Common Nutritional Shortcomings in Vegetarians and Vegans

Round 1

Reviewer 1 Report

In my opinion, this review is not suitable for publication in its current form due to the fact that it is strongly biased against plant based diets in a way that exceeds the wiggle room allowed for the sacrosanct scientific debate among scientists having different positions in nutritional controversies.

Indeed, while the review of individual nutrients and their possible deficiencies in vegan and vegetarian diets is well conducted, the frame within which such data is presented is exceedingly misleading. 

The title itself is strongly misleading, for two reasons:

The term “plant-based diet” is commonly used to refer to diets that focus primarily, but not exclusively, on plant foods. The nutritional deficiencies described in the review are likely the consequence of a strict vegan diet, not a plant based one. Indeed, most of the data presented in the review about nutrient deficiencies come from studies on vegan diet. Using data from vegan diets to suggest that the outcome applies to plant based diets is simply wrong and not acceptable.

The title implies that the nutritional deficiencies are an inevitable consequence of any plant based diet, in itself, but the reality is that they only result from an “unbalanced” plant diet. This is a major difference: any diet can result in nutritional deficiencies, if it is not well planned!

Thus, a more appropriate title for this review would have been something like “Risk of nutritional deficiencies associated with an unbalanced vegan diet”!

Then, the abstract introduces two more misleading concepts:

The argument that nutrient deficiencies of plant based diet may undermine the disease prevention benefits associated with them cannot be held, since most of the available data about disease risk come from epidemiological observations, which already discount any possible nutritional deficiency.

Some of the possible nutritional deficiencies associated with an unbalanced diet apply equally to non plant based diets. For example, vitamin D efficiency currently affects the vast majority of the population (see for example Wilson LR, Tripkovic L, Hart KH, Lanham-New SA. Vitamin D deficiency as a public health issue: using vitamin D2 or vitamin D3 in future fortification strategies. Proc Nutr Soc. 2017 Aug;76(3):392-399, or Cashman KD et al. Vitamin D deficiency in Europe: pandemic? Am J Clin Nutr. 2016 Apr;103(4):1033-44). The authors are right when they say it should be supplemented if sunlight exposure is insufficient, but this is true for everyone, independent of their diet. 

The same applies to the statement about iodine and selenium to be considered “for some subgroups”: of course, some subgroups of vegans will need them just like some subgroups of the whole population. The authors themselves state that seaweed consumption in vegans may even result in an excess of iodine for some other subgroups! Again, it all boils down to the issue of having a balanced diet: vegans eating an adequate but not excessive amount of seaweeds will often have a more adequate iodine status than the rest of the average population!

Author Response

Dear Reviewer,

Many thanks for your time reviewing the manuscript and providing helpful feedback. We agree that the framing of the paper could be perceived as misleading or unclear. In response we have changed the title to something more appropriate – “Common Nutritional Shortcomings in Vegetarians and Vegans”. It was not our intention to mislead readers but rather to inform them. Yes, plant-based diets can be nutritionally adequate when well planned (we have added the position statement of the Academy of Nutrition and Dietetics on vegetarian diets to the intro), but when observed in free living subjects there is irrefutable evidence that vegans and vegetarians are at higher risk of falling short on the nutrients covered than omnivores. The aim of this paper was to raise awareness of these nutrients so that patients and health care professionals can take the appropriate actions to prevent their inadequacy. We have replaced the term “plant-based diet” throughout the text with “vegetarian” and “vegan” to remove ambiguity. The introduction has also been adjusted to better frame the aim of the review.

In response to your first comment on the abstract, our argument is that the beneficial health effects of vegetarian and vegan diets shown in observational studies may be even more potent in the presence of nutritional adequacy (particularly B12 and its implications in CVD). Therefore, the nutritional inadequacy that is widely observed in vegans and vegetarians is likely limiting the disease prevention benefits of these diets and may in cases of deficiency be undermining them. The abstract has been altered to make this clearer.

In response to your second comment, the prevalence of Vitamin D deficiency in the entire population is beyond the scope of this paper. Our paper focuses on the difference in vitamin D status between omnivores and vegetarians/vegans and the potential health consequences arising from this. We are not insinuating that omnivorous diets are perfect. We are highlighting that vegans and vegetarians may need to be even more vigilant than omnivores regarding vitamin D. Additionally, we have made the language surrounding iodine and selenium supplementation less ambiguous.

I hope you find the revisions made acceptable.

Kind regards

Reviewer 2 Report

Dear Authors,

In view of the increasing popularity of plant-based diets (balanced, planetary, flexitarian, vegetarian) and the expected nutritional transformation in this direction for health and environmental reasons, the authors highlighted a shortcoming of these diets. They can pose serious problems in covering the needs for certain vitamins and minerals. The manuscript is well and clearly written and, as a review paper, is based on the current world literature on the nutritional and health aspects of the six nutrients. The concept of showing the health disadvantages or weaknesses of plant-based diets with the consumption of specific foods is a strength of the manuscript.

In this situation, there is a need to weigh up all the 'pros' and 'cons' of plant-based diets. In this connection, I have two suggestions that may enhance the scientific value of the work.

I was under the impression that the authors accidentally took up the defence of meat as a food that must be present in the diet in order to avoid vitamin B12 and D deficiencies, also selenium and iron. In the case of vitamin B12, there are papers in the world literature that report deficiencies of this vitamin also in people who eat a lot of meat or in pregnant women who eat meat - it is worth citing these papers. The results of the current systematic review by Bärebring et al. (2023) show that there is insufficient evidence to assess whether usual or experimental vitamin B12 intake is sufficient in groups at increased risk of B12 deficiency and its consequences (children, pregnant and lactating women, young adults, older adults and vegetarians or vegans).

In discussing the potential deficiencies of these micronutrients, the authors should - perhaps in summary - cite the official position statement of The International Agency for Research on Cancer (IARC) and the cancer agency of the World Health Organization regarding the cancer risks associated with meat consumption. The association of excessive consumption of processed meat (cured, high-temperature or low-heat processed) with colorectal, pancreatic and prostate cancers was considered proven, and the association of the formation of these cancers with the consumption of red meat (mainly beef, pork and mutton) was considered probable. Moreover, recent evidence from large prospective US and European cohort studies and from metaanalyses of epidemiological studies indicates that the long-term consumption of increasing amounts of red meat and particularly of processed meat is associated with an increased risk of total mortality, cardiovascular disease, colorectal cancer and type 2 diabetes.

In this context, it is worthwhile to make more use of the cited source [24], and to refer further to the Position of the Academy of Nutrition and Dietetic on Vegetarian Diets (2016) or the positions of national societies, e.g. The Association of UK Dietitians. Virtually all of them state that the only deficient component in plant-based diets may be vitamin B12.

The second suggestion concerns the vitamin D supplementation recommended by the authors "for those with inadequate sunlight exposure" (in the Abstract and Conclusions). This is an overly popular, superficial, stereotypical and unscientific view of the issue. Vitamin D supplementation throughout the year is recommended for all elderly people and children up to the age of four. Some countries have introduced this recommendation for the whole population and all year round, others for everyone from autumn to spring, for a number of reasons, including the use of anti-UV filter creams. Also people with dark skin (people who have an African or Asian background ) may also not get enough vitamin D from sunlight.

I hope that it will not be a problem for the Authors to supplement the manuscript with these two issues, with references to relevant sources.

Kind regards

Author Response

Dear Reviewer,

Many thanks for your time reviewing the manuscript and providing valuable feedback. The aim of this review is to highlight the increased incidence of nutrient inadequacy in vegetarians and vegans compared with omnivores. This should not be misinterpreted as omnivores having no risk of deficiency. Reviewing the prevalence of nutrient deficiencies in omnivores is beyond the scope of this paper.

The position of this review is not that vegan/vegetarian diets are inherently deficient in the nutrients covered. Of course, plant-based diets can be nutritionally adequate when well planned, but when observed in free living subjects there is irrefutable evidence that vegans and vegetarians are at higher risk of falling short on the nutrients covered than omnivores. The aim of this paper was to raise awareness of these nutrients so that patients and health care professionals can take the appropriate actions to prevent their inadequacy. We have included the position of the academy of nutrition and dietetics in the introduction to make our position clearer. In light of these adjustments, we hope you can see that we are not defending meat as essential, we are simply highlighting that it is often a main source of these nutrients in omnivorous diets. We have cited the review of Bärebring et al to highlight the need for better evidence that B12 supplementation prevents deficiency in vegetarians and vegans.

Regarding Vitamin D, we have added more nuance, briefly mentioning the lifestyle and environmental factors that make sunlight exposure an unreliable source. We hope this amends our previous oversimplification.

Kind regards

Reviewer 3 Report

Thank you very much for the opportunity to read the text.
The authors did a good job describing exactly the ingredients that may be missing from a plant-based diet.
Yet, despite the fact that this is not a research article, and the review I miss the research questions that the authors were looking for answers to during the literature review. Also good, it would have been nice to include some more discussion: and cite a study by the authors that surveyed consumers about their willingness to switch from an animal diet to a plant-based diet and what the outcome was.
The Limitation section is missing.

Author Response

Dear Reviewer,

Many thanks for your time reviewing the manuscript and kind feedback. We have added a limitations section as recommended. We have also added a sentence to the end of the introduction to make the research question more clear. We made the decision to keep the review very focused to make it as practical as possible for readers, hence why there is not much discussion. We do not wish to explore consumer willingness to try plant-based diets in this paper as it feels slightly out of scope and combats our aim for brevity. We hope you understand this aim and are happy with the changes we have made.

Kind Regards

Reviewer 4 Report

This is an interesting review article that focuses on the challenges of vegan diet, vegetarian diet, and plant-based diets, which tend to emphasize only the benefits. But some modification should be needed.

This manuscript gives the impression of listing the result of previous systematic reviews.　Readers might expect novel value which this manuscript will provide. So this should be described more clearly. For example, it might be good to provide guidelines, even just your opinion, on what exactly should be done for those who are about to start a vegan diet.

 Vitamin D section: Reference 46 summarizes the advantages and disadvantages of vitamin D supplementation in parallel. Therefore, I do not think it appropriate to refer to it as the "most" efficient way to increase 25-hydroxyvitamin D in plasma.

 Iodine section: Authors introduced sea vegetables. It is certainly unlikely that Westerners would continue to consume sea vegetables such as seaweed, but how about micro algas, (e.g. spirulina), which has been attracting a lot of attention in recent years? It should be added to discussion.

Author Response

Dear Reviewer,

Many thanks for your time reviewing the manuscript and kind feedback. We have removed the sentence about vitamin D supplementation being the most efficient way to increase plasma 25-hydroxyvitamin D. Regarding iodine, we agree that seaweed is an unlikely choice for westerners, however, spirulina is not an appropriate substitute. It has very low levels of iodine because it is not grown in the sea. We have added a paragraph of recommendations at the end of the manuscript for prospective vegans to provide novel value.

We hope you find the amendments acceptable.

Kind regards

Round 2

Reviewer 1 Report

I appreciate the efforts made by the authors in improving the manuscript. 

By changing the title and the perspective, and eliminating the ambiguity between plant-based and vegetarian diets, it now all makes much more sense.

Author Response

Dear Reviewer,

We are glad that the revisions have made the manuscript more clear. Thank you for your time further reviewing the paper.

Best wishes

Reviewer 2 Report

Dear Authors/Dear Editors,

I appreciate the authors' effort in improving the manuscript. However, I still have comments regarding vitamin D. Already in the abstract, vitamin D appears in second place (after vitamin B12) as potentially deficient. I suggest toning this down a bit, as it is well known that currently only 20% of vitamin D reserve is meant to come from the diet, as contemporary  diets are poor in wild fish (×10 richer in vitamin D), wild eggs, and fresh milk/non-processed milk.  The remaining 80% is expected to be produced in our skin from the UV-B of the sun. In the last decade, the global scientific literature has unanimously highlighted widespread vitamin D deficiency, even in areas with good sunshine, reaching 80-90% of the population. While the problem was already signalled in the 1980s, changing lifestyles, including prolonged indoor exposure, avoidance of the sun, use of sunscreen, and environmental pollution are exacerbating this unfavourable situation. Even sunny countries such as Greece present a high prevalence of vitamin D deficiency.

The next comment concerns recommendations for supplementation dose. Authors write "Adults should take 1,500-2,000 IU/d of oral vitamin D to prevent deficiency" (without citing a source). Meanwhile, Papadimitriou (2017) writes that “according to the Endocrine Society’s clinical practice guidelines, optimal vitamin D supplementation doses up to 1000 IU/d for infants up to 6 months, 1500 IU/d for infants from 6 months to 1 year, 2500 IU/d for children aged 1-3 years, 3000 IU/d for children aged 4-8 years, and 4000 IU/d for everyone over 8 years can be given safely without medical supervision just to prevent vitamin D deficiency”. I have already pointed out in my first review that vitamin D supplementation throughout the year is recommended for all elderly people and children up to the age of 4 years. Some countries have introduced this recommendation for the whole population and all year round, others for everyone from autumn to spring. In conclusion, I suggest to write clearly that these deficiencies affect all omnivores, not only those following a vegan diet.

I have a further suggestion to improve the 'Introduction'. Please add in L.50 that AND in its position statement recommends vegans to supplement reliable sources of vitamin B12, such as fortified foods or supplements. And while meat and other foods of animal origin have been praised as good sources of certain nutrients, it is also necessary to point out that meat carries a risk of cancer, as I already suggested in the first review. In science we need to be objective.

In the 'Conclusions' chapter (correctly No. 10), the authors repeated the recommendations for vitamin and mineral supplementation made in an earlier chapter (correctly No. 8). I suggest avoiding this.

And some minor suggestions:

Keywords and L.266 and L.482 – the term ‘plant-based diets’ remains.

L.436 – it is, however, chapter 7.

L.476-483 – I don't understand what was the purpose of deleting 2 sentences when they were re-written without any changes.

L.484 - this is chapter 8; why does it only apply to vegans? - these tips are also important for future vegetarians. In addition, the sources of recommended supplementation regarding vitamins B12 and D and iodine should be written in the chapter. It is also worth writing 'plant-based milk alternatives' (twice here, but the word 'alternatives' may also be missing throughout the manuscript).

 L.497 - peppers, broccoli, Brussels sprouts, kale, white cabbage or parsley are much richer in vitamin C; among fruits: blackcurrant, strawberries, orange, papaya, kiwi, mandarin, mango; it is worth going beyond this stereotype.

Kind regards

Author Response

Dear Reviewer,

Thank you for your detailed feedback. With regards to vitamin D we have adjusted the recommended dosages to be in line with the upper tolerable level recommended by the Endocrine society and Papadimitriou (2017). We have also added a sentence to clarify that these recommendations also apply to omnivores. To tone down how important diet is in relation to vitamin D status we have added that only 20% of vitamin D comes from diet.

Line 41 - We have added reliable B12 sources to the position statement.

The following sentences have been added to the B12 section (lines 68-74):
“In 2015 The International Agency for Research on Cancer (IARC) classified processed meat as carcinogenic (Group 1) and red meat as probably carcinogenic (Group 2A) due to evidence of a strong association with colorectal cancer [17]. Consumption of red meat was also reported to be positively associated with pancreatic and prostate cancer and processed meat with gastric cancer. This information should be considered by health professionals when recommending sources of vitamin B12 to patients.”

We have changed all remaining “plant-based diet” terms for “vegetarian/vegan diet”.

The numbering of the chapters has been corrected.

Chapter 8 has been adjusted to also include vegetarians and references for recommendations have been added. Plant-based milks has been changed to plant-based milk alternatives throughout the manuscript.

We have added a more detailed list of vitamin C rich fruits to boost iron bioavailability.

Kind regards

Reviewer 3 Report

Thank you for sending a revised version of the article. Unfortunately, it doesn't change anything. As it stands, this article does not add anything scientifically valuable to Vegans and Vegetarians. I asked for the addition of a Discussion section to make the article look scientific. What is presented is a list on selected elements like Vitamin D, Iodine, Selenium, etc. I can find all this in a larger scope in the database of articles on nutrition.

Author Response

Dear Reviewer,

Thank you for reviewing the manuscript again. We have added a discussion section based on your feedback. We hope you find it acceptable. 

Best wishes

Reviewer 4 Report

The modifications that I pointed out were fine.

Author Response

Dear reviewer,

Thank you for your time further reviewing the manuscript.

Kind regards

Round 3

Reviewer 2 Report

Dear Authors,

I am satisfied with the revised version of the manuscript. Issues that could mislead readers have been clarified, necessary additions have been made to the text (including new references) and proper diet names have been introduced. Chapter numbering has also been corrected. Conclusions have been made clear and transparent by removing repetition regarding supplementation doses. In my opinion, the scientific value of the current version of the manuscript is adequate for publication in Dietetics.

Kind regards

Reviewer 3 Report

Accept