Multi-Mycotoxin Long-Term Monitoring Survey on North-Italian Maize over an 11-Year Period (2011-2021): The Co-Occurrence of Regulated, Masked and Emerging Mycotoxins and Fungal Metabolites

Abstract

Maize is considered one of the most susceptible crops to mycotoxin-producing fungi throughout the world, mainly belonging to the Fusarium spp. and Aspergillus spp. Maize is mainly used as animal feeds in Italy, as well as for human consumption, being essential for all the protected designation of origin (DOP) products. Our study investigated the occurrence of regulated mycotoxins in 3769 maize grain samples collected from 88 storage centers by the National Monitoring Network over an 11-year period (2011-2021). Moreover, an in-depth survey over a 4-year period, characterized by extremely different meteorological conditions, was conducted to investigate the co-occurrence of regulated, masked, and emerging mycotoxins. The survey confirmed that Fusarium spp. was the most frequent fungi and fumonisins were the main mycotoxins that were constantly detected in the different years and areas. Moreover, the areas characterized by high fumonisin levels were also the most prone to contamination by emerging mycotoxins produced by the same Fusarium species of the Liseola section. On the other hand, as a result of climatic changes, maize grains have also been affected by the increased frequency of aflatoxin accumulation. Deoxynivalenol, zearalenone, and other emerging mycotoxins produced by the same Fusarium species as the Discolor section occurred more abundantly in some areas in Northern Italy and in years characterized by predisposing meteorological conditions.

Keywords: Aspergillus; Fusarium; aflatoxin B1; deoxynivalenol; fumonisins; survey; zearalenone.

Figure 1

Distribution of the Italian National Maize Monitoring Network in five macro-geographical areas: W, west (Torino) in red; C, center in green; SP, south of the Po River (blue); A, Adriatic (yellow); and E, east (Venezia) in purple.

Figure 2

(A) Meteorological trend during the 2011–2021 period. (B) Meteorological trend in the different investigated geographical maize areas (averaged for 2011–2021 years).

Figure 3

Diffusion of regulated mycotoxins in maize lots from drying and storage centers located in different areas in Northern Italy. For each mycotoxin, the best year with the lowest incidence and contamination was compared with the worst year, with the highest one. Each mycotoxin was expressed as a percentage of incidence over different ranges of increasing contamination, pertaining to Regulations (EC) no. 1126/2007 and no. 165/2010 [3,4]: (A) diffusion of FBs; (B) diffusion of AF B₁; (C) diffusion of DON; (D) diffusion of ZEA.

Figure 4

Contamination levels of FBs referring to the average toxin levels found in maize lots from drying and storage centers located in different areas in Northern Italy during the 2011–2021 period. Means followed by different letters are significantly different (p-value < 0.05), according to the REGW-F test, conducted separately for each year (ns = not significant, that is, the different areas were not statistically different from each other as far as the FB contamination level is concerned).

Figure 5

Contamination levels of AF B₁ referring to the average toxin levels found in maize lots from drying and storage centers located in different areas in Northern Italy during the 2012–2021 period. Means followed by different letters are significantly different (p-value < 0.05), according to the REGW-F test, conducted separately for each year (ns = not significant, that is, the different areas were not statistically different from each other as far as the AF B₁ contamination level is concerned).

Figure 6

Contamination levels of DON referring to the average toxin levels found in maize lots from drying and storage centers located in different areas in Northern Italy during the 2013–2021 period. Means followed by different letters are significantly different (p-value < 0.05), according to the REGW-F test, conducted separately for each year (ns = not significant, that is, the different areas were not statistically different from each other as far as the DON contamination level is concerned; b * = the areas A, W, SP and C were not statistically different from each other and they were assigned the letter b; *** = the areas were significantly different (p-value < 0.05) and they were assigned different letters as follows: area W→a; areas E and A→ab; areas C and SP→b).

Figure 7

Contamination levels of ZEA referring to the average toxin levels found in maize lots from drying and storage centers located in different areas in Northern Italy during the 2014–2021 period. Means followed by different letters are significantly different (p-value < 0.05), according to the REGW-F test, conducted separately for each year (ns = not significant, that is, the different areas were not statistically different from each other as far as the ZEA contamination level is concerned).

Figure 8

Diffusion of regulated mycotoxins in maize lots from drying and storage centers located in the Po Valley. The worst year, that is, the one with the highest incidence and contamination, was expressed for each mycotoxin as a percentage of incidence over different ranges of increasing contamination, pertaining to Regulations (EC) no. 1126/2007 and no. 165/2010 [3,4]: (A) diffusion of FBs; (B) diffusion of AF B₁; (C) diffusion of DON; (D) diffusion ZEA.

Figure 9

Diffusion of regulated mycotoxins in maize lots from drying and storage centers located in the Po Valley. The mean concentration, detected during the investigated years, was expressed for each mycotoxin as a percentage of incidence over different ranges of increasing contamination, pertaining to Regulations (EC) no. 1126/2007 and no. 165/2010 [3,4]: (A) diffusion of FBs; (B) diffusion of AF B₁; (C) diffusion of DON; (D) diffusion of ZEA.

Figure 10

Score plots of the considered maize lots (N = 3769) from drying and storage centers located in different areas in Northern Italy during the 2014–2021 period, marked according to the year (A) and area (B). The loadings (highlighted values > |0.5|) of each parameter (regulated mycotoxins and meteorological parameters) are reported with the two first principal components.

Figure 11

Score plots of the maize lots (N = 200) from drying and storage centers located in different areas in Northern Italy during the 2012–2015 period, marked according to the year (A) and area (B). The loadings (highlighted values > |0.5|) of each parameter (masked and emerging mycotoxins, other fungal metabolites, meteorological and insect parameters) are reported with the two first principal components.