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RESEARCH

Commentary

Fecal Microbiota Transplantation to Prevent and


Treat Chronic Disease: Implications for Dietetics
Practice
Irene Opoku-Acheampong, MPH; Taylor McLaud, MPH; Olivia S. Anderson, MPH, PhD, RD

beneficial effects are Bifidobacterium, Faecalibacterium, and


ARTICLE INFORMATION
Roseburia, all having anti-inflammatory properties.10 How-
Article history: ever, not all bacteria are always beneficial11 and can become
Submitted 11 March 2021
Accepted 28 August 2021 pathogenic and disease causing,12 depending on their quan-
tity in the gut and host lifestyle factors.5,10 Such bacteria
include Escherichia coli and Salmonella typhimurium.13 These
Keywords: bacteria can produce toxins that hinder protective mecha-
Clostridium difficile nisms the body has in place to fight pathogens.13
Chronic disease Gut dysbiosis, the alteration of the microbial community
Fecal microbiota transplantation
Gut microbiome leading to negative health outcomes, can be caused by many
factors, such as antibiotic use, stress, or poor diet.5 These
2212-2672/Copyright ª 2022 by the Academy of Nutrition and Dietetics.
factors can cause excessive growth of harmful bacteria and
https://doi.org/10.1016/j.jand.2021.08.112 increased susceptibility to pathogens in the gut causing
dysfunction and disorder, presenting as disease or inflam-
mation.3,5 For example, high dietary intake of animal-based

T
HE INCIDENCE OF CHRONIC DISEASE IS A GROWING protein can cause an imbalance in the gut and lead to car-
public health concern because 133 million Americans diovascular disease.14 Although short-chain fatty acids
live with at least one condition.1 Chronic disease is (SCFAs) can be beneficial to the human body, such as
costly to treat, altogether accounting for 75% of US contributing to cellular energy use or stress alleviation, SCFAs
health care spending and it is the country’s leading cause of can also be another potential source of gut dysfunction and
mortality.1 A multitude of factors are responsible for the inflammation in the intestinal microbiome.3,15 SCFAs can pass
increasing prevalence of chronic health conditions. One such through the bloodebrain barrier and cause neurological
factor believed to influence the development of chronic symptoms.16 Gut bacteria have a mutually beneficial rela-
conditions is the gut microbiome.2 Rehabilitating the micro- tionship in healthy people and studies in mice have shown
biome can alleviate pain associated with chronic conditions that without the microbiome there would be abnormalities.3
and reduce the cost of symptom management.3 Gut dysbiosis is not stagnant and thus has the potential to
The microbiome, gut bacterial content, is unique to each be modified. For example, as fecal microbiota transplantation
individual based on diet, presence of disease or infection, and (FMT) becomes more widely used, the ability of diet to
other factors.3 The microbiome is involved in various pro- modify the microbiota has also been appreciated.17 Regis-
cesses within the human body, including immunity, meta- tered dietitians (RDs) could play an integral role by working
bolic health, and brain function.4,5 Although there is a general with patients who have undergone FMT to sustain the newly
definition of a healthy gut, specifics of the actual makeup of it colonized gut and provide education on appropriate foods for
vary based on population, geography, lifestyle, and more.6 For an improved outcome. RDs should be aware of FMT and be
instance, athletic populations have distinct microbiota com- prepared to provide suitable interventions. This commentary
positions, with an increased ratio of Bacteroidetes to Firmi- describes the potential of FMT to be used as an alternative
cutes, compared with inactive populations.7 Geographical and prominent treatment of chronic disease linked to
differences will certainly cause differences in microbiota inflammation and reduced gut microbiome diversity. By
composition due to availability and consumption of specific increasing microbiota diversity and richness, FMT can be a
foods.8 Further, the functional redundancy, or highly cost-effective and long-lasting treatment that may prevent
conserved gene composition or functional capacity of the relapse of infections or disease and improve medical costs.
microbiome across human beings is potentially considered a
marker of a healthy microbiota.9 Although microbiota di-
versity and richness have been shown to promote a healthy AN OVERVIEW OF FMT
gut, the diverse bacteria do function analogously while being The earliest use of FMT was in the 16th century, documented
made up of similar genes. Determining which microbes in a Chinese emergency medicine handbook.18 FMT is the
benefit the gut is also an area of uncertainty because the infusion of feces filtrated from a healthy donor into the in-
potential effects of some microbes are known but the testines of a recipient to manage a disease.19 After infusion,
research is not exhaustive. Some bacteria known to have the “healthy” bacteria colonize the gut in dysbiosis,

ª 2022 by the Academy of Nutrition and Dietetics. JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 33
RESEARCH

promoting symbiosis and ridding the gut of dominant, metabolic phenotypic expression, it is promising that FMT
harmful bacteria by outcompeting them.20 can increase insulin sensitivity in a person with type 2 dia-
Current methods of FMT include fecal suspension in the betes.31 Specific microbes that have shown promise to
form of an enema, infusion through nasoduodenal tube, improve insulin sensitivity are Bacillus spp,32 Bifidobacterium,
infusion through the upper gastrointestinal (GI) tract using a and Butyricimonas33 by potentially reducing adipose tissue
nasogastric tube, colonoscopy, or by swallowing a capsule.19 inflammation.34
FMT delivery methods have been administered in various
experimental settings, including hospitals or homes, but Cancer
because FMT is still considered an investigational treatment Animal research has shown promising effects of FMT in
for most conditions, a clinical setting is recommended.21,22 To treating cancer symptoms and complications such as
donate fecal matter for FMT, there is an extensive screening cachexia or progression of malignancy in several types of
process regarding existing conditions, allergies, lifestyle cancers, including lung cancer, colon cancer, or leukemia.35,36
practices, and medication use of the potential donor.23 The For example, Enterococcus hirae and Barnesiella intestiniho-
stool and blood of potential donors are screened for minis bacteria can inhibit the growth and progression of
communicable diseases.24 More successful outcomes have malignancy related to colon cancer.35 These bacteria with
been documented in donors who share similar microbiome potential antitumor promoting mechanisms can be intro-
characteristics with a recipient before infection or disorder; duced into the gut via FMT after a cancer diagnosis, or be
however, similar advantages are noted in donors who may transplanted into those at high-risk of developing cancer due
not have similar microbial intestinal makeup but are to organ damage and inflammation as a preventive
healthy.19 treatment.

THE SUCCESS OF FMT TO TREAT CLOSTRIDIUM Psychiatric Disorders


DIFFICILE INFECTIONS The intimate connection between the gut and brain has led to
FMT has shown the most success in treating C difficile, a investigation of FMT as a treatment of psychiatric disorders,
bacterium responsible for 500,000 GI-related illnesses per such as mood disorders, substance use disorder, and eating
year in the United States.25 In a systematic review by Quraishi disorders.37 Examples of potential mechanisms of the gut and
and colleagues,20 there was a 92% success rate in the treat- brain relationship is through immune, endocrine, and neural
ment of C difficile infections with FMT. Observational studies pathways. For example, a gut in dysbiosis has increased levels
were found to have as high as a 90% cure rate from C difficile of SCFAs and these specifically influence the vagus nerve.37
infections using FMT and a randomized control trial in in- Chinna and colleagues37 proposed that psychiatric symp-
dividuals with recurrent C difficile infections showed an 81% toms, such as compulsivity and anxiety, could be managed by
cure rate compared with a 31% cure rate in individuals transferring microbiota of individuals without psychiatric
treated with an antibiotic.26,27 As such, FMT is currently only disorders to individuals with these disorders.
approved for C difficile infections as treatment in that FMT has
shown the most success. Due to the remarkable results of Neurodegenerative Diseases
FMT in treating C difficile infections, experts are investigating Research has shown promise of FMT in treating neurode-
other ways in which FMT can be used.24 generative diseases such as Parkinson disease (PD). For
example, evidence from animal studies suggests that com-
POTENTIAL IMPLICATIONS OF FMT ON CHRONIC ponents of the microbiome can either prevent or promote
DISEASE PD.38 Many patients with PD experience GI symptoms before
FMT is currently being investigated for the treatment of their diagnosis, indicating an important relationship between
cardiometabolic, neurological, psychiatric, neoplastic, auto- the gut and nervous system. Animal studies have demon-
immune/inflammatory, and GI disorders.19 This wide range of strated that FMT from non-PD to PD mice reduces SCFA
potential treatment with FMT demonstrates the importance make-up in their gut.38 Similarly, gut microbiota from PD
of the microbiome and potential for a cost-effective, safe mice transplanted into non-PD mice can cause motor ab-
treatment for chronic disease. Although trials have begun in normalities.21 Although these animal studies have been
human beings for many chronic conditions, it is important to promising for the future of FMT, extensive research is needed
note as conditions are discussed in this section, that addi- to understand the mechanisms of using FMT to treat PD or
tional research is required to determine whether or not FMT other neurodegenerative diseases in human beings.
should be considered and approved as a recommended
intervention for these chronic diseases. INFLUENCE OF FMT ON PUBLIC HEALTH AND
DIETETICS PRACTICES
Metabolic Health The utilization of FMT in clinical settings will have an influ-
Changes in diversity of the microbiome seem to play an ence in public health as the prevalence of chronic disease
important role in altering metabolic functions that cause continues to rise. RDs have the potential to play a key role in
disease.28 Certain microbes that promote dysbiosis have been the success of FMT. To help optimize FMT success, RDs may
identified to cause obesity in mice,29 affecting metabolic provide nutrition counseling services as part of health care
homeostasis and causing insulin resistance. Research sug- teams.
gests30 that FMT from a donor with a diverse and balanced Consultation with RDs to improve dietary intake and
microbiome may be able to correct for insulin resistance. Due nutritional status could also have the potential to support
to the nature of the microbiota’s ability to alter the host’s long-term success of FMT.39 Once a new microbial

34 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS January 2022 Volume 122 Number 1
RESEARCH

community is introduced into the gut, the host must provide being perceived as a valid and effective treatment. If this
prebiotics,40 which are defined as “substrates that are selec- stigma is widely accepted, institutions may not want to invest
tively utilized by the host microorganisms conferring a in a treatment that no one is willing to use no matter how
healthy benefit.”41 RDs could develop meal plans and pre- encouraging outcomes may be.
scribe specific medical nutrition therapies to support an FMT
patient’s new gut microbiota and prevent any deficiencies or
potential negative outcomes. RDs are also proficient in solv- THE FUTURE OF FMT
ing nutrition challenges,42 which may be integral for long- Advances in sequencing technologies can be used to identify
term FMT success. Nutrition challenges can include working biomarkers for disease to produce more customized thera-
with patients to integrate a meal plan contextually relevant pies for improved effectiveness and availability of FMT.44
to the patient’s culture and medical history. To enhance pa- Advancements in the selection of specific species and the
tient success, RDs can work with patients to help them method of transplantation of the donor stool may improve
overcome personal barriers to altering their diet such as outcomes of FMT.44 Determining the perfect microbial
helping them to identify strategies for increasing food access. composition is difficult because of several factors, including
RDs can also play a role in future diet-related research bacterial diversity, variability of microbiota make-up be-
studies. For example, fiber intake has been identified as a tween individuals, function of some bacteria, and establish-
means of managing intestinal diseases and preventing flare- ment of species that are still unknown in the GI tract,39 but
ups. Clancy and colleagues17 explored the relevance of di- determining a range of “healthy” microbiota may help
etary intake of fiber, according to the dietary guidelines, to develop criteria for the highest standard of donor micro-
patients with irritable bowel syndrome and inflammatory biota.44 Even in the case that FMT is not used directly to treat
bowel disease (IBD) who received FMT. RDs assessed partic- chronic diseases, it may result in new discoveries in the
ipants’ food diaries and it was determined that these FMT pathophysiology of these diseases and potentially other dis-
patients had higher intake of fiber than the population coveries in microbial remedial uses.45
average. Although studies have looked at the effects of FMT in The potential role that RDs could have in the use of FMT to
patients with irritable bowel syndrome and IBD, few have treat and manage chronic conditions is promising, but several
controlled for dietary intake; and this is a niche that should steps are required to make FMT a reliable and effective
be explored with controlled trials and in which RDs should be treatment option.45 For FMT to become widely accepted as a
included. RDs are trained in dietary assessment and should form of treatment for gut dysbiosis disorders, more ran-
have an integral role in research focused on the relationship domized controlled trials that include research on post-FMT
between dietary intake and FMT interventions. nutrition are needed. Once dietary guidelines are established,
RDs could incorporate evidence-based practices that support
the provision of nutrients to maintain symbiosis. Overall, RDs
LIMITATIONS OF FMT have a potential role in ensuring the success of FMT to
Although FMT is promising in treating chronic diseases improve chronic conditions, and as a result, improving pop-
connected to gut dysbiosis, the long-lasting effects of FMT ulation health.36,46,47
still need to be determined due to the lack of trials that
control for diet and short-term studies dominating the liter-
ature.26 One challenge of post-FMT is providing proper nu-
References
trients to the newly established microbiome to maintain 1. Raghupathi W, Raghupathi V. An empirical study of chronic diseases
symbiosis. Healthy microbiomes contain a balance of bacteria in the United States: a visual analytics approach. Int J Environ Res
and can only survive based on what the host, a human being Public Health. 2018;15(3):431.
in this case, consumes. In the case that there is a change in 2. Marotz CA, Zarrinpar A. Treating obesity and metabolic syndrome
diet that does not support this balance, healthy bacteria will with fecal microbiota transplantation. Yale J Biol Med. 2016;89(3):
383-388.
diminish and the microbes previously present in the dys-
3. Chassaing B, Gewirtz AT. Gut microbiota, low-grade inflammation,
biotic gut will return.26 Therefore, evidence-based nutrition and metabolic syndrome. Toxicol Pathol. 2013;42(1):49-53.
therapy provided by RDs can be a tool for prolonging FMT 4. D’Amelio P, Sassi F. Gut microbiota, immune system, and bone. Calcif
success. Long-lasting effects of FMT have been questioned Tissue Int. 2018;102(4):415-425.
after FMT patients reported side effects, such as IBD flare-ups, 5. Hawrelak JA, Myers SP. The causes of intestinal dysbiosis: a review.
although it is not clear whether they would have occurred Alt Med Rev. 2004;9(2):180-197.
even without the transplantation.19 Accordingly, Wang and 6. Mayer EA, Tillisch K, Gupta A. Gut/brain axis and the microbiota. J
Clin Invest. 2015;125(3):926-938.
colleagues43 conducted a systematic review to determine the
reported mild and serious side effects following FMT. The 7. Shanahan F, Ghosh TS, O’Toole PW. The healthy microbiome-what is
the definition of a healthy gut microbiome? Gastroenterology.
most common side effect reported was stomach discomfort, 2021;160(2):483-494.
including symptoms such as constipation, vomiting, cramp- 8. Jäger R, Mohr AE, Carpenter KC, et al. International Society of Sports
ing, and bloating.43 Some serious side effects were reported Nutrition Position Stand: probiotics. J Int Soc Sports Nutr. 2019;16(1):
in the literature, although not as frequent, and included 62.
pathogen infections. More precise measures of these adverse 9. Tian L, Wang XW, Wu AK, et al. Deciphering functional redundancy
in the human microbiome. Nat Commun. 2020;11(1):6217.
effects will aid in differentiating between disease- or FMT-
10. Zuo T, Sun Y, Wan Y, et al. Human-gut-DNA virome variations across
related symptoms.2
geography, ethnicity, and urbanization. Cell Host Microbe.
Lastly, there are social and cultural stigmas associated with 2020;28(5):741-751.e4.
transplantation of fecal matter into an individual from 11. Louca S, Polz MF, Mazel F, et al. Function and functional redundancy
someone else.2 This stigma can have some influence on FMT in microbial systems. Nat Ecol Evol. 2018;2(6):936-943.

January 2022 Volume 122 Number 1 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 35
RESEARCH

12. Sethi S, Shukla R, Bala K, Gautam V, Angrup A, Ray P. Emerging 30. Vrieze A, Van Nood E, Holleman F, Salojärvi J, Kootte RS,
metronidazole resistance in Bacteroides spp. and its association with Bartelsman JFWM, et al. Transfer of intestinal microbiota from lean
the NIM gene: a study from North India. J Glob Antimicrob Resist. donors increases insulin sensitivity in individuals with metabolic
2019;16:210-214. syndrome. Gastroenterology. 2012;143(4):913-916.e7.
13. Hu Z, Zhang W. Signaling natural products from human pathogenic 31. Kootte RS, Levin E, Salojärvi J, Smits LP, Hartstra AV, Udayappan SD,
bacteria. ACS Infect Dis. 2020;6(1):25-33. et al. Improvement of insulin sensitivity after lean donor feces in
14. Balloux F, van Dorp L. Q&A: What are pathogens, and what have they metabolic syndrome is driven by baseline intestinal microbiota
done to and for us? BMC Biol. 2017;15(1):91. composition. Cell Metab. 2017;26(4):611-619.e6.

15. van de Wouw M, Boehme M, Lyte JM, Wiley N, Strain C, O’Sullivan O. 32. Kim B, Kwon J, Kim MS, et al. Protective effects of Bacillus
Short-chain fatty acids: microbial metabolites that alleviate stress- probiotics against high-fat diet-induced metabolic disorders in mice.
induced brain-gut axis alterations. J Physiol. 2018;596(20):4923-4944. PLoS One. 2018;13(12):e0210120. https://doi.org/10.1371/journal.
pone.0210120.
16. Danneskiold-Samsøe NB, Dias de Freitas Queiroz Barros H, Santos R,
33. Kok CR, Hutkins R. Yogurt and other fermented foods as sources of
et al. Interplay between food and gut microbiota in health and dis-
ease. Food Res Int. 2019;115:23-31. health-promoting bacteria. Nutr Rev. 2018;76(suppl 1):4-15.
34. Lee H, Lee Y, Kim J, et al. Modulation of the gut microbiota by
17. Clancy AK, Lee C, Hamblin H, et al. Dietary intakes of recipients of
metformin improves metabolic profiles in aged obese mice. Gut
faecal microbiota transplantation: an observational pilot study. Nu-
Microbes. 2018;9(2):155-165.
trients. 2021;13(5):1487.
35. Herramans KM, Riner AN, Cameron ME, Trevino JG. The microbiota
18. Ju B. History of FMT & methods of treatment. Accessed June 1, 2021. and cancer cachexia. Int J Mol Sci. 2019;20(24):6267.
https://ecampusontario.pressbooks.pub/healthdiseasetopics/chapter/
7-2-history-of-fmt-methods-of-treatment/. 36. Chen D, Wu J, Jin D, Wang B, Cao H. Fecal microbiota transplantation
in cancer management: current status and perspectives. Int J Cancer.
19. Choi HH, Cho YS. Fecal microbiota transplantation: current applica- 2018;145(8):2021-2031.
tions, effectiveness, and future perspectives. Clin Endosc. 2016;49(3):
257-265. 37. Chinna MA, Forth E, Wallace CJK, Milev R. Effect of fecal microbiota
transplant on symptoms of psychiatric disorders: a systematic re-
20. Quraishi MN, Widlak M, Bhala N, et al. Systematic review with meta- view. BMC Psychiatry. 2020;20(1):299.
analysis: the efficacy of faecal microbiota transplantation for the
treatment of recurrent and refractory Clostridium difficile infection. 38. Fang X. Microbial treatment: the potential application for Parkin-
Aliment Pharmacol Ther. 2017;46(5):479-493. son’s disease. Neurol Sci. 2019;40(1):51-58.
21. Sun MF, Zhu YL, Zhou ZL, et al. Neuroprotective effects of fecal 39. Gentile CL, Weir TL. The gut microbiota at the intersection of diet and
microbiota transplantation on MPTP-induced Parkinson’s disease human health. Science. 2018;362(6416):776-780.
mice: gut microbiota, glial reaction and TLR4/TNF-a signaling 40. Hutkins RW, Krumbeck JA, Bindels LB, et al. Prebiotics: why defini-
pathway. Brain Behav Immun. 2018;70:48-60. tions matter. Curr Opin Biotechnol. 2016;37:1-7.
22. Gulati M, Singh SK, Corrie L, Kaur IP, Chandwani L. Delivery routes 41. Gibson G, Hutkins R, Sanders M, et al. Expert consensus document:
for faecal microbiota transplants: available, anticipated, and The International Scientific Association for Probiotics and
inspired. Pharmacol Res; 2020:159. Prebiotics (ISAPP) consensus statement on the definition and
23. Woodworth MH, Neish EM, Miller NS, et al. Laboratory testing of donors scope of prebiotics. Nat Rev Gastroenterol Hepatol. 2017;14(8):491-
502.
and stool samples for fecal microbiota transplantation for recurrent
Clostridium difficile infection. J Clin Microbiol. 2017;55(4):1002-1010. 42. Academy Quality Management Committee. Academy of Nutrition
and Dietetics: revised 2017 Scope of Practice for the Registered
24. Bakken JS, Borody T, Brandt LJ, et al. Treating Clostridium difficile
infection with fecal microbiota transplantation. Clin Gastroenterol Dietitian Nutritionist. J Acad Nutr Diet. 2018;118(1):141-165.
Hepatol. 2011;9(12):1044-1049. 43. Wang S, Xu M, Wang W, et al. Systematic review: adverse events
25. Centers for Disease Control and Prevention. What is C. diff?. https:// of fecal microbiota transplantation. PloS One. 2016;11(8):
e0161174.
www.cdc.gov/cdiff/what-is.html. Updated November 16, 2020.
Accessed June 5, 2021. 44. Staley C, Khoruts A, Sadowsky MJ. Contemporary applications of
26. Liubakka A, Vaughn BP. Clostridium difficile infection and fecal fecal microbiota transplantation to treat intestinal diseases in
microbiota transplant. AACN Adv Crit Care. 2016;27(3):324-337. humans. Arch Med Res. 2017;48(8):766-773.

27. van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of 45. Leshem A, Horesh N, Elinav E. Fecal microbial transplantation and its
donor feces for recurrent Clostridium difficile. N Engl J Med. potential application in cardiometabolic syndrome. Frontier Immu-
2013;368(5):407-415. nol. 2019;10:1341.
28. Haw J, Chuong K, Doherty K. FMT regulatory challenges and the lived 46. Aron-Wisnewsky J, Clément K, Nieuwdorp M. Fecal microbiota
experiences of people with IBD. Am J Bioethics. 2017;17(5):59-61. transplantation: a future therapeutic option for obesity/diabetes?
Curr Diab Rep. 2019;19(8):51.
29. Niederwerder MC. Fecal microbiota transplantation as a tool to treat
and reduce susceptibility to disease in animals. Vet Immunol Immu- 47. Valiquette L, Low DE, Pépin J, McGeer A. Clostridium difficile infection
nopathol. 2018;206:65-72. in hospitals: a brewing storm. CMAJ. 2004;171(1):27-29.

36 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS January 2022 Volume 122 Number 1
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AUTHOR INFORMATION
I. Opoku-Acheampong is a dietetic intern, Department of Nutritional Sciences, School of Public Health, University of Michigan, Ann Arbor, MI. T.
McLaud is a dietetic intern, Department of Nutritional Sciences, School of Public Health, University of Michigan, Ann Arbor, MI. O. S. Anderson is a
clinical assistant professor, University of Michigan, School of Public Health, Department of Nutritional Sciences, Ann Arbor, MI.
Address correspondence to: Olivia S. Anderson, MPH, PhD, RD, Department of Nutritional Sciences, School of Public Health, University of
Michigan, 1415 Washington Heights, Ann Arbor, MI 48109. E-mail: oliviasa@umich.edu
STATEMENT OF POTENTIAL CONFLICT OF INTEREST
No potential conflict of interest was reported by the authors.
FUNDING/SUPPORT
The authors thank the University of Michigan’s Edward Ginsberg Center Translation Grant program for support of master of public health/dietetic
students in producing a “real world” writing product significant for the field of dietetics under the support of their faculty mentor.
AUTHOR CONTRIBUTIONS
I. Opoku-Acheampong and T. McLaud collectively decided on the significance of the topic to offer perspectives and context on through a
commentary. I. Opoku-Acheampong and T.McLaud wrote the first draft of the commentary. O. Anderson provided guidance on the topic
specifically on the relevance to the dietetics field, critically reviewed the text, and wrote additional text required for a commentary manuscript.
All authors reviewed subsequent drafts of the manuscript.

THE ART OF DIETETICS


As the slugs waged war on their tops, these sweet nantes carrots kept doing their thing underground. Carrots for the win!.
Photo taken by Laura Holtrop, MS, RDN.
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January 2022 Volume 122 Number 1 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS 37

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