email protected]

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ACCEPTED MANUSCRIPT Abstract

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Background

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During pregnancy, women face continuous nutritional challenges. Although it is a

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personal choice, the adoption of a vegetarian dietary pattern during pregnancy must be

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regarded as a situation that may be associated with some risks and benefits for the

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mother and the fetus.

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Scope and Approach

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In the present review, the most frequent nutritional deficits among pregnant vegetarians

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will be discussed, namely, those that refer to vitamin B12, zinc, iron, omega-3 fatty

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acids and vitamin D. If properly planned, vegetarian diets may also be associated with

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some important health benefits. The main potential outcomes of vegetarianism for

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pregnant women, fetal development and for the early and later life of the newborns will

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also be reviewed.

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Key Findings and Conclusions

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Taken together, despite some of the controversial published data, vegetarianism appears

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to be a safe dietary pattern during pregnancy. So, the option for vegetarianism must be

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considered a personal choice that like any other feeding pattern may pose some

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nutritional risks but also bring some potential health outcomes both for the mother and

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for the children. In order to deal with the nutritional requirements during pregnancy, it

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is recommended that vegetarian mothers follow strict nutritional counseling.

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Keywords

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Vegetarianism; Pregnancy; Nutritional risks; Health outcomes

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ACCEPTED MANUSCRIPT 1. Introduction

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Diet during pregnancy is one of the most important factors that may be adjusted in order

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to deal with the continuous challenges that women face during gestation. It can have

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profound consequences not only for the mother, but also for the fetus, during the early

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life of the newborns, and even throughout all their life (Nyaradi, Li, Hickling, Foster, &

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Oddy, 2013; Zeisel, 2009). The main concerns of a pregnant diet must include high

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hygiene standards, avoid potentially toxic molecules, provide adequate amounts of

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energy and macronutrients and satisfy the needs (sometimes increased) of vitamins and

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minerals. Thus, following a healthy and balanced diet is of outmost importance during

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pregnancy (Agnoli, Baroni, Bertini, Ciappellano, Fabbri, Papa, et al., 2017; Melina,

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Craig, & Levin, 2016; Nyaradi, Li, Hickling, Foster, & Oddy, 2013).

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Although there are no ideal diets, which are always beneficial and do not have any kind

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of limitations, the way people view eating has significantly changed in the last years.

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Indeed, food is now seen not only as a primary need to support the basic functions of

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human body, but also an important tool to promote a healthy life (Fung & Hu, 2003; Hu

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& Willett, 2002). In this context, growing attention has been paid to vegetarianism,

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since there are evidences that it can be linked to lower weight, lower blood pressure and

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cholesterol serum levels and, consequently, it may protect against cardiovascular

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diseases (Calder, 2015; Calder & Yaqoob, 2009; Estruch, Ros, Salas-Salvado, Covas,

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Corella, Aros, et al., 2013; Yokoyama, Nishimura, Barnard, Takegami, Watanabe,

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Sekikawa, et al., 2014), metabolic syndrome (Ajala, English, & Pinkney, 2013; Zhang

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& Ning, 2011) and some types of cancer (Pistollato, Sumalla Cano, Elio, Masias

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Vergara, Giampieri, & Battino, 2015). Vegetarian diets are food patterns that avoid,

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restrict or abolish foods from animal origins. For example, lacto-ovo vegetarians are

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allowed to consume milk products and eggs, while vegans do not eat any food from

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ACCEPTED MANUSCRIPT animal sources (Snow, 2017). Besides that, it is also important to highlight that even

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among the different vegetarian patterns, there are important differences that rely on the

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restriction of specific kinds of plant foods (grains, legumes, vegetables, fruits, nuts and

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seeds), or even in the ways they are consumed (cooked vs. raw). Thus, assessing the

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impact of vegetarianism in different parameters is far of being a simple task, because it

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comprises a heterogeneous set of different feeding patterns. The reasons behind the

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adoption of a vegetarian diet may be diverse and include cultural, religious or personal

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preferences (including health-related and animal welfare issues) (Burdge, Tan, &

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Henry, 2017; Corrin & Papadopoulos, 2017). The amount of vegetarians is increasing

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and may account for up to 10% of total population (Penney & Miller, 2008). For

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example, in 2016, about 3.3% of American adults followed a vegetarian dietary pattern,

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and among them, about half were vegan (Melina, Craig, & Levin, 2016). Moreover,

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vegetarianism seems to be more popular among young adults (~6%) than in older ones

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(~2%) (Melina, Craig, & Levin, 2016). Regarding Europe, significant differences are

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found in different countries. Overall, it is estimated that about 5% of Europeans are

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vegetarians. Countries like Italy, Germany, Austria and France are those with the

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highest percentage (~9-13%). The more restrictive the vegetarian dietary pattern, the

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greater the risk of incurrence in some kind of nutritional deficit, so, accurate and

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nonjudgmental nutritional counseling may represent an indispensable step towards a

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healthy pregnancy and fetal development.

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According to the American Dietetic Association and the Canadian Dietary Association,

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vegetarianism may be adopted in all stages of life, including pregnancy (Craig &

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Mangels, 2009; "Position of the American Dietetic Association and Dietitians of

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Canada: vegetarian diets," 2003; Rizzo, Lagana, Rapisarda, La Ferrera, Buscema,

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Rossetti, et al., 2016). It poses some potential nutritional risks, but at the same time, it

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ACCEPTED MANUSCRIPT seems to have important health outcomes both for the mother and for the offspring

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(Pistollato, Sumalla Cano, Elio, Masias Vergara, Giampieri, & Battino, 2015). At the

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present, the search for healthy lifestyles, which include healthier feeding choices,

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combined with an increase concern about ecology and sustainability, is rising. Indeed,

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the reduction in the consumption of meat and meat-derived products, as well as the

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consumption of organic products is gaining supporters all over the world. These options

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are usually associated with healthier lifestyles and, thus, may be linked to several health

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benefits during pregnancy, not only for the mothers, but also for children (Simões-Wüst,

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Moltó-Puigmartí, van Dongen, Dagnelie, & Thijs, 2017; Torjusen, Brantsæter, Haugen,

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Lieblein, Stigum, Roos, Holmboe-Ottesen, Meltzer, 2010). In a study conducted in the

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Netherlands, it was reported that vegetarians were more prone to organic food

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consumption. Moreover, participants with a more often consumption of this type of

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products revealed a higher education level and a lower body mass index. Torjusen et al.

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(14) found in a large Norwegian cohort study that there was a relatively small

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proportion of organic food intake, and that the most frequent organic food choices

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involved eggs and vegetables. Those consumers included a higher percentage of

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vegetarians, as well as people with more active lifestyles and lower body mass index.

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Interestingly, no significant relationships were established between organic food

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consumption and education level, or with higher incomes. Taken together, it seems that

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the consumption of organic products is often related with specific cultural and

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socioeconomic characteristics, although with important apparent differences between

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different populations. Moreover, further studies are required to unravel the specific

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contribution of those changes in feeding patterns and in the related health outcomes.

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Only knowing the potential benefits and risks of this feeding pattern, the nutritional

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challenges that a pregnant woman faces can be overcome with a well-planned

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vegetarian diet. The present review aims to address the main nutritional benefits and

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risks of pregnant vegetarian women, as well as the main outcomes of vegetarianism to

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mother’s and children’s health.

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2. Nutritional benefits

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Although vegetarianism is a restrictive feeding pattern, and, consequently, may be

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linked to some nutritional potential deficits, it is also associated to some nutritional

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advantages, due to the high consumption of products from vegetal origin.

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One of the main benefits is the high consumption of fiber, which usually increases with

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the restriction degree of vegetarian patterns (Ahola, Forsblom & Groop, 2018; Li, 2014;

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Pistollato, Sumalla Cano, Elio, Masias Vergara, Giampieri, & Battino, 2015). Fiber

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consumption has been linked to many different positive health outcomes, namely, the

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decrease in the risk of different chronic diseases, some cancers (particularly those

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affecting gastrointestinal tract), and also a decreased incidence of a wide range of

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digestive disorders (Anderson, Baird, Davis Jr, Ferreri, Knudtson, Koraym, Waters &

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Williams, 2009). Considering the cardiovascular health, it is also important to highlight

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that cholesterol has an exclusive animal origin, which means that vegetarianism is

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associated to a very low or even null intake of this nutrient (depending on the restrictive

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level of the adopted pattern) (Li, 2014; Pistollato, Sumalla Cano, Elio, Masias Vergara,

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Giampieri, & Battino, 2015; Craig, 2009). Consequently, this can decrease the risk of

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cardiovascular diseases, such as atherosclerosis or stroke. Another important benefit of

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vegetarianism is the high intake of folate (Li, 2014; Craig, 2009). Although this vitamin

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can also be obtained from animal sources, it is mainly found in plant-based products.

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The main outcomes of a proper folate intake are a healthy cardiovascular system, as

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well as a well-developed nervous system (Craig, 2009). This is particularly relevant

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ACCEPTED MANUSCRIPT during pregnancy since folate deficiency is usually associated to neural tube defects

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and/or increased risk of preeclampsia (van Gool, Hirche, Lax & Schaepdrijver, 2018;

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Bulloch, Lovell, Jordan, McCowan, Thompson & Wall, 2018). Vitamin C status of

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vegetarians is also usually high (Craig, 2009), which may be particularly relevant for a

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proper tissue renovation (vitamin C plays a very important role on collagen

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biosynthesis), as well as to ensure a high functionality of immune system (Carr &

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Maggini, 2017). In addition to macro- and micronutrient intake, vegetarianism is also

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usually linked to a significantly higher consumption of antioxidants and other bioactive

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compounds (Ahola, Forsblom & Groop, 2018; Li, 2014; (Anderson, Baird, Davis Jr,

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Ferreri, Knudtson, Koraym, Waters & Williams, 2009), when compared to omnivores.

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Oxidative stress plays a key role on a wide range of disorders, especially in non-

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communicable diseases, such as cancer, chronic diseases or type 2 diabetes mellitus. A

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proper consumption of antioxidants may significantly decrease the risk of those diseases

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(Li, 2014; Pistollato, Sumalla Cano, Elio, Masias Vergara, Giampieri, & Battino, 2015;

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Craig, 2009).

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Taken together, there are numerous and important benefits associated to vegetarianism.

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Those can have a profound effect in daily life of vegetarians. However, some of the

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highlighted potential advantages, may be particularly relevant during pregnancy, since

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nutritional requirements may be changed during that period, and also because some

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nutritional deficits may pose serious risks not only for the mother, but also for the

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development and health of the offspring (for example, folate deficiency).

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3. Nutritional risks

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Across the literature, there are many papers ascribing different nutritional risks for

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vegetarians, particularly in vegetarian pregnant women. One of the main potential

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ACCEPTED MANUSCRIPT outcomes of a vegetarian diet is protein deficiency, not only quantitatively, but also in

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some essential amino acids. In addition, there are several micronutrients whose

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ingestion may be insufficient in vegetarians (Koebnick, Hoffmann, Dagnelie, Heins,

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Wickramasinghe, Ratnayaka, et al., 2004; Piccoli, Clari, Vigotti, Leone, Attini,

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Cabiddu, et al., 2015; Sharma, Soni, Murthy, & Malhotra, 2003). In the following

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section, the main deficiencies of micronutrients that may be related with vegetarianism

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during pregnancy will be discussed.

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2.1. Vitamin B12

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Vitamin B12 is also known as cobalamin. It is a water-soluble vitamin whose needs are

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higher during pregnancy and even higher during lactation. It is essential for

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erythropoiesis, synthesis of nucleic acids and for the integrity of myelin sheaths

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(Pistollato, Sumalla Cano, Elio, Masias Vergara, Giampieri, & Battino, 2015). Vitamin

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B12 is only present in significant amounts in animal foods, though it can also be found

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in small quantities in vegetal products such as sauerkraut and in tea leaves, in some

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algae like chlorella and spirulina and in fungii such as shiitake and porcini mushrooms

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(Rizzo, et al., 2016; Watanabe, Yabuta, Tanioka, & Bito, 2013). Regarding algae, it is

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important to highlight that some of them may also present vitamin B12 analogues that

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may decrease the efficiency of vitamin B12 (Watanabe, Yabuta, Tanioka, & Bito,

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2013).

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Several reports have shown that vegetarianism during pregnancy may be associated

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with vitamin B12 deficiency, particularly in the case of vegan diets (Koebnick, et al.,

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2004; Piccoli, et al., 2015). The mean plasma vitamin B12 values of vegetarians are

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usually 17-39% below the normal values (Pawlak, Lester, & Babatunde, 2014). This

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condition may contribute to a higher incidence of neural tube defects and impaired

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ACCEPTED MANUSCRIPT neurodevelopment, less lean mass and higher adiposity, insulin resistance, and increased

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risk of some cancers, namely, those from colon and breast tissues (Rush, Katre, &

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Yajnik, 2014). In addition, newborns breastfed by vegetarian mothers may also present

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low levels of vitamin B12 (Weiss, Fogelman, & Bennett, 2004). Those children may

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present lethargy, hypotonia, slow development and megaloblastic anemia, particularly

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during the second trimester of life (Chalouhi, Faesch, Anthoine-Milhomme, Fulla,

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Dulac, & Cheron, 2008). Nevertheless, since folate and vitamin B12 are both required

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for erythropoiesis, and due to the fact that vegetarians usually present a high intake of

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the former, some of the symptoms associated to vitamin B12 deficiency may be

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somehow compensated (Agnoli, et al., 2017).

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In order to avoid the described deleterious consequences, supplements or fortified foods

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may represent a very important strategy to deal with those deficiencies (Snow, 2017,

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2018), not only for the mother (Pepper & Black, 2011; Weiss, Fogelman, & Bennett,

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2004), but also for the offspring (Chalouhi, Faesch, Anthoine-Milhomme, Fulla, Dulac,

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& Cheron, 2008; Herrmann & Knapp, 2002). To this aim, the main Vegetarian Food

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Guides only consider a vegetarian diet "well-planned" if it includes a reliable source of

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vitamin B12 (Messina, Melina, & Mangels, 2003; Baroni, Goggi, & Battino, 2017).

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3.2. Zinc

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Zinc is a mineral that is required for numerous physiological processes, such as

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regulation of gene expression, functioning of immune system, cell signaling, enzyme

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action, among others (Foster & Samman, 2010). Due to its importance, zinc deficiency

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may have dramatic effects on growth, bone and sexual maturation, and may cause

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disturbances in immune response. Zinc is more abundant and bioavailable in food from

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animal origin (Hunt, 2003), so, vegetarian diet may be linked to some degree of zinc

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ACCEPTED MANUSCRIPT deficiency. The main animal sources of zinc are meat and milk (and their derivatives),

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while the main vegetable sources are whole grain cereals (Agnoli, et al., 2017). Phytate,

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oxalate and dietary fiber, which are mainly found in plant-based products, have

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inhibitory effects on zinc intestinal absorption (Pistollato, Sumalla Cano, Elio, Masias

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Vergara, Giampieri, & Battino, 2015). On the other hand, cysteine and some

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hydroxyacids present in fruits can have an opposite effect (Wegmuller, Tay, Zeder,

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Brnic, & Hurrell, 2014). Summing all the factors, it is described that zinc absorption in

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vegetarians is about 15-26% while in omnivores it can reach 33-35% (R. S. Gibson,

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1994; Hunt, Matthys, & Johnson, 1998). Besides that, pregnancy is also associated to

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higher zinc requirements, due to the importance of this mineral not only for the correct

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functioning of the body of the mother, but also for the fetal development (Swanson &

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King, 1987).

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So, zinc deficiency may be another deleterious outcome related with vegetarianism

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during pregnancy (Abraham, 1982; Burdge, Tan, & Henry, 2017), although there are

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also reports that demonstrate an absence of relationship between them (King, Stein, &

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Doyle, 1981). Recently, a meta-analysis about the zinc status on vegetarian mothers was

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conducted (Foster, Herulah, Prasad, Petocz, & Samman, 2015). It was not observed any

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significant difference between them and omnivore mothers, in the duration of gestation

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and in the birthweight of the children. In one study, significantly lower urinary zinc

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values were observed in vegetarians (Campbell-Brown, Ward, Haines, North, Abraham,

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McFadyen, et al., 1985). However, globally the ingestion of zinc by pregnant women

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was below the recommendations, in both groups (vegetarians and non-vegetarians),

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although in the former group mean ingestion was slightly lower. So, rather than a

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specific concern about vegetarian mothers, zinc deficiency appears to be a global

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concern affecting pregnancy in a transversal way (Foster, Herulah, Prasad, Petocz, &

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ACCEPTED MANUSCRIPT Samman, 2015). Since the relationship between modest zinc deficiency and pregnancy

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outcomes is scarcely documented (R. S. Gibson, 1994; Swanson & King, 1987), the real

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impact of the observed low zinc ingestion remains to be defined. It was proposed that if

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zinc intake during the pre- and postdelivery period is adequate, the nutritional status of

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their infants may be considered normal ("Vegetarian weaning. Nutrition Standing

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Committee of the British Paediatric Association," 1988). Thus, it seems important to

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create strategies to increase zinc ingestion during pregnancy, particularly by women

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with a feeding pattern exclusively composed by plant-based foods. Increasing the

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ingestion of wheat, pumpkin seeds, nuts, pulses, some types of mushrooms, and, if

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necessary, zinc supplementation, may help to achieve proper zinc levels during

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pregnancy. In addition, the creation of strategies to improve zinc bioavailability may

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also represent an important attitude to avoid a zinc nutritional deficiency by pregnant

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vegetarian.

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Regarding breast milk, zinc concentration appears to be somehow independent of

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maternal zinc intake (Krebs, Westcott, Culbertson, Sian, Miller, & Hambidge, 2012).

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This suggests that zinc amount in maternal milk may be maintained under homeostatic

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mechanisms. Its concentration is typically highest in colostrum and starts to gradually

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decrease during lactation (Foster & Samman, 2015). This means that special attention

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must be given to zinc intake, after the introduction of new foods in the feeding pattern

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of infants (Foster & Samman, 2015).

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3.3. Iron

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Besides zinc, iron may also be present in lower amounts in vegetarian mothers. This is

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due to the lower bioavailability of iron usually present in plant-based foods, when

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compared with those from animal origin (Craig, 2010; Hunt, 2003). This is mainly due

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ACCEPTED MANUSCRIPT to the fact that in plants iron is in the non-heme form. The consumption of food with

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high content of polyphenols or oxalate may also account for a decrease in iron

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bioavailability due to a decreased intestinal absorption, so special attention should be

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paid to tea, coffee, cocoa, spinach, among others.

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Soybean is one of the main sources of iron for vegetarians (Hurrell & Egli, 2010). In

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order to increase the bioavailability of iron, vegetarians are recommended to have a high

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intake of vitamin C during the meals (Hunt & Roughead, 2000). In addition, the

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presence of organic acids such as citric, malic, lactic and tartaric acids, and carotenes

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and vitamin A also appear to contribute to higher intestinal absorption of iron (Collings,

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Harvey, Hooper, Hurst, Brown, Ansett, et al., 2013; Craig, 1994). Since phytate

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decreases the bioavailability of iron, cereals and pulses may be soaked before

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consumption, in order to activate endogenous phytases (Agnoli, et al., 2017).

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On a general way, pregnant vegetarians are susceptible to present iron deficiencies

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(Agnoli, et al., 2017; Pistollato, Sumalla Cano, Elio, Masias Vergara, Giampieri, &

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Battino, 2015). Nevertheless, in one published report, it was observed that vegetarians

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were more prone to ingest adequate amounts of iron and to take supplements during the

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first semester of pregnancy (Alwan, Greenwood, Simpson, McArdle, Godfrey, & Cade,

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2011). If proper iron levels are achieved, breast milk may present a mineral composition

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similar to that of omnivore mothers (Craig & Mangels, 2009; "Vegetarian weaning.

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Nutrition Standing Committee of the British Paediatric Association," 1988). Iron

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deficiency may cause important handicaps in children, such as poor physical

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development and low productivity and cognitive performance (Alwan, Greenwood,

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Simpson, McArdle, Godfrey, & Cade, 2011; Zimmermann & Hurrell, 2007). Iron

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supplementation during pregnancy and breastfeeding is thus recommended, either in

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vegetarian or non-vegetarian women, when hemoglobin levels drop under 105g/L.

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3.4. Omega-3 fatty acids

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Omega-3 fatty acids are a heterogeneous class of lipids with many important health-

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promoting effects. Linolenic acid is the most abundant in plant foods, being mainly

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found in flaxseeds, hemp and chia seeds, walnuts and seaweeds (Davis & Kris-Etherton,

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2003). Eicosapentaenoic and docosahexanoenoic acids (EPA and DHA, respectively)

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are other important omega-3 fatty acids, which are molecules with a very modest

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presence in plant-based products. The main dietary sources of these fatty acids are fatty

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fishes (such as tuna, sardines, herring, anchovies and mackerel), meat and dairy

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products (Tur, Bibiloni, Sureda, & Pons, 2012).

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Omega-3 fatty acid deficiencies may occur in vegetarians, mainly in EPA and DHA.

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This is more frequent in vegetarians following monotonous and poorly-planned diets

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(Burdge, Tan, & Henry, 2017; Melina, Craig, & Levin, 2016; Reddy, Sanders, & Obeid,

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1994). These deficiencies can have an important impact not only during fetal

312

development, but also in the content of DHA in breast milk (Michaelsen, Dewey, Perez-

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Exposito, Nurhasan, Lauritzen, & Roos, 2011; Sanders & Reddy, 1992). Low levels of

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omega-3 fatty acids may be related to brain developmental defects, as well as to a

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variety of growth and metabolic disturbances (R. A. Gibson, Muhlhausler, & Makrides,

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2011). One simple way to overcome this problem is by increasing the consumption of

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vegetable products such as flaxseeds, flaxseed oil, chia seeds and walnuts (Agnoli, et

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al., 2017; Baroni, Goggi, & Battino, 2017). The intake of those fatty acids during the

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pregestational and perigestational periods also appears to be important for a successful

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supply of fatty acids to the fetus (Haggarty, 2004). So, an appropriate nutritional

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intervention may be performed as early as possible.

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ACCEPTED MANUSCRIPT 3.5. Vitamin D

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Although vitamin D can be synthesized in the human body, a process that requires UV

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light exposure, this only occurs in relevant extent in places under significant sunlight

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exposure. Low levels of vitamin D can cause rickets in children and osteomalacia in

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adults (Pistollato, Sumalla Cano, Elio, Masias Vergara, Giampieri, & Battino, 2015).

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There are only few significant sources of vitamin D, mainly fat fishes and fortified

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foods (Pistollato, Sumalla Cano, Elio, Masias Vergara, Giampieri, & Battino, 2015).

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Globally, it is accepted that vitamin D deficiency is prevalent all over the world

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(Hovdenak & Haram, 2012; Kazemi, Sharifi, Jafari, & Mousavinasab, 2009), a situation

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that may be more frequent in pregnant vegetarians (Dasgupta, Saikia, & Sarma, 2012;

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Pistollato, Sumalla Cano, Elio, Masias Vergara, Giampieri, & Battino, 2015). Thus,

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supplementation appears to be an effective tool to ensure normal levels of vitamin D,

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particularly in regions that have poor sunlight exposure, or in low-income countries

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(Barger, 2010; Dasgupta, Saikia, & Sarma, 2012; Hovdenak & Haram, 2012; Kazemi,

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Sharifi, Jafari, & Mousavinasab, 2009).

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4. Impact on mother’s health

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The global effects that a vegetarian diet can have on pregnant women are diverse and,

341

on a general way, poorly documented. It is described that it can contribute to lower

342

blood pressure and, consequently, to decrease the risk of hypertensive disorders of

343

pregnancy, such as pre-eclampsia or eclampsia (Carter, Furman, & Hutcheson, 1987;

344

Piccoli, et al., 2015). In another study, it was also reported a significant decrease on the

345

prevalence of hypertension associated with proteinuria (Reddy, Sanders, & Obeid,

346

1994). These observations reinforce the hypothesis that preeclampsia is associated with

347

an increase in the consumption of saturated fat and sugar, and a decreased intake of

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ACCEPTED MANUSCRIPT fiber (Frederick, Williams, Dashow, Kestin, Zhang, & Leisenring, 2005). In line with

349

this, it was proposed that the consumption of at least three daily servings of vegetables

350

may decrease blood pressure during pregnancy (Carter, Furman, & Hutcheson, 1987).

351

Pregravid overweight has been associated with an increased risk of chronic diseases

352

incidence by the offspring. An adequate intake of fruits and vegetables, as occur in

353

vegetarianism, may help to control this variable (Laraia, Bodnar, & Siega-Riz, 2007).

354

More recently, vegetarian diets were suggested to be involved in a better weight control

355

in pregnant women, contributing to a lower or similar weight gain as compared with

356

omnivores (Piccoli, et al., 2015; Streuling, Beyerlein, Rosenfeld, Schukat, & von Kries,

357

2011). In one study it was observed that adopting a vegetarian dietary pattern in the first

358

trimester of pregnancy may be linked to a lower gestational weight gain (Stuebe, Oken,

359

& Gillman, 2009).

360

It is also believed that, due to the high amounts of fiber ingested by vegetarian mothers,

361

the risk of developing gestational diabetes may be lower. In this context, it was

362

suggested that an increment of 10g/day of ingested fiber may decrease up to 26% de

363

risk of developing tat disease (Zhang, Liu, Solomon, & Hu, 2006).

364

Considering the gestational duration, some studies proposed that vegetarianism may be

365

associated with a shorter time period, although almost always within the expected

366

duration (Piccoli, et al., 2015). The only exception was reported in a study where the

367

incidence of preterm delivery seemed to be increased in vegetarian mothers (Alwan,

368

Greenwood, Simpson, McArdle, Godfrey, & Cade, 2011). Regarding the type of

369

delivery, there is conflicting data. Indeed, it was reported that this type of feeding

370

pattern may also be associated with either an increase or a decrease in cesarean

371

deliveries (Pistollato, Sumalla Cano, Elio, Masias Vergara, Giampieri, & Battino, 2015;

372

Reddy, Sanders, & Obeid, 1994).

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ACCEPTED MANUSCRIPT Another potential benefit of vegetarian diets may comprise a decrease in the incidence

374

of calf cramps during pregnancy (Koebnick, Leitzmann, Garcia, Heins, Heuer, Golf, et

375

al., 2005), which may be at least partly explained by higher intakes of magnesium.

376

Lower maternal mortality and changes in the incidence of postpartum depression have

377

also been linked to vegetarianism during pregnancy (Carter, Furman, & Hutcheson,

378

1987; Pistollato, Sumalla Cano, Elio, Masias Vergara, Giampieri, & Battino, 2015).

379

Considering the latter, it is a frequent problem (13%) that usually starts during the first

380

month after delivery. Vegetarianism has been associated with an increase in the

381

incidence of postpartum depression, but the underlying mechanisms remain to be

382

elucidated (Hogg-Kollars, Mortimore, & Snow, 2011).

383

Finally, a recent systematic review revealed that if a vegetarian diet is well-planned,

384

balanced and varied, with no nutritional deficits, it is not associated with any relevant

385

negative health outcome (Piccoli, et al., 2015).

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5. Impact on fetal development

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The impact of vegetarian diets on fetal development is perhaps one of the most

389

controversial aspects of vegetarianism. The available data is still scarce and further

390

studies are required to have an integrated and more detailed perspective about it. There

391

are reports that claim that vegetarianism during pregnancy is associated to a lower

392

birthweight (~20-200g), although in the majority of the cases it was not proved

393

statistical significance of the results (Campbell-Brown, et al., 1985; Pistollato, Sumalla

394

Cano, Elio, Masias Vergara, Giampieri, & Battino, 2015; Reddy, Sanders, & Obeid,

395

1994; Ward, Abraham, McFadyen, Haines, North, Patel, et al., 1988). In another set of

396

published reports, it was described a higher birthweight (Fonnebo, 1994; Lakin,

397

Haggarty, Abramovich, Ashton, Moffat, McNeill, et al., 1998). In line with this, two

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ACCEPTED MANUSCRIPT additional studies have shown that a high intake of vegetables and fruits may be linked

399

to an increase not only in birthweight but also in fetal size (Mikkelsen, Osler, Orozova-

400

Bekkevold, Knudsen, & Olsen, 2006; Rao, Yajnik, Kanade, Fall, Margetts, Jackson, et

401

al., 2001). Both studies highlighted the putative role of green leafy vegetables on this

402

outcome.

403

Globally, the interpretation of these data is far from being a simple task, since age, sex,

404

ethnics and culture are variables that may influence the global effects of vegetarian diets

405

on birthweight. One study also revealed that vegetarian mothers had an increased

406

probability to have children with congenital malformations, namely, hypospadias (North

407

& Golding, 2000), but the details about this association remain to be unraveled.

408

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6. Impact on children development

410

Vegetarian diets are often associated to a lower exposure to toxic molecules. Moreover,

411

it is also characterized by higher intakes of antioxidants and other bioactive molecules

412

that may confer additional protection against external agents. Consequently, this feeding

413

pattern may have a profound impact on offspring not only during fetal development, but

414

also in the development of the newborns, and later in life.

415

Nitrate, nitrite and N-nitroso compounds are known to increase the incidence of neural

416

tube defects and pediatric brain tumors (Pistollato, Sumalla Cano, Elio, Masias Vergara,

417

Giampieri, & Battino, 2015). The main dietary sources of these molecules are cured

418

meat and smoked fish (Lijinsky, 1999), which are absent in vegetarian diet patterns,

419

although pickled vegetables may also contain relevant amounts of them. Globally, the

420

risk of developing diseases associated to nitrate, nitrite and N-nitroso compounds is

421

lower in children from vegetarian mothers (Brender, Werler, Shinde, Vuong, Kelley,

422

Huber, et al., 2012; Pogoda, Preston-Martin, Howe, Lubin, Mueller, Holly, et al., 2009).

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ACCEPTED MANUSCRIPT The incidence of some immune dysfunction, particularly hypersensibility reactions,

424

appears to be decreased with the adoption of a vegetarian diet during pregnancy

425

(Pistollato, Sumalla Cano, Elio, Masias Vergara, Giampieri, & Battino, 2015). More

426

precisely, the increased maternal intake of antioxidants, particularly vitamin A, C and E,

427

may reduce the risk of eczema, wheeze, asthma and atopic dermatitis (Miyake, Sasaki,

428

Tanaka, & Hirota, 2010; Nurmatov, Devereux, & Sheikh, 2011). In the case of diabetes,

429

it was proposed that plant-based diets during pregnancy may be protective for children,

430

although there is a lack of evidence to support this hypothesis (Pistollato, Sumalla Cano,

431

Elio, Masias Vergara, Giampieri, & Battino, 2015).

432

Orofacial clefts are congenital defects that are strongly associated to a low intake of

433

folic acid. Not surprisingly, an increased intake of vegetables and other plant-derived

434

foods, appear to confer some protection against those defects (Krapels, van Rooij, Ocke,

435

West, van der Horst, & Steegers-Theunissen, 2004; Pistollato, Sumalla Cano, Elio,

436

Masias Vergara, Giampieri, & Battino, 2015).

437

The present evidence points to a very significant influence of maternal dietary habits on

438

the incidence of the majority of pediatric tumors (Mosby, Cosgrove, Sarkardei, Platt, &

439

Kaina, 2012). The potentially protective foods include green leafy vegetables, fruit and

440

other plant-derived products. The beneficial effects appear to be linked to their high

441

vitamin and mineral content, as well as the presence of important antioxidants and other

442

bioactive components. These molecules may cause a significant decrease in the risk of

443

pediatric acute lymphoblastic leukemia, Wilms tumor, primitive neuroectodermal

444

tumors and anaplastic astrocytomas (Jensen, Block, Buffler, Ma, Selvin, & Month,

445

2004; Linabery, Johnson, & Ross, 2012; Pistollato, Sumalla Cano, Elio, Masias

446

Vergara, Giampieri, & Battino, 2015; Pogoda, et al., 2009; Spector, Xie, Robison,

447

Heerema, Hilden, Lange, et al., 2005).

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ACCEPTED MANUSCRIPT 448

7. Conclusions

450

The feeding pattern is one of the most important exogenous factors that may influence

451

the continuous changes that occur during pregnancy. Maternal under- or overnutrition

452

are considered risk factors for the development of several chronic diseases, that may

453

compromise the life of either the mother or the children. Not surprisingly, vegetarianism

454

may have a profound impact on mother’s health, fetal development and in the

455

development of the newborns. From an obstetric point of view, it is important to stress

456

out that the global outcomes of vegetarianism may be considerably more complex and

457

intricate than the sum of all the individual effects on both mother’s and child’s health.

458

Also, some of the potential benefits attributable to vegetarianism may be an indirect

459

consequence of it, rather than a specific effect of this feeding pattern. For example, the

460

better weight control and the decrease in the blood pressure may be linked to

461

improvements in several health markers in both the mother and the offspring. Also, the

462

adoption of vegetarianism is frequently related to healthier habits which may also

463

contribute to better health outcomes. Table 1 summarizes the main potential health

464

outcomes of vegetarianism during pregnancy. Some of the effects were directly proven

465

and are now well-documented (for example, vitamin B12 deficiency or effects on blood

466

pressure), while others are mainly assumed indirectly (for example, lower incidence of

467

gestational diabetes). The analysis of the available information regarding this issue is a

468

very difficult task, due to the high heterogeneity of data, experimental protocols,

469

variability among the characteristics of the study groups and the intricate and very

470

complex relationship between diet and lifestyle.

471

Taken together, it is important to highlight that vegetarianism may be associated to an

472

increased risk of some nutritional deficits only if the diet is not well-planned. This may

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ACCEPTED MANUSCRIPT have serious clinical outcomes and, due to that, pregnant vegetarians should seek a strict

474

follow-up by nutritionists with expertise in vegetarian nutrition. Well-planned

475

vegetarian diets appear to be safe during pregnancy, since they provide all the required

476

nutrients. Properly planned vegetarian diets are not only perfectly compatible with a

477

normal pregnancy, but may also present additional benefits in some cases, even in pre-

478

pregnancy. Thus nutritional counselling must be considered a very important strategy

479

for women in childbearing age, in order to help them to become healthier and,

480

consequently, to have healthier pregnancies. Although pre-pregnancy counselling is far

481

from being a generalized practice, this situation might have a profound impact from a

482

public health perspective. The choice for a vegetarian feeding pattern during pregnancy

483

is a personal choice that must take into account the potential risks and benefits of it.

484

Pregnant vegetarians, like pregnant omnivores, should be able to take the better

485

decisions regarding what they eat, when they eat and how many they eat. Only

486

considering feeding as a whole it is possible to achieve a healthy pregnancy.

487

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Ahola, A. J., Forsblom, C., & Groop, P. H. (2018). Adherence to special diets and its

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pregnant women. Am J Clin Nutr, 34, 1049-1055.

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Folate status during pregnancy in women is improved by long-term high vegetable

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M. (2012). Comparison of complementary feeding strategies to meet zinc requirements

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American vegetarians. J Am Diet Assoc, 103, 771-775.

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Roos, N. (2011). Food sources and intake of n-6 and n-3 fatty acids in low-income

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ACCEPTED MANUSCRIPT countries with emphasis on infants, young children (6-24 months), and pregnant and

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lactating women. Matern Child Nutr, 7 Suppl 2, 124-140.

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Mikkelsen, T. B., Osler, M., Orozova-Bekkevold, I., Knudsen, V. K., & Olsen, S. F.

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ACCEPTED MANUSCRIPT

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ACCEPTED MANUSCRIPT Table 1 – Main potential outcomes of vegetarianism during pregnancy.

Main potential health outcomes of vegetarianism during pregnancy All cases (n vegetarians) 109 (27) [Koebnick, Hoffmann, Dagnelie, Heins, Vitamin B12

RI PT

Wickramasinghe, Ratnayaka, Gruendel, Lindemans & Leitzmann, 2004]

60 (20) [Abraham, 1982]; 23 (17) [King, Stein & Zinc

Doyle, 1981]; 45

(25) [Haddad, Berk, Kettering,

Hubbard & Peters, 1999]

Nutritional deficiencies

32 (14) [Thomas & Ellis, 1977]; 46 (21) [Sharma,

Iron Omega-3 fatty acids

SC

Kiran, Ramnath, Khushiani & Singh, 1994]

19 (4) [Lakin, Haggarty, Abramovich, Ashton, Moffat,

M AN U

McNeill, Danielian & Grubb, 1998]

Vitamin D

Lower blood pressure

Maternal outcomes

Fraser, 2013]

775 (775) [Carter, Furman & Hutcheson, 1987]; 144 (48) [Reddy, Sanders & Obeid, 1994]

Better weight control

1388 (50) [Stuebe, Oken & Gillman, 2009]

Lower risk of gestational diabetes

13110 (ND) [Zhang, Liu, Solomon & Hu, 2006]

TE D

Lower incidence of calf cramps Shorter gestational duration

Increased incidence of postpartum

EP

depression

108 (27) [Koebnick, Leitzmann, Garcia, Heins, Heuer, Golf, Katz, Hoffmann & Leitzmann, 2005]

144 (48) [Reddy, Sanders & Obeid, 1994] 100 (19) [Hogg-Kollars, Mortimore & Snow, 2011] 144 (48) [Reddy, Sanders & Obeid, 1994]; 144 (59) [Campbell-Brown, Ward, Haines, North, Abraham,

Lower-to-normal birthweight?

AC C

71752 (27493) [Rizzo, Jaceldo-Siegl, Sabate &

McFadyen, Turnlund & King, 1985]; 32 & Ellis, 1977]; 165

Fetal outcomes

(14) [Thomas

(112) [Ward, Abraham,

McFadyen, Haines, North, Patel & Bhatt, 1988]

19 (4) [Lakin, Haggarty, Abramovich, Ashton, Moffat, Normal-to-high birthweight?

McNeill, Danielian & Grubb, 1998]; 7285

(ND)

[Fonnebo, 1994]

Increased risk of hypospadias Lower risk of neural tube defects

7928 (3211) [North & Golding, 2000] 201 (120) [Koebnick, Heins, Hoffmann, Dagnelie & Leitzmann, 2001]

3441 (ND) [Pogoda, Preston-Martin, Howe, Lubin,

Children outcomes

Lower risk of brain tumors

Mueller, Holly, Filippini, Peris-Bonet, McCredie, Cordier & Choi, 2009]

Lower risk of immune system dysfunction

763 (ND) [Miyake, Sasaki, Tanaka & Hirota, 2010]

ACCEPTED MANUSCRIPT Lower risk of orofacial clefts

355 (50) [Krapels, van Rooij, Ocke, West, van der Horst & Steegers-Theunissen, 2004]

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ND = not defined

ACCEPTED MANUSCRIPT During pregnancy women face some nutritional challenges Vegetarianism may be associated with deficiencies in different micronutrients

Vegetarianism can be safely adopted during pregnancy

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Vegetarianism may be linked to health benefits for the mother and the children

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Pregnant vegetarians must follow rigorous nutritional counselling