Child's Nervous System

, Volume 35, Issue 4, pp 637–644 | Cite as

Systematic review of clinician awareness of mycotoxin impact in neural tube defects and best practices for pediatric neurosurgeons: implications for public health and policy

  • Rebecca Y. DuEmail author
  • Melissa A. LoPresti
  • Caroline C. Hadley
  • Sandi Lam
Original Paper



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.


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.


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.


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.


Neural tube defect Spina bifida Mycotoxin Fumonisin Folate Public health Global neurosurgery Public policy 

Abbreviations and acronyms


Codex Alimentarius Commission


European Food Consumption Database


European Union


Food and Drug Administration


Food and Agriculture Organization


National Library of Medicine


Neural tube defects


United States


World Health Organization



We thank Dr. Leland Albright for his insights in the preparation of this manuscript and guidance on his important work done in Kijabe, Kenya.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to disclose.

Supplementary material

381_2018_4023_MOESM1_ESM.docx (35 kb)
ESM 1 (DOCX 35 kb)


  1. 1.
    Avantaggiato G, Quaranta F, Desiderio E, Visconti A (2002) Fumonisin contamination of maize hybrids visibly damaged by Sesamia. J Sci Food Agric 83:13–18CrossRefGoogle Scholar
  2. 2.
    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 63:137–146CrossRefGoogle Scholar
  3. 3.
    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 113:1779–1783CrossRefGoogle Scholar
  4. 4.
    Bankole S, Schollenberger M, Drochner W (2006) Mycotoxins in food systems in sub Saharan Africa: a review. Mycotoxin Res 22:163–169CrossRefGoogle Scholar
  5. 5.
    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 27:677–687CrossRefGoogle Scholar
  6. 6.
    Bhandari N, Raghubir P, Sharma (2002) Modulation of selected cell signaling genes in mouse liver by fumonisin B1. Chem Biol Interact 139:317–331CrossRefGoogle Scholar
  7. 7.
    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 25:801–806CrossRefGoogle Scholar
  8. 8.
    Bullerman LB, Bianchini A (2007) Stability of mycotoxins during food processing. Int J Food Microbiol 119:140–146CrossRefGoogle Scholar
  9. 9.
    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 62:988–996CrossRefGoogle Scholar
  10. 10.
    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: Accessed 9 April 2018
  11. 11.
    Chulze SN (2010) Strategies to reduce mycotoxin levels in maize during storage: a review. Food Addit Contam Part A 27:651–657CrossRefGoogle Scholar
  12. 12.
    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 44:3240–3243CrossRefGoogle Scholar
  13. 13.
    Domijan A-M (2013) Fumonisin B1: a neurotoxic mycotoxin / fumonizin B1: Neurotoksični Mikotoksin. Arch Ind Hyg Toxicol 63:531–544Google Scholar
  14. 14.
    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 56:145–181CrossRefGoogle Scholar
  15. 15.
    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 73:487–497CrossRefGoogle Scholar
  16. 16.
    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: Accessed 9 April 2018
  17. 17.
    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 85:191–198CrossRefGoogle Scholar
  18. 18.
    Hendricks K (1999) Fumonisins and neural tube defects in South Texas. Epidemiol Camb Mass 10:198–200CrossRefGoogle Scholar
  19. 19.
    Huff WE, Hagler WM (1985) Density segregation of corn and wheat naturally contaminated with aflatoxin, Deoxynivalenol and Zearalenone. J Food Prot 48:416–420CrossRefGoogle Scholar
  20. 20.
    Humpf H-U, Voss KA (2004) Effects of thermal food processing on the chemical structure and toxicity of fumonisin mycotoxins. Mol Nutr Food Res 48:255–269CrossRefGoogle Scholar
  21. 21.
    International Agency for Research on Cancer (IARC) (2015) Effects of aflatoxins and fumonisins on child growth. Working Group Report. IARC, Lyon, pp 17–22Google Scholar
  22. 22.
    Jelinek CF, Pohland AE, Wood GE (1989) Worldwide occurrence of mycotoxins in foods and feeds—an update. J Assoc Off Anal Chem 72:223–230Google Scholar
  23. 23.
    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 25:650–659CrossRefGoogle Scholar
  24. 24.
    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 35:126–129CrossRefGoogle Scholar
  25. 25.
    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 56:3723–3726Google Scholar
  26. 26.
    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 134:711–716CrossRefGoogle Scholar
  27. 27.
    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 32:960–969CrossRefGoogle Scholar
  28. 28.
    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 114:237–241CrossRefGoogle Scholar
  29. 29.
    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: Accessed 9 April 2018
  30. 30.
    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 21:1537–1546Google Scholar
  31. 31.
    Ryu D, Hanna MA, Bullerman LB (1999) Stability of zearalenone during extrusion of corn grits. J Food Prot 62:1482–1484CrossRefGoogle Scholar
  32. 32.
    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 18:1004–1010CrossRefGoogle Scholar
  33. 33.
    Scott PM, Lawrence GA (1994) Stability and problems in recovery of fumonisins added to corn-based foods. J AOAC Int 77:541–545Google Scholar
  34. 34.
    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 94:882–892CrossRefGoogle Scholar
  35. 35.
    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 11:25–32CrossRefGoogle Scholar
  36. 36.
    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 43:1198–1201CrossRefGoogle Scholar
  37. 37.
    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 365:1950–1956CrossRefGoogle Scholar
  38. 38.
    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 25:162–179CrossRefGoogle Scholar
  39. 39.
    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 26:896–906CrossRefGoogle Scholar
  40. 40.
    Van Der Westhuizen L, Shephard GS, Gelderblom WCA, Torres O (2013) Fumonisin biomarkers in maize eaters and implications for human disease. World Mycotoxin J 6:223–232CrossRefGoogle Scholar
  41. 41.
    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 26:1–9CrossRefGoogle Scholar
  42. 42.
    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 65:7088–7096CrossRefGoogle Scholar
  43. 43.
    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 94:790–803CrossRefGoogle Scholar
  44. 44.
    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 124:1–12CrossRefGoogle Scholar
  45. 45.
    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 22:270–279CrossRefGoogle Scholar
  46. 46.
    Wild CP, Gong YY (2010) Mycotoxins and human disease: a largely ignored global health issue. Carcinogenesis 31:71–82CrossRefGoogle Scholar
  47. 47.
    World Health Organization (WHO) (2006) Mycotoxins in African foods: implications to food safety and health. AFRO Food Saf Newsl. Accessed 9 April 2018
  48. 48.
    Wu F, Groopman JD, Pestka JJ (2014) Public health impacts of foodborne mycotoxins. Annu Rev Food Sci Technol 5:351–372CrossRefGoogle Scholar
  49. 49.
    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:e0151586CrossRefGoogle Scholar
  50. 50.
    Zaki MM, El-Midany SA, Shaheen HM, Rizzi L (2012) Mycotoxins in animals: occurrence, effects, prevention and management. J Toxicol Environ Health Sci 4:13–28CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Rebecca Y. Du
    • 1
    Email author
  • Melissa A. LoPresti
    • 1
  • Caroline C. Hadley
    • 1
  • Sandi Lam
    • 1
  1. 1.Department of Neurosurgery, Baylor College of Medicine; Division of Pediatric NeurosurgeryTexas Children’s HospitalHoustonUSA

Personalised recommendations