Aspergilli were reported in a total of ca. 90 foods (Table S1
) which is higher than that for Fusarium
, or Mucor
. Seven species of aspergilli were recorded. A. flavus
was listed the most from foods which may reflect its significance as the producer of the most important mycotoxins, the aflatoxins, in that the identification of this fungus would take precedence over others within food mycology. A. fumigatus
was the second most frequent species listed from the foods and is of great importance as a human pathogen. Aspergillus niger
was frequently found in foods in which aspergilli were detected, and is a producer of the important mycotoxins ochratoxin A and fumonisin B2.
was reported frequently from cereals such as barley, rice and wheat and other individual foods. The fungus was common from nuts, being recorded from copra, hazelnuts, peanuts, and walnuts. A. flavus
was again listed more frequently and was only not recorded from cashews and candle nuts (Table S1
). A. fumigatus
was reported from melon seeds and oilseeds, and A. flavus
was from amaranth, oil, rape, sesame, and sunflower seeds. Bread was a source of A. flavus
: A. fumigatus
was isolated from baldi bread (Table S1
). It is likely that freshly baked bread would be free of fungal contamination and not present a health risk. A. flavus
was listed frequently from beans (Table S1
) which could be a serious source of infection. Cocoa was reported as a source of A. fumigatus
, whereas A. flavus
and A. niger
were recorded from coffee. A. fumigatus
was found from low fat buffalo cheese and processed cheese: these may represent particular risks. A. flavus
was reported from milk and cheese which may be worthy of further research. The foods mentioned above are likely sources of infection with these most dangerous FF.
Remarkably, A. fumigatus
was unrecorded from fruit, except pickled mangoes, and fruit may be useful for immunocompromised individuals. A. flavus
was common and found from dried fruit, citrus, litchis, pineapples, pomegranates and tomatoes, some of which are tropical. The fungus was seldom reported from more common fruits such as apples, bananas, grapes, pears and oranges (Table S1
), some of which are from temperate climate crops. This difference might be explained by the species being associated with warmer climates. In addition, A. fumigatus
is a thermophilic species and may not grow optimally in temperate climates. A recommendation is that fruits from temperate climates could be safer in a general sense, although more work is required.
Few herbs, spices and truffles were reported to contain A. fumigatus
, which is noteworthy, although the general category of “spices” was contaminated. A. flavus
is more common, with contamination of peppers being important. A. fumigatus
was found from dried fish, stored eggs, and cured and processed meat (Table S1
), and A. flavus
had a different profile within this group of foods. These foods may pose particular risks. A. fumigatus
was not reported from baked goods (except baldi bread which is a specialized commodity), beans (apart from soybeans), beverages (apart from cocoa), fruit (apart from pickled mangoes), and herbs (Table S1
), and these may be safe from this perspective.
The maximum number of Aspergillus species detected in a particular commodity was three for corn/maize (including a snack) (A. flavus was one of the fungi detected), rice, hazelnuts, peanuts, and walnuts. These foods present a considerable risk. A. fumigatus and A. flavus were reported in soybeans, barley, rice, wheat, “spices”, copra, hazelnuts, peanuts, walnuts, and oilseeds, which consequently represent high risk foods.
Fusaria were reported from a wide range of food [17
] (Table 1
), particularly from fruit, beans, vegetables, and cereals, but were not listed in baked goods (Table S1
). Only one case of the genus being isolated from dairy (F. moniliforme
[current valid name is F. verticillioides
] from cheese) and beverages (F. oxysporum
from cacao beans and leaves, which together are considered as one substrate) was reported. Numerous species are recoded from herbs/spices/truffles: F. oxysporum
was reported from truffles. Hence, these might be an important source of infections by this genus. Nuts are obvious fomites and species were reported frequently from seeds, with an overall profile similar to nuts. Fusaria were common throughout the vegetables, indicating they may be serious sources of infection.
) was most frequently isolated from foods of the fusaria recorded, which may relate to the involvement of this fungus in wilts of crops where they would be reported frequently in plant pathology related papers. Fusarium verticillioides
was listed frequently (Table S1
) and fungus is a well-known fumonisin mycotoxin producer, perhaps explaining why many foods are reported as contaminated by this fungus, because it is particularly important. Fumonisin contamination of corn and other cereals is primarily from F. verticillioides
, which was typically reported as F. moniliforme
until ca. 10 years ago. The trichothecene producing fungus Fusarium graminearum
was only recorded from 0.8% of the foods, and may be rare in other foods apart from corn/maize. Fusarium solani
was reported frequently which causes foot and root rot of diverse hosts and may explain its frequency of detection. Many of the foods had numerous species of Fusarium
reported from them, including: (a) corn/maize, sorghum, bananas and peanuts (seven); (b) soybeans (six); and (c) coriander (four) (Table S1
2.4. General Discussion
In general, the greatest sources of potential infection are nuts and cereals (Table S1
) and these are well known to harbour biodeteriorating fungi. Foods grown close to the soil appear as more highly contaminated (e.g., vegetables, peanuts, and cereals) and soil is known as a frequent source of pathogenic FF [43
]. The contamination of fruit may relate to the plant pathogenic activities of some human disease fungi, especially the fusaria. Finally, baked goods are almost free of the most infective fungi and appear to be safe, although the less important FFHP may be present (Table S1
Soy products, butter, margarine, dried milk, condensed milk, jams, jellies, eggs, and salmon, amongst others, are examples of what may be safe products when Table 2
and Table S1
are considered. These have none of the three most important fungi described herein and only few of the lesser pathogens. However, further testing is required to establish their safety more clearly.
The foods from which aspergilli, fusaria and Mucor
were not detected can be determined from Table S1
and Table 2
: these may be considered as “low risk” under this present assessment. Table 2
is compiled from foods from which at least one pathogenic fungi was reported. Information on foods from which fungi were not isolated when tested would not be published in general. The current authors recommend these results are published in the future for the advancement of producing safe food. The foods from which aspergilli, fusaria and Mucor
were not reported represent those foods from which at least one other FFHP was listed (Table S1
), and hence cannot be considered as free from FFHP.
Bouakline et al. [5
] considered that Aspergillus
in food is an indirect source of airway or digestive tract colonisation of particular concern to haematology units. They provided a list of 36 foods from which fungi were isolated taken from ward kitchens, a central kitchen and a hospital pharmacy and focused on the aspergilli, where some were identified to species and A. fumigatus
was prevalent. FF were far more frequent than yeasts. The others were identified as members of the Mucorales, Trichoderma
: pepper and tea were contaminated highly with aspergilli and members of the Mucorales.
In general, candidates undergoing conditioning therapy and recipients of haematopoietic cell transplantation (HCT) should avoid foods that increase the risk of exposure to fungi [6
]: a table of foods that HCT recipients may eat and should avoid is provided. The foods groups include dairy, meat, meat substitutes, fruits, nuts, starters, soups, vegetables, bread, grains, cereals, beverages, desserts and others. Much of the information in [6
] is devoted to yeasts and the FF diseases mentioned only include aspergillosis and fusariosis. Zygomycetes and Scedosporium prolificans
are discussed indirectly, but which foods were associated with particular fungi was not indicated.
Sipsas and Kontoyiannis [7
] describe the risk of particular lifestyles on invasive fungal (yeast and FF) infections and mention diet briefly. Brenier-Pinchart et al. [8
] established a protocol for food management for allogeneic stem-cell transplant recipients in a protected ward in relation to FF. They confirm that other FF infections were rising apart from the known increase from A. fumigatus
and confirm that the gastrointestinal tract might be a portal of entry from contaminated food ingestion or food intentionally containing fungi (e.g., blue cheese). Pepper and teas bags were prohibited and foods containing fungi as part of the food production process were recommended as to be avoided. FF were isolated every year from 1992 to 2002 in their analysis of protected food for patients.
Opportunistic fungal infections remain common consequences of cancer treatment [9
], when the patients are often at home between treatments with uncontrolled access to foods, similar to people in the general population. Alternaria
spp. were reported from fresh fruits, mouldy cheese and smoked foods: consumption should be restricted during profound neutropenia. Eating the following requires to be avoided: (a) thick skinned fruit such as bananas, grapefruits and oranges (as the skin could contaminate the flesh); (b) other fruits such as apples and strawberries during neutropenia periods; and (c) ethnic spices and nuts including black and white pepper, Brazil nuts, almonds, cashews, chestnuts, hazelnuts, pistachios and walnuts. A list of recommendations of food to eat and not eat is provided, although yeast and FF are not distinguished and the foodstuffs are considered from the point of view of fungi in general, rather than specific taxa.
The data presented in Table S1
are consistent with the list of recommended and not recommended foods in [6
]. For example, fruit and vegetables may be appropriate for HCT recipients if they are suitably washed and peeled, even if they were highly contaminated before preparation.
Bouakline et al. [5
] mention that, for example, cereals, melon, apple juice and chocolate were not contaminated by fungi. However, FF have been isolated from these commodities (Table S1
) and cereals were particularly frequently reported, as would be expected. Indeed, particular care is required with cereals. A wider range of fungi has been isolated (Table S1
) from at least some of the commodities listed in [5
]; hence, the threat from FF is greater than they indicated. The situation is different in [8
] because the food they tested was highly controlled in an attempt to limit the fungal load. The food recommendations in [9
] for patients with haematological cancers concur with the findings of the current paper, although more emphasis on avoiding untreated cereals would have been advantageous.
Cooking will destroy the problematic fungi in unprocessed food such as fresh vegetables, thus infections may occur before cooking and in the field. However, fresh vegetables are consumed frequently. It is important to point out that individual foods could cause particular problems despite not being considered a risk. For example, although dairy products appear safe, recent indication of yogurt as a source of infection by Mucor
]) needs acknowledgment. Certain foods will be surveyed more often than others and it is likely that cereals and nuts are particularly highly sampled which will tend to bias results. In general, there is a lack of awareness that ingestion of contaminated food is a source of infection and that so many fungi may be involved. Propagules may enter the atmosphere from contaminated food for example in stored food in warehouses. Agricultural workers, or those working in fresh product markets, may be exposed in this manner, as could those preparing food for eating and cooking, although the risk may be considered as small on most occasions. If a person is exposed to large amounts of inocula over a long period of time, then even immunocompetent individuals may succumb (cf. farmer’s lung diseases). These infections are not from eating food per se.
Paterson and Lima [44
] considered the effect of global warming on the presence of fungi on food and considered that thermotolerant and thermophilic fungi may dominate by succession over mesophilic fungi. A. fumigatus
was considered the greatest risk from this perspective. Hence, diseases from this fungus may be more prevalent in the future. A. flavus
may also present a greater future risk, especially in temperate countries in the near future.
It cannot be assumed that the identifications of the FF from food or from patients are correct in all cases. The identification of many FF is notoriously difficult [1
] and there are misidentifications in the literature. The fungi are often variable in culture and identifications using morphology is often based on minute difference in the structure of conidiophores for example, which are difficult to distinguish even for experts. The tables presented herein act as a foundation from which further work can be undertaken. The present paper provides more detailed information of the taxa of most concern and on which foods they may be present from data that already exists in the literature. It is important that these data are referred to in addition to fungal isolations and identifications undertaken de novo.