Abstract
Purpose
In lower-income populations, high rates of neural tube defects (NTDs) are a concern. Nutritional folate deficiencies and mycotoxins in contaminated food supplies increase risk of NTDs. As physicians in public health and involved in the care of children with NTDs, pediatric neurosurgeons have an interest in the treatment and prevention of NTDs. We aimed to evaluate the literature to assess the awareness and the existence of best practices/educational materials on this issue to better guide management.
Methods
A systematic review using the National Library of Medicine PubMed database was conducted to find articles related to mycotoxins in foods causing neural tube defects. Additional citation searches of key publications and personal collections were used. Two reviewers evaluated the resulting studies for subject area analysis. Best practice recommendations were drawn from articles selected for full-text review.
Results
Seventy-three articles were identified. Most articles were found in “nutritional sciences” (18), “teratology” (14), and “toxicology” (13). No articles were found in neurosurgery. Thirty-two additional articles were identified through other sources to screen best practice recommendations. Of the 105 articles, 34 journal articles were included in best practice recommendation guidelines. Key recommendations included education of proper food storage, hygienic agricultural practices, decontamination techniques, diet diversification, folate supplementation, risk assessment, and food safety policy and public health initiatives.
Conclusion
There is an absence of neurosurgical literature–related mycotoxins and NTDs. We suggest a set of best practices/educational materials on this topic and advocate pediatric neurosurgery engagement in public health initiatives targeted towards populations most affected by mycotoxins.
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Abbreviations
- CAC:
-
Codex Alimentarius Commission
- EFSA:
-
European Food Consumption Database
- EU:
-
European Union
- FDA:
-
Food and Drug Administration
- FOA:
-
Food and Agriculture Organization
- NLM:
-
National Library of Medicine
- NTD:
-
Neural tube defects
- USA:
-
United States
- WHO:
-
World Health Organization
References
Avantaggiato G, Quaranta F, Desiderio E, Visconti A (2002) Fumonisin contamination of maize hybrids visibly damaged by Sesamia. J Sci Food Agric 83:13–18
Azaiez I, Meca G, Manyes L, Luciano FB, Fernández-Franzón M (2013) Study of the chemical reduction of the fumonisins toxicity using allyl, benzyl and phenyl isothiocyanate in model solution and in food products. Toxicon 63:137–146
Azziz-Baumgartner E, Lindblade K, Gieseker K, Rogers HS, Kieszak S, Njapau H, Schleicher R, McCoy LF, Misore A, DeCock K, Rubin C, Slutsker L, the Aflatoxin Investigative Group * (2005) Case–control study of an acute Aflatoxicosis outbreak, Kenya, 2004. Environ Health Perspect 113:1779–1783
Bankole S, Schollenberger M, Drochner W (2006) Mycotoxins in food systems in sub Saharan Africa: a review. Mycotoxin Res 22:163–169
Bergamini E, Catellani D, Dall’asta C, Galaverna G, Dossena A, Marchelli R, Suman M (2010) Fate of Fusarium mycotoxins in the cereal product supply chain: the deoxynivalenol (DON) case within industrial bread-making technology. Food Addit Contam Part Chem Anal Control Expo Risk Assess 27:677–687
Bhandari N, Raghubir P, Sharma (2002) Modulation of selected cell signaling genes in mouse liver by fumonisin B1. Chem Biol Interact 139:317–331
Bowman RM, Boshnjaku V, McLone DG (2009) The changing incidence of myelomeningocele and its impact on pediatric neurosurgery: a review from the Children’s Memorial Hospital. Childs Nerv Syst 25:801–806
Bullerman LB, Bianchini A (2007) Stability of mycotoxins during food processing. Int J Food Microbiol 119:140–146
Callihan P, Zitomer NC, Stoeling MV, Kennedy PC, Lynch KR, Riley RT, Hooks SB (2012) Distinct generation, pharmacology, and distribution of sphingosine 1-phosphate and dihydrosphingosine 1-phosphate in human neural progenitor cells. Neuropharmacology 62:988–996
Chilaka CA, De Boevre M, Atanda OO, De Saeger S (2017) The status of Fusarium mycotoxins in Sub-Saharan Africa: a review of emerging trends and post-harvest mitigation strategies towards food control. Toxins 9 Available: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5308251/. Accessed 9 April 2018
Chulze SN (2010) Strategies to reduce mycotoxin levels in maize during storage: a review. Food Addit Contam Part A 27:651–657
Doko MB, Canet C, Brown N, Sydenham EW, Mpuchane S, Siame BA (1996) Natural co-occurrence of Fumonisins and Zearalenone in cereals and cereal-based foods from eastern and southern Africa. J Agric Food Chem 44:3240–3243
Domijan A-M (2013) Fumonisin B1: a neurotoxic mycotoxin / fumonizin B1: Neurotoksični Mikotoksin. Arch Ind Hyg Toxicol 63:531–544
Gelineau-van Waes J, Voss KA, Stevens VL, Speer MC, Riley RT (2009) Maternal fumonisin exposure as a risk factor for neural tube defects. Adv Food Nutr Res 56:145–181
Gelineau-van Waes J, Starr L, Maddox J, Aleman F, Voss KA, Wilberding J, Riley RT (2005) Maternal fumonisin exposure and risk for neural tube defects: mechanisms in an in vivo mouse model. Birth Defects Res A Clin Mol Teratol 73:487–497
Githuku JN, Azofeifa A, Valencia D, Ao T, Hamner H, Amwayi S et al (2014) Assessing the prevalence of spina bifida and encephalocele in a Kenyan hospital from 2005–2010: implications for a neural tube defects surveillance system. Pan Afr Med J 18 Available: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4473786/. Accessed 9 April 2018
Haidukowski M, Pascale M, Perrone G, Pancaldi D, Campagna C, Visconti A (2004) Effect of fungicides on the development of Fusarium head blight, yield and deoxynivalenol accumulation in wheat inoculated under field conditions with Fusarium graminearum and Fusarium culmorum. J Sci Food Agric 85:191–198
Hendricks K (1999) Fumonisins and neural tube defects in South Texas. Epidemiol Camb Mass 10:198–200
Huff WE, Hagler WM (1985) Density segregation of corn and wheat naturally contaminated with aflatoxin, Deoxynivalenol and Zearalenone. J Food Prot 48:416–420
Humpf H-U, Voss KA (2004) Effects of thermal food processing on the chemical structure and toxicity of fumonisin mycotoxins. Mol Nutr Food Res 48:255–269
International Agency for Research on Cancer (IARC) (2015) Effects of aflatoxins and fumonisins on child growth. Working Group Report. IARC, Lyon, pp 17–22
Jelinek CF, Pohland AE, Wood GE (1989) Worldwide occurrence of mycotoxins in foods and feeds—an update. J Assoc Off Anal Chem 72:223–230
Lancova K, Hajslova J, Kostelanska M, Kohoutkova J, Nedelnik J, Moravcova H, Vanova M (2008) Fate of trichothecene mycotoxins during the processing: milling and baking. Food Addit Contam Part Chem Anal Control Expo Risk Assess 25:650–659
Lee US, Jang HS, Tanaka T, Oh YJ, Cho CM, Ueno Y (1987) Effect of milling on decontamination of fusarium mycotoxins nivalenol, deoxynivalenol and zearalenone in Korean wheat. J Agric Food Chem 35:126–129
Luo Y, Yoshizawa T, Katayama T (1990) Comparative study on the natural occurrence of fusarium mycotoxins (trichothecenes and zearalenone) in corn and wheat from high- and low-risk areas for human esophageal cancer in China. Appl Environ Microbiol 56:3723–3726
Marasas WFO, Riley RT, Hendricks KA, Stevens VL, Sadler TW, Gelineau-van Waes J, Missmer SA, Cabrera J, Torres O, Gelderblom WCA, Allegood J, Martínez C, Maddox J, Miller JD, Starr L, Sullards MC, Roman AV, Voss KA, Wang E, Merrill AH Jr (2004) Fumonisins disrupt sphingolipid metabolism, folate transport, and neural tube development in embryo culture and in vivo: a potential risk factor for human neural tube defects among populations consuming fumonisin-contaminated maize. J Nutr 134:711–716
Matumba L, Van Poucke C, Njumbe Ediage E, Jacobs B, De Saeger S (2015) Effectiveness of hand sorting, flotation/washing, dehulling and combinations thereof on the decontamination of mycotoxin-contaminated white maize. Food Addit Contam Part Chem Anal Control Expo Risk Assess 32:960–969
Missmer SA, Suarez L, Felkner M, Wang E, Merrill AH, Rothman KJ et al (2006) Exposure to fumonisins and the occurrence of neural tube defects along the Texas-Mexico border. Environ Health Perspect 114:237–241
Phillips TD, Lemke SL, Grant PG (2002) Characterization of clay-based Enterosorbents for the prevention of Aflatoxicosis, in mycotoxins and food safety. In: Advances in Experimental Medicine and Biology. Springer, pp 157–171 Available: https://link.springer.com/chapter/10.1007/978-1-4615-0629-4_16. Accessed 9 April 2018
Ramljak D, Calvert RJ, Wiesenfeld PW, Diwan BA, Catipovic B, Marasas WF, Victor TC, Anderson LM, Gelderblom WC (2000) A potential mechanism for fumonisin B(1)-mediated hepatocarcinogenesis: cyclin D1 stabilization associated with activation of Akt and inhibition of GSK-3beta activity. Carcinogenesis 21:1537–1546
Ryu D, Hanna MA, Bullerman LB (1999) Stability of zearalenone during extrusion of corn grits. J Food Prot 62:1482–1484
Samar MM, Neira MS, Resnik SL, Pacin A (2001) Effect of fermentation on naturally occurring deoxynivalenol (DON) in Argentinean bread processing technology. Food Addit Contam 18:1004–1010
Scott PM, Lawrence GA (1994) Stability and problems in recovery of fumonisins added to corn-based foods. J AOAC Int 77:541–545
Suarez L, Felkner M, Brender JD, Canfield M, Zhu H, Hendricks KA (2012) Neural tube defects on the Texas-Mexico border: what we’ve learned in the 20 years since the Brownsville cluster. Birth Defects Res A Clin Mol Teratol 94:882–892
Sydenham EW, Van der Westhuizen L, Stockenström S, Shephard GS, Thiel PG (1994) Fumonisin-contaminated maize: physical treatment for the partial decontamination of bulk shipments. Food Addit Contam 11:25–32
Sydenham EW, Stockenstrom S, Thiel PG, Shephard GS, Koch KR, Marasas WFO (1995) Potential of alkaline hydrolysis for the removal of Fumonisins from contaminated corn. J Agric Food Chem 43:1198–1201
Turner PC, Sylla A, Gong YY, Diallo MS, Sutcliffe AE, Hall AJ, Wild CP (2005) Reduction in exposure to carcinogenic aflatoxins by postharvest intervention measures in West Africa: a community-based intervention study. Lancet Lond Engl 365:1950–1956
Turner PC, Flannery B, Isitt C, Ali M, Pestka J (2012) The role of biomarkers in evaluating human health concerns from fungal contaminants in food. Nutr Res Rev 25:162–179
Valle-Algarra FM, Mateo EM, Medina A, Mateo F, Gimeno-Adelantado JV, Jimenez M (2009) Changes in ochratoxin a and type B trichothecenes contained in wheat flour during dough fermentation and bread-baking. Food Addit Contam Part Chem Anal Control Expo Risk Assess 26:896–906
Van Der Westhuizen L, Shephard GS, Gelderblom WCA, Torres O (2013) Fumonisin biomarkers in maize eaters and implications for human disease. World Mycotoxin J 6:223–232
Voss KA, Howard PC, Riley RT, Sharma RP, Bucci TJ, Lorentzen RJ (2002) Carcinogenicity and mechanism of action of fumonisin B1: a mycotoxin produced by fusarium moniliforme (= F. verticillioides). Cancer Detect Prev 26:1–9
Voss K, Ryu D, Jackson L, Riley R, Gelineau-van Waes J (2017) Reduction of Fumonisin toxicity by extrusion and Nixtamalization (alkaline cooking). J Agric Food Chem 65:7088–7096
Waes JG, Rainey MA, Maddox JR, Voss KA, Sachs AJ, Gardner NM et al (2012) Increased sphingoid base-1-phosphates and failure of neural tube closure after exposure to fumonisin or FTY720. Birth Defects Res A Clin Mol Teratol 94:790–803
Wagacha JM, Muthomi JW (2008) Mycotoxin problem in Africa: current status, implications to food safety and health and possible management strategies. Int J Food Microbiol 124:1–12
Wang J-S, Luo H, Billam M, Wang Z, Guan H, Tang L, Goldston T, Afriyie-Gyawu E, Lovett C, Griswold J, Brattin B, Taylor RJ, Huebner HJ, Phillips TD (2005) Short-term safety evaluation of processed calcium montmorillonite clay (NovaSil) in humans. Food Addit Contam 22:270–279
Wild CP, Gong YY (2010) Mycotoxins and human disease: a largely ignored global health issue. Carcinogenesis 31:71–82
World Health Organization (WHO) (2006) Mycotoxins in African foods: implications to food safety and health. AFRO Food Saf Newsl. www.afro.who.int/des. Accessed 9 April 2018
Wu F, Groopman JD, Pestka JJ (2014) Public health impacts of foodborne mycotoxins. Annu Rev Food Sci Technol 5:351–372
Zaganjor I, Sekkarie A, Tsang BL, Williams J, Razzaghi H, Mulinare J, Sniezek JE, Cannon MJ, Rosenthal J (2016) Describing the prevalence of neural tube defects worldwide: a systematic literature review. PLoS One San Franc 11:e0151586
Zaki MM, El-Midany SA, Shaheen HM, Rizzi L (2012) Mycotoxins in animals: occurrence, effects, prevention and management. J Toxicol Environ Health Sci 4:13–28
Acknowledgements
We thank Dr. Leland Albright for his insights in the preparation of this manuscript and guidance on his important work done in Kijabe, Kenya.
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Du, R.Y., LoPresti, M.A., Hadley, C.C. et al. Systematic review of clinician awareness of mycotoxin impact in neural tube defects and best practices for pediatric neurosurgeons: implications for public health and policy. Childs Nerv Syst 35, 637–644 (2019). https://doi.org/10.1007/s00381-018-4023-3
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DOI: https://doi.org/10.1007/s00381-018-4023-3