Essential Fatty Acid Deficiency Associates with Growth Faltering and Environmental Enteric Dysfunction in Children
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design and Specimen Collection
2.2. NEFA Profiling by Gas Chromatography Coupled with Flame Ionization Detection (GC-FID)
2.3. Investigated Clinical Biomarkers of EED
2.4. Statistical Analysis
3. Results
3.1. Summary of the Study Cohorts
3.2. Serum NEFA Profiles at 3–6 and 9 Months of Age in Pakistan Children
3.3. Enzyme Activity Indices Using Product/Precursor Ratios
3.4. Correlations between Non-Esterified Fatty Acid Concentrations and Growth Outcomes
3.5. Non-Esterified Fatty Acids and Cholestasis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Salameh, E.; Morel, F.B.; Zeilani, M.; Dechelotte, P.; Marion-Letellier, R. Animal Models of Undernutrition and Enteropathy as Tools for Assessment of Nutritional Intervention. Nutrients 2019, 11, 2233. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Iqbal, N.T.; Syed, S.; Sadiq, K.; Khan, M.N.; Iqbal, J.; Ma, J.Z.; Umrani, F.; Ahmed, S.; Maier, E.A.; Denson, L.A.; et al. Study of Environmental Enteropathy and Malnutrition (SEEM) in Pakistan: Protocols for biopsy based biomarker discovery and validation. BMC Pediatr. 2019, 19, 247. [Google Scholar] [CrossRef] [PubMed]
- Gilmartin, A.A.; Petri, W.A., Jr. Exploring the role of environmental enteropathy in malnutrition, infant development and oral vaccine response. Philos. Trans. R. Soc. B Biol. Sci. 2015, 370, 20140143. [Google Scholar] [CrossRef] [Green Version]
- Keusch, G.T.; Denno, D.M.; Black, R.E.; Duggan, C.; Guerrant, R.L.; Lavery, J.V.; Nataro, J.P.; Rosenberg, I.H.; Ryan, E.T.; Tarr, P.I.; et al. Environmental Enteric Dysfunction: Pathogenesis, Diagnosis, and Clinical Consequences. Clin. Infect. Dis. 2014, 59 (Suppl. 4), S207–S212. [Google Scholar] [CrossRef] [Green Version]
- Kosek, M.; Guerrant, R.L.; Kang, G.; Bhutta, Z.; Yori, P.P.; Gratz, J.; Gottlieb, M.; Lang, D.; Lee, G.; Haque, R.; et al. Assessment of Environmental Enteropathy in the MAL-ED Cohort Study: Theoretical and Analytic Framework. Clin. Infect. Dis. 2014, 59 (Suppl. 4), S239–S247. [Google Scholar] [CrossRef] [PubMed]
- Houssaini, F.Z.; Foulon, T.; Iraqi, M.R.; Payen, N.; Groslambert, P. Lipids, lipoproteins, and fatty acids during infantile marasmus in the Fes area of Morocco. Biomed. Pharmacother. 1999, 53, 278–283. [Google Scholar] [CrossRef] [PubMed]
- Holman, R.T.; Johnson, S.B.; Mercuri, O.; Itarte, H.J.; Rodrigo, M.A.; De Tomas, M.E. Essential fatty acid deficiency in malnourished children. Am. J. Clin. Nutr. 1981, 34, 1534–1539. [Google Scholar] [CrossRef]
- Smit, E.N.; Muskiet, F.A.; Boersma, E.R. The possible role of essential fatty acids in the pathophysiology of malnutrition: A review. Prostaglandins, Leukot. Essent. Fat. Acids 2004, 71, 241–250. [Google Scholar] [CrossRef]
- Smit, E.N.; Dijkstra, J.M.; Schnater, T.A.; Seerat, E.; Muskiet, F.A.; Boersma, E.R. Effects of malnutrition on the erythrocyte fatty acid composition and plasma vitamin E levels of Pakistani children. Acta Paediatr. 1997, 86, 690–695. [Google Scholar] [CrossRef]
- Wolff, J.A.; Margolis, S.; Bujdoso-Wolff, K.; Matusick, E.; MacLean, W.C., Jr. Plasma and Red Blood Cell Fatty Acid Composition in Children with Protein-Calorie Malnutrition. Pediatr. Res. 1984, 18, 162–167. [Google Scholar] [CrossRef] [Green Version]
- Marin, M.C.; De Tomas, M.E.; Mercuri, O.; Fernandez, A.; de Serres, C.T. Interrelationship between protein-energy malnutrition and essential fatty acid deficiency in nursing infants. Am. J. Clin. Nutr. 1991, 53, 466–468. [Google Scholar] [CrossRef] [PubMed]
- Koletzko, B.; Abiodun, P.O.; Laryea, M.D.; Bremer, H.J. Fatty acid composition of plasma lipids in Nigerian children with protein-energy malnutrition. Eur. J. Pediatr. 1986, 145, 109–115. [Google Scholar] [CrossRef] [PubMed]
- Franco, V.; Hotta, J.K.; Jorge, S.M.; dos Santos, J.E. Plasma fatty acids in children with grade III protein-energy malnutrition in its different clinical forms: Marasmus, marasmic kwashiorkor, and kwashiorkor. J. Trop. Pediatr. 1999, 45, 71–75. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, S.C.H.; Dickerman, S. Iron, thyroid hormone and essential fatty acid status of Honduran preschoolers. Nutr. Res. 1985, 5, 21–30. [Google Scholar] [CrossRef]
- Spector, A.A. Plasma Free Fatty Acid and Lipoproteins as Sources of Polyunsaturated Fatty Acid for the Brain. J. Mol. Neurosci. 2001, 16, 159–166, discussion 215–121. [Google Scholar] [CrossRef]
- Kimura, I.; Ichimura, A.; Ohue-Kitano, R.; Igarashi, M. Free Fatty Acid Receptors in Health and Disease. Physiol. Rev. 2020, 100, 171–210. [Google Scholar] [CrossRef] [Green Version]
- Rodríguez-Carrio, J.; López, P.; Sánchez, B.; González, S.; Gueimonde, M.; Margolles, A.; de los Reyes-Gavilán, C.G.; Suárez, A. Intestinal Dysbiosis Is Associated with Altered Short-Chain Fatty Acids and Serum-Free Fatty Acids in Systemic Lupus Erythematosus. Front. Immunol. 2017, 8, 23. [Google Scholar] [CrossRef] [Green Version]
- Haberman, Y.; Iqbal, N.T.; Ghandikota, S.; Mallawaarachchi, I.; Braun, T.; Dexheimer, P.J.; Rahman, N.; Hadar, R.; Sadiq, K.; Ahmad, Z.; et al. Mucosal Genomics Implicate Lymphocyte Activation and Lipid Metabolism in Refractory Environmental Enteric Dysfunction. Gastroenterology 2021, 160, 2055–2071.e0. [Google Scholar] [CrossRef]
- Zhao, X.; Setchell, K.D.R.; Huang, R.; Mallawaarachchi, I.; Ehsan, L.; Iii, E.D.; Zhao, J.; Syed, S.; Ma, J.Z.; Iqbal, N.T.; et al. Bile Acid Profiling Reveals Distinct Signatures in Undernourished Children with Environmental Enteric Dysfunction. J. Nutr. 2021, 151, 3689–3700. [Google Scholar] [CrossRef]
- Lepage, G.; Roy, C.C. Direct transesterification of all classes of lipids in a one-step reaction. J. Lipid Res. 1986, 27, 114–120. [Google Scholar] [CrossRef]
- Sagel, S.D.; Wagner, B.D.; Ziady, A.; Kelley, T.; Clancy, J.P.; Narvaez-Rivas, M.; Pilewski, J.; Joseloff, E.; Sha, W.; Zelnick, L.; et al. Utilizing centralized biorepository samples for biomarkers of cystic fibrosis lung disease severity. J. Cyst. Fibros. 2020, 19, 632–640. [Google Scholar] [CrossRef] [PubMed]
- Rodríguez-Carrio, J.; Salazar, N.; Margolles, A.; González, S.; Gueimonde, M.; de los Reyes-Gavilán, C.G.; Suárez, A. Free Fatty Acids Profiles Are Related to Gut Microbiota Signatures and Short-Chain Fatty Acids. Front. Immunol. 2017, 8, 823. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, N.; Dow, M.; Woodside, B.; German, J.B.; Quehenberger, O.; Shih, P.-A.B. Food-Intake Normalization of Dysregulated Fatty Acids in Women with Anorexia Nervosa. Nutrients 2019, 11, 2208. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Peretti, N.; Marcil, V.; Drouin, E.; Levy, E. Mechanisms of lipid malabsorption in Cystic Fibrosis: The impact of essential fatty acids deficiency. Nutr. Metab. 2005, 2, 11. [Google Scholar] [CrossRef] [Green Version]
- Werner, A.; Kuipers, F.; Verkade, H.J. Fat Absorption and Lipid Metabolism in Cholestasis. In Madame Curie Bioscience Database; Landes Bioscience: Austin, TX, USA, 2000–2013; Available online: https://www.ncbi.nlm.nih.gov/books/NBK6420/ (accessed on 1 February 2023).
- Dai, L.; Goncalves, C.M.V.; Lin, Z.; Huang, J.; Lu, H.; Yi, L.; Liang, Y.; Wang, D.; An, D. Exploring metabolic syndrome serum free fatty acid profiles based on GC–SIM–MS combined with random forests and canonical correlation analysis. Talanta 2015, 135, 108–114. [Google Scholar] [CrossRef]
- Van Hees, N.J.M.; Giltay, E.J.; Geleijnse, J.M.; Janssen, N.; Van der Does, W. DHA Serum Levels Were Significantly Higher in Celiac Disease Patients Compared to Healthy Controls and Were Unrelated to Depression. PLoS ONE 2014, 9, e97778. [Google Scholar] [CrossRef] [Green Version]
- Aghdassi, E.; Ma, D.W.L.; Morrison, S.; Hillyer, L.M.; Clarke, S.; Gladman, D.D.; Urowitz, M.B.; Fortin, P.R. Alterations in Circulating Fatty Acid Composition in Patients with Systemic Lupus Erythematosus: A pilot study. J. Parenter. Enter. Nutr. 2011, 35, 198–208. [Google Scholar] [CrossRef]
- Soliman, A.T.; ElZalabany, M.M.; Salama, M.; Ansari, B.M. Serum leptin concentrations during severe protein-energy malnutrition: Correlation with growth parameters and endocrine function. Metabolism 2000, 49, 819–825. [Google Scholar] [CrossRef]
- Ormseth, M.J.; Swift, L.L.; Fazio, S.; Linton, M.F.; Raggi, P.; Solus, J.F.; Oeser, A.; Bian, A.; Gebretsadik, T.; Shintani, A.; et al. Free fatty acids are associated with metabolic syndrome and insulin resistance but not inflammation in systemic lupus erythematosus. Lupus 2013, 22, 26–33. [Google Scholar] [CrossRef] [Green Version]
- Tvrzicka, E.; Kremmyda, L.-S.; Stankova, B.; Zak, A. Fatty acids as biocompounds: Their role in human metabolism, health and disease--A review. Part 1: Classification, dietary sources and biological functions. Biomed. Pap. 2011, 155, 117–130. [Google Scholar] [CrossRef]
- Hua, M.-C.; Su, H.-M.; Yao, T.-C.; Kuo, M.-L.; Lai, M.-W.; Tsai, M.-H.; Huang, J.-L. Alternation of plasma fatty acids composition and desaturase activities in children with liver steatosis. PLoS ONE 2017, 12, e0182277. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sardesai, V.M. The Essential Fatty Acids. Nutr. Clin. Pract. 1992, 7, 179–186. [Google Scholar] [CrossRef] [Green Version]
- Lepage, G.; Levy, E.; Ronco, N.; Smith, L.; Galeano, N.; Roy, C.C. Direct transesterification of plasma fatty acids for the diagnosis of essential fatty acid deficiency in cystic fibrosis. J. Lipid Res. 1989, 30, 1483–1490. [Google Scholar] [CrossRef] [PubMed]
- Brenner, R.R. Regulatory Function of delta6 Desaturase—Key Enzyme of Polyunsaturated Fatty Acid Synthesis. Adv. Exp. Med. Biol. 1977, 83, 85–101. [Google Scholar] [CrossRef] [PubMed]
- De Alaniz, M.J.T.; de Gomez Dumm, I.N.; Brenner, R.R. Effect of different acids with delta 9,12-dienoic structures on Δ9 desaturation activity in rat liver microsomes. Lipids 1986, 21, 425–429. [Google Scholar] [CrossRef]
- Socha, P.; Koletzko, B.; Swiatkowska, E.; Pawlowska, J.; Stolarczyk, A.; Socha, J. Essential fatty acid metabolism in infants with cholestasis. Acta Paediatr. 1998, 87, 278–283. [Google Scholar] [CrossRef]
- Cowardin, C.A.; Syed, S.; Iqbal, N.; Jamil, Z.; Sadiq, K.; Iqbal, J.; Ali, S.A.; Moore, S.R. Environmental enteric dysfunction: Gut and microbiota adaptation in pregnancy and infancy. Nat Rev Gastroenterol Hepatol 2022. [CrossRef]
- Gluckman, P.D.; A Hanson, M.; Mitchell, M.D. Developmental origins of health and disease: Reducing the burden of chronic disease in the next generation. Genome Med. 2010, 2, 14. [Google Scholar] [CrossRef] [Green Version]
- Szajewska, H.; Horvath, A.; Koletzko, B. Effect of n−3 long-chain polyunsaturated fatty acid supplementation of women with low-risk pregnancies on pregnancy outcomes and growth measures at birth: A meta-analysis of randomized controlled trials. Am. J. Clin. Nutr. 2006, 83, 1337–1344. [Google Scholar] [CrossRef] [Green Version]
- Calder, P.C.; Kremmyda, L.-S.; Vlachava, M.; Noakes, P.S.; Miles, E.A. Is there a role for fatty acids in early life programming of the immune system? Proc. Nutr. Soc. 2010, 69, 373–380. [Google Scholar] [CrossRef] [Green Version]
Demographics and Anthropometrics | Healthy Control (WHZ > 0, HAZ > −1 at Enrollment) | Undernourished Children (WHZ < −2 at Enrollment) | ||
---|---|---|---|---|
N | 51 | 365 | ||
Female, % | 24 (47%) | 142 (39%) | ||
Age, m | 3–6 | 9 | 3–6 | 9 |
HAZ | −0.665 (−0.951, −0.379) | −0.905 (−1.238, −0.572) | −2.361 (−2.515, −2.207) | −2.504 (−2.664, −2.344) |
WAZ | 0.699 (0.443, 0.955) | 0.638 (0.381, 0.896) | −2.63 (−2.70, −2.56) | −2.04 (−2.16, −1.91) |
Enzyme | Substrate | Product | Activity |
---|---|---|---|
SCD-16 | C16:0 | C16:1 | |
SCD-18 | C18:0 | C18:1 | |
D8D | C20:3n-3 | C20:4n-3 (ND) | ∆8 |
C20:2n-6 | C20:3n-6 | ∆8 | |
D6D | C18:3n-3 | C18:4n-3 (ND) | ∆6 |
C18:2n-6 | C18:3n-6 | ∆6 | |
D5D | C20:4n-3 (ND) | C20:5n-3 | ∆5 |
C20:3n-6 | C20:4n-6 | ∆5 | |
D4D | C22:5n-3 | C22:6n-3 | ∆4 |
C22:4n-6 | C22:5n-6 | ∆4 | |
ELOVL5 | C18:3n-3 | C20:3n-3 | C18 → 20 |
C22:3n-3 | C20 → 22 | ||
C18:2n-6 | C20:2n-6 | C18 → 20 | |
C22:2n-6 | C20 → 22 | ||
C18:3n-6 | C20:3n-6 | C18 → 20 | |
C20:5n-3 | C22:5n-3 | C20 → 22 | |
C20:4n-6 | C22:4n-6 | C20 → 22 | |
C22:5n-3 | C24:5n-3 (ND) | C22 → 24 | |
ELOVL6 | C16:0 | C18:0 | C16 → 18 |
NEFA | Age | n | WHZ | HAZ | WAZ | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|
r | 95% CI | p-Value | r | 95% CI | p-Value | r | 95% CI | p-Value | |||
C10:0 | 3–6 M | 385 | −0.162 | (−0.258, −0.063) | 0.001 | −0.036 | (−0.136, 0.064) | 0.484 | −0.107 | (−0.205, −0.007) | 0.036 |
9 M | 339 | 0.087 | (−0.020, 0.192) | 0.110 | 0.032 | (−0.075, 0.138) | 0.560 | 0.067 | (−0.040, 0.172) | 0.219 | |
C12:0 | 3–6 M | 385 | −0.164 | (−0.260, −0.065) | 0.001 | −0.148 | (−0.244, −0.049) | 0.004 | −0.183 | (−0.278, −0.085) | 0.0003 |
9 M | 339 | 0.026 | (−0.081, 0.132) | 0.639 | 0.024 | (−0.083, 0.130) | 0.660 | 0.016 | (−0.091, 0.122) | 0.770 | |
C14:0 | 3–6 M | 385 | −0.080 | (−0.179, 0.020) | 0.115 | −0.134 | (−0.231, −0.035) | 0.008 | −0.130 | (−0.227, −0.030) | 0.011 |
9 M | 339 | 0.054 | (−0.053, 0.160) | 0.323 | 0.002 | (−0.105, 0.109) | 0.975 | 0.025 | (−0.082, 0.131) | 0.648 | |
C16:0 | 3–6 M | 385 | 0.136 | (0.037, 0.233) | 0.008 | 0.090 | (−0.010, 0.188) | 0.076 | 0.127 | (0.027, 0.224) | 0.013 |
9 M | 339 | 0.031 | (−0.076, 0.137) | 0.569 | −0.014 | (−0.120, 0.093) | 0.803 | 0.018 | (−0.089, 0.124) | 0.746 | |
C18:0 | 3–6 M | 385 | 0.109 | (0.009, 0.207) | 0.032 | 0.113 | (0.013, 0.211) | 0.027 | 0.126 | (0.026, 0.223) | 0.014 |
9 M | 339 | −0.007 | (−0.113, 0.100) | 0.902 | 0.059 | (−0.048, 0.165) | 0.278 | 0.032 | (−0.075, 0.138) | 0.558 | |
C18:1 n-9 cis | 3–6 M | 385 | −0.108 | (−0.206, −0.008) | 0.034 | −0.107 | (−0.205, −0.007) | 0.037 | −0.137 | (−0.234, −0.038) | 0.007 |
9 M | 339 | −0.018 | (−0.124, 0.089) | 0.741 | −0.190 | (−0.291, −0.085) | 0.0004 | −0.122 | (−0.226, −0.016) | 0.025 | |
C18:1 n-7 | 3–6 M | 385 | 0.001 | (−0.099, 0.101) | 0.988 | −0.039 | (−0.138, 0.061) | 0.442 | −0.030 | (−0.130, 0.070) | 0.558 |
9 M | 339 | 0.011 | (−0.096, 0.117) | 0.834 | −0.176 | (−0.277, −0.071) | 0.001 | −0.104 | (−0.208, 0.003) | 0.056 | |
C18:2 n-6 cis | 3–6 M | 385 | 0.134 | (0.035, 0.231) | 0.009 | 0.068 | (−0.032, 0.167) | 0.186 | 0.125 | (0.025, 0.222) | 0.014 |
9 M | 339 | −0.041 | (−0.147, 0.066) | 0.452 | 0.146 | (0.040, 0.249) | 0.007 | 0.059 | (−0.048, 0.165) | 0.282 | |
C18:3 n-6 | 3–6 M | 385 | −0.027 | (−0.127, 0.073) | 0.596 | −0.139 | (−0.236, −0.040) | 0.006 | −0.120 | (−0.217, −0.020) | 0.019 |
9 M | 339 | −0.018 | (−0.124, 0.089) | 0.736 | 0.033 | (−0.074, 0.139) | 0.543 | 0.005 | (−0.102, 0.112) | 0.934 | |
C20:0 | 3–6 M | 385 | −0.110 | (−0.208, −0.010) | 0.031 | −0.036 | (−0.136, 0.064) | 0.477 | −0.082 | (−0.181, 0.018) | 0.108 |
9 M | 339 | 0.006 | (−0.101, 0.112) | 0.906 | 0.018 | (−0.089, 0.124) | 0.746 | 0.011 | (−0.096, 0.117) | 0.835 | |
C20:1 n-9 | 3–6 M | 385 | −0.098 | (−0.196, 0.002) | 0.055 | −0.022 | (−0.122, 0.078) | 0.666 | −0.068 | (−0.167, 0.032) | 0.182 |
9 M | 339 | 0.135 | (0.029, 0.238) | 0.013 | −0.017 | (−0.123, 0.090) | 0.752 | 0.071 | (−0.036, 0.176) | 0.194 | |
C20:4 n-6 | 3–6 M | 385 | 0.047 | (−0.053, 0.146) | 0.359 | 0.133 | (0.034, 0.230) | 0.009 | 0.121 | (0.021, 0.218) | 0.017 |
9 M | 339 | −0.032 | (−0.138, 0.075) | 0.562 | 0.171 | (0.066, 0.273) | 0.002 | 0.084 | (−0.023, 0.189) | 0.121 | |
C22:6 n-3 | 3–6 M | 385 | 0.022 | (−0.078, 0.122) | 0.669 | 0.218 | (0.121, 0.311) | 0.00002 | 0.174 | (0.075, 0.269) | 0.001 |
9 M | 339 | −0.030 | (−0.136, 0.077) | 0.585 | 0.206 | (0.102, 0.306) | 0.0001 | 0.105 | (−0.002, 0.209) | 0.053 | |
C24:0 | 3–6 M | 385 | −0.073 | (−0.172, 0.027) | 0.153 | −0.101 | (−0.199, −0.001) | 0.048 | −0.110 | (−0.208, −0.010) | 0.031 |
9 M | 339 | 0.048 | (−0.059, 0.154) | 0.375 | 0.076 | (−0.031, 0.181) | 0.163 | 0.074 | (−0.033, 0.179) | 0.177 | |
MUFA | 3–6 M | 385 | −0.126 | (−0.223, −0.026) | 0.014 | −0.104 | (−0.202, −0.004) | 0.042 | −0.146 | (−0.242, −0.047) | 0.004 |
9 M | 339 | 0.005 | (−0.102, 0.112) | 0.929 | −0.214 | (−0.313, −0.110) | 0.0001 | −0.123 | (−0.227, −0.017) | 0.024 | |
PUFA | 3–6 M | 385 | 0.094 | (−0.006, 0.192) | 0.064 | 0.089 | (−0.011, 0.187) | 0.080 | 0.121 | (0.021, 0.218) | 0.017 |
9 M | 339 | −0.034 | (−0.140, 0.073) | 0.527 | 0.167 | (0.062, 0.269) | 0.002 | 0.077 | (−0.030, 0.182) | 0.156 | |
n6-PUFA | 3–6 M | 385 | 0.113 | (0.007, 0.217) | 0.026 | 0.084 | (−0.016, 0.182) | 0.101 | 0.126 | (0.026, 0.223) | 0.014 |
9 M | 339 | −0.038 | (−0.144, 0.069) | 0.485 | 0.176 | (0.071, 0.277) | 0.001 | 0.080 | (−0.027, 0.185) | 0.143 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Narvaez-Rivas, M.; Setchell, K.D.R.; Galandi, S.L.; Zhao, X.; Iqbal, N.T.; Ahmed, S.; Iqbal, J.; Syed, S.; Ali, S.A.; Moore, S.R. Essential Fatty Acid Deficiency Associates with Growth Faltering and Environmental Enteric Dysfunction in Children. Metabolites 2023, 13, 489. https://doi.org/10.3390/metabo13040489
Narvaez-Rivas M, Setchell KDR, Galandi SL, Zhao X, Iqbal NT, Ahmed S, Iqbal J, Syed S, Ali SA, Moore SR. Essential Fatty Acid Deficiency Associates with Growth Faltering and Environmental Enteric Dysfunction in Children. Metabolites. 2023; 13(4):489. https://doi.org/10.3390/metabo13040489
Chicago/Turabian StyleNarvaez-Rivas, Monica, Kenneth D. R. Setchell, Stephanie L. Galandi, Xueheng Zhao, Najeeha Talat Iqbal, Sheraz Ahmed, Junaid Iqbal, Sana Syed, Syed Asad Ali, and Sean R. Moore. 2023. "Essential Fatty Acid Deficiency Associates with Growth Faltering and Environmental Enteric Dysfunction in Children" Metabolites 13, no. 4: 489. https://doi.org/10.3390/metabo13040489