Nutrients: Vegans, Vegetarians, and Omnivores: How Does Dietary Choice Influence Iodine Intake? A Systematic Review

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nutrients

Article
Vegans, Vegetarians, and Omnivores: How Does
Dietary Choice Influence Iodine Intake?
A Systematic Review
Elizabeth R. Eveleigh, Lisa J. Coneyworth, Amanda Avery and Simon J. M. Welham *
Division of Food, Nutrition & Dietetics, School of Biosciences, The University of Nottingham,
Sutton Bonington LE12 5RD, UK; elizabeth.eveleigh@nottingham.ac.uk (E.R.E.);
lisa.coneyworth@nottingham.ac.uk (L.J.C.); amanda.avery@nottingham.ac.uk (A.A.)
* Correspondence: simon.welham@nottingham.ac.uk

Received: 4 May 2020; Accepted: 26 May 2020; Published: 29 May 2020 

Abstract: Vegan and vegetarian diets are becoming increasingly popular. Dietary restrictions may
increase the risk of iodine deficiency. This systematic review aims to assess iodine intake and status in
adults following a vegan or vegetarian diet in industrialised countries. A systematic review and quality
assessment were conducted in the period May 2019–April 2020 according to Preferred Reporting Items
for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. Studies were identified in Ovid
MEDLINE, Embase, Web of Science, PubMed, Scopus, and secondary sources. Fifteen articles met
inclusion criteria. Participants included 127,094 adults (aged ≥ 18 years). Vegan groups presented the
lowest median urinary iodine concentrations, followed by vegetarians, and did not achieve optimal
status. The highest iodine intakes were recorded in female vegans (1448.0 ± 3879.0 µg day−1 ) and
the lowest in vegetarians (15.6 ± 21.0 µg day−1 ). Omnivores recorded the greatest intake in 83% of
studies. Seaweed contributed largely to diets of vegans with excessive iodine intake. Vegans appear
to have increased risk of low iodine status, deficiency and inadequate intake compared with adults
following less restrictive diets. Adults following vegan and vegetarian diets living in countries with
a high prevalence of deficiency may be more vulnerable. Therefore, further monitoring of iodine
status in industrialised countries and research into improving the iodine intake and status of adults
following vegan and vegetarian diets is required.

Keywords: iodine status; iodine intake; iodine deficiency; vegan; vegetarian

1. Introduction
Vegan and vegetarian diets have gained popularity over the past decade. Characteristically,
vegans do not consume any animal-derived products including eggs, dairy, meat, and fish. Vegetarians
exclude meat and fish but may consume milk and eggs. A subclass of the vegetarian diet may consume
fish but not meat, termed pescatarians. Despite these definitions, varying levels of strictness and
adherence to dietary restriction exist at the level of the individual [1].
The prevalence of vegetarian and vegan diets differs globally. In developing regions, meat-free
diets are traditionally adopted owing to religious, social, ecological, or economic constraints as opposed
to personal choice [2]. In industrialised countries, most individuals are afforded the choice of food
consumption and level of dietary restriction. Populations in developed countries may adopt these diets
for environmental, ethical, religious, health beliefs or social reasons. Presently, well-planned vegan
and vegetarian diets have been regarded by the British Dietetic Association and other organizations in
industrialised countries to be suitable throughout the lifespan, inclusive of infancy and pregnancy [3–5].
However, concerns have been raised regarding the ability of these diets to adequately provide essential
micronutrients, such as iodine [6].

Nutrients 2020, 12, 1606; doi:10.3390/nu12061606 www.mdpi.com/journal/nutrients


Nutrients 2020, 12, 1606 2 of 20

Iodine is an essential micronutrient, required in trace quantities, which is vital for the synthesis of
thyroid hormones—triiodothyronine (T3) and thyroxine (T4) [7]. The thyroid hormones are crucial for
the regulation of metabolism, growth, and neurological development [8]. Iodine deficiency presents
as a spectrum of clinical disorders termed ‘iodine deficiency disorders’ (IDD’s) which occur when
recommended intakes are not achieved (150 µg day−1 ) [8]. These include hypothyroidism, goitre abnormal
thyroid nodular pathology, and cretininism in infants born to mothers with a low iodine status during
pregnancy and lactation [7,9]. Low iodine intake may be a risk factor for thyroid nodule formation,
particularly in females [10,11]. Most nodules are harmless; however, some may result in thyroid
dysfunction or malignancy [11]. Excessive iodine intake (>1000 µg day−1 ) may lead to hyperthyroidism
in individuals with preexisting thyroid disease or iodine deficiency [12]. Iodine deficiency is not limited
to developing countries—mild–moderate deficiency exists in industrialised nations including Europe, UK,
Australia and select populations in the USA [9]. In 2011, iodine nutrition was highlighted as a significant
public health concern following estimates indicating that 2 billion people globally were deficient [13].
Recent data collected by the WHO show a global decline in iodine deficiency between 1993 and 2019,
suggesting that less than 8.5% of the world’s population are affected [14]. However, subgroups of
European populations are still at increased risk of iodine deficiency [6].
Iodine deficiency traditionally was assessed by monitoring the prevalence of visible goitre in
populations [7]. After the development of newer methods for measuring iodine status, it was recognized
that low-level deficiency may be present in industrialised populations not displaying obvious thyroid
enlargement [15]. Various biomarkers can be used to estimate population iodine status and intake [15].
Urinary iodine concentration (UIC) is the most common and practical marker [16]. This is because
>90% of the iodine ingested from dietary sources is readily excreted in the urine [17]. Spot UIC and 24 h
measures can be used to detect and monitor iodine adequacy and deficiency. However, these estimates
only correspond to recent intake [16]. Additionally, thyroid function tests are required routinely to detect
iodine adequacy in vulnerable populations such as pregnant and/or lactating women and infants [16].
Dietary iodine can be estimated indirectly by UIC or by common dietary assessment methods [15].
Limitations of the methods used must be considered. Biomarkers of status and dietary intake methods
are not always the same between studies which adds to the challenge of reliably comparing iodine amid
populations [18].
Individuals residing in developing countries, who are reliant on plant-based foods in their diet,
have a higher prevalence of iodine deficiency [19]. The bioavailability of iodine from plant sources
has been suggested to be determined by rainfall and water collection on crop leaves with much of the
iodine within plants not being bioavailable [20]. In industrialised countries where people consume a
‘Western diet’, the key dietary sources of iodine are bread fortified by iodised salt, cow0 s milk, and dairy
products [21]. Seafood, eggs, and seaweed are also iodine rich but are not regularly consumed [22].
Water and salt iodination strategies are present in most states in the US and select countries in
Europe [23,24]. Countries such as the UK have yet to establish a mandatory salt fortification program
and despite regular manufacturing of iodised salt, it is not widely available for public purchase [25].
For this reason, individuals who consume diets excluding iodine-rich food, principally dairy,
eggs, and/or fish, have increased risk of iodine deficiency [26]. Further complicating this issue is the
growing availability and acceptance of plant-based food ‘alternatives’, regularly consumed by vegans
and vegetarians, that naturally have negligible iodine content and are not regularly fortified [27,28].
The size of the plant-based ‘alternatives’ food market has been reported to have almost doubled
between 2014 and 2017 in the UK [29].
Currently, two reviews exist investigating iodine in the diets of vegans and vegetarians, one in
2005, which was updated in 2009 by the same authors [30,31]. The most recent review included
eight studies, covering a period between 1981 and 2003, with the conclusion that strict vegans and
vegetarians living in Europe have iodine values below recommended levels and are at risk of deficiency.
In the years since publication, these diets have become more widely accepted and it is likely that food
consumption practices have changed considerably since this last assessment of iodine intake in adults
Nutrients 2020, 12, 1606 3 of 20

following vegan and vegetarian diets. Given the potential health consequences of iodine deficiency,
it is important to re-examine whether adults following either a vegan or vegetarian diet are still at risk
of iodine deficiency.
Thus, the aim of this review is to assess the iodine intake and status in adults following a vegan
or vegetarian diet in industrialised countries across time. The objectives included (1) evaluation of
the methods used to assess iodine; (2) determination of the iodine intake and food consumption in
vegan and vegetarian adults; (3) assessment of the iodine status and prevalence of iodine deficiency
using urinary iodine concentration (UIC); (4) comparison of the iodine intake, status and prevalence of
deficiency between vegans, vegetarians and omnivores; and (5) consideration of gender differences in
estimates of iodine nutrition.

2. Materials and Methods


This systematic review was according to the Preferred Reporting Items for Systematic Reviews
and Meta-Analyses (PRISMA) checklist [32].
A systematic search of literature was performed from 20 May 2019 to April 2020. Electronic
databases (Ovid MEDLINE, Embase, Web of Science, PubMed, and Scopus) were searched using text
terms with appropriate truncation, and Medical Subject Headings. Search term sensitivity and relevance
of article identification was tested using preliminary searches in Ovid MEDLINE (Supplementary
Table S1). All database searches were refined by ‘Humans, Adults (aged < 18 years) and English
Language’. Identified relevant studies were saved onto EndNoteTM online and duplicates were
removed. To limit bias, relevance was confirmed by two investigators. Additional relevant articles
were sourced from reference lists of included studies.
The current systematic review addressed study eligibility using the population–intervention–
comparison–outcome (PICOS) formulation (Table 1) [33]. Additionally, only articles with full paper
availability published in/after 1990 were considered for inclusion.

Table 1. Population–intervention–comparison–outcome (PICOS) criteria for study inclusion


and exclusion.

Criteria Category Inclusion Exclusion


Individuals (aged < 18 y), unless results display
Adults (aged ≥ 18 y) residing in separate data; adults residing in developing
Population
industrialised nations. countries; populations with a high prevalence
of thyroid disorders.
Participants with any type of dietary
Use of a dietary grouping without defining
Intervention/exposure preference or restriction.
diet characteristics.
Voluntary or otherwise.
Comparators Differing dietary preference or restriction. None.
No analysis of iodine intake or status; use of
Iodine intake or status measured by UIC or
Outcome measure thyroid measures alone for iodine intake
analysis of dietary records.
and status.
Study design Any study design with relevant outcomes. None.

Data extraction was completed independently. The terms used for data extraction were discussed
and finalised by two secondary researchers. A modified version of “Data collection form for intervention
review—RCTs and non-RCTs” by The Cochrane Collaboration was used for data extraction [34].
Adaptions considered the characteristics of interest and study design. To permit comparison between
groups, ‘moderate vegans’ were considered as vegetarians. ‘Mixed diet’ and ‘meat eaters’ as omnivores
and ‘living food dieters’ as vegans. Due to variation in nomenclature, demi vegetarians will be
considered separately. To make comparisons between genders, where possible, data on males and
females were extracted separately.
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