Fumonisin B-1 as a Urinary Biomarker of Exposure in a Maize Intervention Study Among South African Subsistence Farmers

Background: The consumption of maize highly contaminated with carcinogenic fumonisins has been linked to high oesophageal cancer rates. The aim of this study was to validate a urinary fumonisin B-1 (UFB1) biomarker as a measure of fumonisin exposure and to investigate the reduction in exposure following a simple and culturally acceptable intervention.

Methods: At baseline home-grown maize, maize-based porridge, and first-void urine samples were collected from female participants (n = 22), following their traditional food practices in Centane, South Africa. During intervention the participants were trained to recognize and remove visibly infected kernels, and to wash the remaining kernels. Participants consumed the porridge prepared from the sorted and washed maize on each day of the two-day intervention. Porridge, maize, and urine samples were collected for FB1 analyses.

Results: The geometric mean (95% confidence interval) for FB1 exposure based on porridge (dry weight) consumption at baseline and following intervention was 4.84 (2.87-8.14) and 1.87 (1.40-2.51) mg FB1/kg body weight/day, respectively, (62% reduction, P < 0.05). UFB1C, UFB1 normalized for creatinine, was reduced from 470 (295-750) at baseline to 279 (202-386) pg/mg creatinine following intervention (41% reduction, P = 0.06). The UFB1C biomarker was positively correlated with FB1 intake at the individual level (r - 0.4972, P < 0.01). Urinary excretion of FB1 was estimated to be 0.075% (0.054%-0.104%) of the FB1 intake.

Conclusion: UFB1 reflects individual FB1 exposure and thus represents a valuable biomarker for future fumonisin risk assessment.

Impact: The simple intervention method, hand sorting and washing, could positively impact on food safety and health in communities exposed to fumonisins. Cancer Epidemiol Biomarkers Prev; 20(3); 483-9. (C)2011 AACR.

Simple intervention method to reduce fumonisin exposure in a subsistence maize-farming community in South Africa

In the Centane magisterial area of South Africa, high rates of oesophageal cancer have been associated with home-grown maize contaminated with fumonisins. The aim of this study was to implement a simple intervention method to reduce fumonisin exposure in a subsistence-farming community. The hand-sorting and washing procedures, based on traditional maize-based food preparation practices, were previously customised under laboratory-controlled conditions. Home-grown maize and maize-based porridge collected at baseline were analysed for fumonisin B1, B2 and B3. The geometric mean (95% confidence interval) of fumonisin contamination in the home-grown maize at baseline was 1.67 (1.21-2.32) mg kg-1 and 1.24 (0.75-2.04) mg kg -1 (dry weight) in the porridge. Fumonisin exposure was based on individual stiff porridge consumption and the specific fumonisin levels in the porridge (dry weight) consumed. Porridge (dry weight) consumption at baseline was 0.34 kg day-1 and fumonisin exposure was 6.73 (3.90-11.6) mu g kg-1 body weight day-1. Female participants (n = 22) were trained to recognise and remove visibly infected/damaged kernels and to wash the remaining maize kernels. The discarded kernels represented 3.9% by weight and the fumonisins varied from 17.1 to 76.9 mg kg-1. The customised hand-sorting and washing procedures reduced fumonisin contamination in the maize and porridge by 84 and 65%, respectively. The intervention reduced fumonisin exposure by 62% to 2.55 (1.94-3.35) mu g kg-1 body weight day-1. This simple intervention method has the potential to improve food safety and health in subsistence-farming communities consuming fumonisin-contaminated maize as their staple diet.

Multiple mycotoxin exposure determined by urinary biomarkers in rural subsistence farmers in the former Transkei, South Africa

Subsistence farmers are exposed to a range of mycotoxins. This study applied novel urinary multi-mycotoxin LC-MS/MS methods to determine multiple exposure biomarkers in the high oesophageal cancer region, Transkei, South Africa. Fifty-three female participants donated part of their maize-based evening meal and first void morning urine, which was analysed both with sample clean-up (single and multi-biomarker) and by a 'dilute-and-shoot' multi-biomarker method. Results were corrected for recovery with LOD for not detected. A single biomarker method detected fumonisin B1 (FB1) (87% incidence; mean±standard deviation 0.342±0.466 ng/mg creatinine) and deoxynivalenol (100%; mean 20.4±49.4 ng/mg creatinine) after hydrolysis with β-glucuronidase. The multi-biomarker 'dilute-and-shoot' method indicated deoxynivalenol-15-glucuronide was predominantly present. A multi-biomarker method with β-glucuronidase and immunoaffinity clean-up determined zearalenone (100%; 0.529±1.60 ng/mg creatinine), FB1 (96%; 1.52±2.17 ng/mg creatinine), α-zearalenol (92%; 0.614±1.91 ng/mg creatinine), deoxynivalenol (87%; 11.3±27.1 ng/mg creatinine), β-zearalenol (75%; 0.702±2.95 ng/mg creatinine) and ochratoxin A (98%; 0.041±0.086 ng/mg creatinine). These demonstrate the value of multi-biomarker methods in measuring exposures in populations exposed to multiple mycotoxins. This is the first finding of urinary deoxynivalenol, zearalenone, their conjugates, ochratoxin A and zearalenols in Transkei.

Holocene climate change and past Irish societal response

The extent to which North Atlantic Holocene climatic perturbations influenced past human societies is an area of considerable uncertainty and fierce debate. Ireland is ideally placed to help resolve this issue, being occupied for over 9000 yr and located on the eastern Atlantic seaboard, a region dominated by westerly airflow. Irish bog and lake tree populations provide unambiguous evidence of major shifts in surface moisture through the Holocene similar to cycles recorded in the marine realm of the North Atlantic, indicating significant changes in the latitude and intensity of zonal atmospheric circulation across the region. To test for human response to these cycles we summed the probabilities of 465 radiocarbon ages obtained from Irish archaeological contexts and observe enhanced archaeological visibility during periods of sustained wet conditions. These results suggest either increasing density of human populations in key, often defensive locations, and/or the development of subsistence strategies to overcome changing conditions, the latter recently proposed as a significant factor in avoiding societal collapse. Regardless, we demonstrate environmental change is a significantly more important factor in influencing human activity in the landscape than has hitherto been acknowledged.

Land-use patterns and cultural change in the Middle to Late Bronze Age in Ireland: inferences from pollen records

In Ireland, the Middle to Late Bronze Age (1500-600 cal. B.C.) is characterised by alternating phases of prolific metalwork production (the Bishopsland and Dowris Phases) and apparent recessions (the Roscommon Phase and the Late Bronze Age-Iron Age transition). In this paper, these changes in material culture are placed in a socio-economic context by examining contemporary settlement and land-use patterns interpreted from the pollen record. The vegetation histories of six tephrochronologically-linked sites are presented that provide high-resolution and chronologically well-resolved insights into changes in landscape use over the Middle to Late Bronze Age. The records are compared with published pollen records in an attempt to discern if there are any trends of woodland clearance and abandonment from which changes in settlement patterns can be inferred. The results suggest that prolific metalworking industries correlate chronologically with expansive farming activity, which indicates that they were supported by a productive subsistence economy. Conversely, declines in metalwork production occur during periods when farming activity is generally less extensive and perhaps more centralised, and it is proposed that disparate socio-economic or –political factors, rather than a collapse of the subsistence economy, lies behind the demise of metalworking industries.

Iron Age Pastoral Nomadism and Agriculture in the Eastern Eurasian Steppe: Implications from Dental Palaeopathology and Stable Carbon and Nitrogen Isotopes

Iron Age societies of the eastern Eurasian steppe are traditionally viewed as nomadic pastoralists. However, recent archaeological and anthropological research in Kazakhstan has reminded us that pastoralist economies can be highly complex and involve agriculture. This paper explores the nature of the pastoralist economies in two Early Iron Age populations from the burial grounds of Ai-Dai and Aymyrlyg in Southern Siberia. These populations represent two cultural groups of the Scythian World - the Tagar Culture of the Minusinsk Basin and the Uyuk Culture of Tuva. Analysis of dental palaeopathology and carbon and nitrogen stable isotopes suggests that domesticated cereals, particularly millet, and fish formed a major component of the diet of both groups. The findings contribute to the emerging picture of the nuances of Early Iron Age subsistence strategies on the eastern steppe.

Harvest Shortfalls, Grain prices, and Famines in Preindustrial England

The frequency of bad harvests and price elasticity of demand are measured using new data on English grain yields 1268–1480 and 1750–1850 and a revised price series. The analysis shows that major harvest shortfalls were a significant component of most historical subsistence crises, as back-to-back shortfalls were of the worst famines. Although serious harvest shortfalls long remained an unavoidable fact of economic life, by c.1800 yields had become less variable and prices less harvest sensitive. By the eve of the Industrial Revolution, England had become effectively famine-free.

Missing Links, Cultural Modernity and the Dead: Anatomically Modern Humans in the Great Cave of Niah (Sarawak, Borneo)

The Great Cave of Niah in Sarawak (northern Borneo) came into the gaze of Western Science through the work of Alfred Russell Wallace, who came to Sarawak in the 1850s to search for ‘missing links’ in his pioneering studies of evolution and the natural history of Island Southeast Asia and Australasia. The work of Tom and Barbara Harrisson in the 1950s and 1960s placed the Great Cave, and particularly their key find, the ‘Deep Skull’, at the nexus of the evolving archaeological framework for the region: for decades the skull, dated in 1958 by adjacent charcoal to c.40,000 BP, was the oldest fossil of an anatomically modern human anywhere in the world and thus critical to ideas about human evolution and dispersal. Although several authorities later questioned the provenance and antiquity of the Deep Skull, renewed investigations of the Harrisson excavations since 2000 have shown that it can be attributed securely to a specific location in the Pleistocene stratigraphy, with direct U-series dating on a piece of the skull indicating an age for it of c.37,500 BP and the first evidence for associated human activity at the site going back to c.50,000 BP. The new work also indicates that the skull is part of a cultural deposit, perhaps a precursor to the long tradition in Borneo of processing of the dead and secondary burial. These indicators of cultural complexity chime with the complexity of the subsistence behaviour of the early users of the caves discussed by Philip Piper and Ryan Rabett in chapter ten of this volume.

Growing rice aerobically markedly decreases arsenic accumulation

Arsenic (As) exposure from consumption of rice can be substantial, particularly for the population on a subsistence rice diet in South Asia. Paddy rice has a much enhanced As accumulation compared with other cereal crops, and practical measures are urgently needed to decrease As transfer from soil to grain. We investigated the dynamics of As speciation in the soil solution under both flooded and aerobic conditions and compared As accumulation in rice shoot and grain in a greenhouse experiment. Flooding of soil led to a rapid mobilization of As, mainly as arsenite, in the soil solution. Arsenic concentrations in the soil solution were 7-16 and 4-13 times higher under the flooded than under the aerobic conditions in the control without As addition and in the +As treatments (10 mg As kg(-1) as arsenite or arsenate), respectively. Arsenate was the main As species in the aerobic soil. Arsenic accumulation in rice shoots and grain was markedly increased under flooded conditions; grain As concentrations were 10-15-fold higher in flooded than in aerobically grown rice. With increasing total As concentrations in grain, the proportion of inorganic As decreased, while that of dimethylarsinic acid (DMA) increased. The concentration of inorganic As was 2.6-2.9 fold higher in the grain from the flooded treatment than in that from the aerobic treatment. The results demonstrate that a greatly increased bioavailability of As under the flooded conditions is the main reason for an enhanced As accumulation by flooded rice, and growing rice aerobically can dramatically decrease the As transfer from soil to grain.

Variation in arsenic speciation and concentration in Paddy Rice related to Dietary Exposure

Ingestion of drinking water is not the only elevated source of arsenic to the diet in the Bengal Delta. Even at background levels, the arsenic in rice contributes considerably to arsenic ingestion in subsistence rice diets. We set out to survey As speciation in different rice varieties from different parts of the globe to understand the contribution of rice to arsenic exposure. Pot experiments were utilized to ascertain whether growing rice on As contaminated soil affected speciation and whether genetic variation accounted for uptake and speciation. USA long grain rice had the highest mean arsenic level in the grain at 0.26 µg As g-1 (n = 7), and the highest grain arsenic value of the survey at 0.40 µg As g-1. The mean arsenic level of Bangladeshi rice was 0.13 µg As g-1 (n = 15). The main As species detected in the rice extract were AsIII, DMAV, and AsV. In European, Bangladeshi, and Indian rice 64 ± 1% (n = 7), 80 ± 3% (n = 11), and 81 ± 4% (n = 15), respectively, of the recovered arsenic was found to be inorganic. In contrast, DMAV was the predominant species in rice from the USA, with only 42 ± 5% (n = 12) of the arsenic being inorganic. Pot experiments show that the proportions of DMAV in the grain are significantly dependent on rice cultivar (p = 0.026) and that plant nutrient status is effected by arsenic exposure. Ingestion of drinking water is not the only elevated source of arsenic to the diet in the Bengal Delta. Even at background levels, the arsenic in rice contributes considerably to arsenic ingestion in subsistence rice diets. We set out to survey As speciation in different rice varieties from different parts of the globe to understand the contribution of rice to arsenic exposure. Pot experiments were utilized to ascertain whether growing rice on As contaminated soil affected speciation and whether genetic variation accounted for uptake and speciation. USA long grain rice had the highest mean arsenic level in the grain at 0.26 µg As g-1 (n = 7), and the highest grain arsenic value of the survey at 0.40 µg As g-1. The mean arsenic level of Bangladeshi rice was 0.13 µg As g-1 (n = 15). The main As species detected in the rice extract were AsIII, DMAV, and AsV. In European, Bangladeshi, and Indian rice 64 ± 1% (n = 7), 80 ± 3% (n = 11), and 81 ± 4% (n = 15), respectively, of the recovered arsenic was found to be inorganic. In contrast, DMAV was the predominant species in rice from the USA, with only 42 ± 5% (n = 12) of the arsenic being inorganic. Pot experiments show that the proportions of DMAV in the grain are significantly dependent on rice cultivar (p = 0.026) and that plant nutrient status is effected by arsenic exposure.

Optimising sorting and washing of home-grown maize to reduce fumonisin contamination under laboratory-controlled conditions

Subsistence farming communities with low socio-economic status reliant on a mono cereal maize diet are exposed to fumonisin levels that exceed the provisional maximum tolerable daily intake of 2 mu g kg(-1) body weight day(-1) recommended by the Joint FAO/WHO Expert Committee on Food Additives. In the rural Centane magisterial district, Eastern Cape Province, South Africa, it is customary during food preparation to sort visibly infected maize kernels from good maize kernels and to wash the good kernels prior to cooking. However, this customary practice seems not to sufficiently reduce the fumonisin levels. This is the first study to optimise the reduction of fumonisin mycotoxins in home-grown maize based on customary methods of a rural population, under laboratory-controlled conditions. Maize obtained from subsistence farmers was analysed for the major naturally occurring fumonisins (FB1, FB2 and FB3) by fluorescence HPLC. Large variations were observed in the unsorted and the experimental maize batches attributable to the non-homogeneous distribution of fumonisin contamination in maize kernels. Optimised hand-sorting of maize kernels by removing the visibly infected/damaged kernels (fumonisins, 53.7 +/- 15.0 mg kg(-1), 2.5% by weight) reduced the mean fumonisins from 2.32 +/- 1.16 mg kg(-1) to 0.68 +/- 0.42 mg kg(-1). Hand washing of the sorted good maize kernels for a period of 10 min at 25 degrees C resulted in optimal reduction with no additional improvement for wash periods up to 15 h. The laboratory optimised sorting reduced the fumonisins by 71 +/- 18% and an additional 13 +/- 12% with the 10 min wash. Based on these results and on local practices and practicalities the protocol that would be recommended to subsistence farmers consists of the removal of the infected/damaged kernels from the maize followed by a 10 min ambient temperature water wash. (C) 2010 Elsevier Ltd. All rights reserved.

Mycotoxins and human disease: a largely ignored global health issue

Aflatoxins and fumonisins (FB) are mycotoxins contaminating a large fraction of the world's food, including maize, cereals, groundnuts and tree nuts. The toxins frequently co-occur in maize. Where these commodities are dietary staples, for example, in parts of Africa, Asia and Latin America, the contamination translates to high-level chronic exposure. This is particularly true in subsistence farming communities where regulations to control exposure are either non-existent or practically unenforceable. Aflatoxins are hepatocarcinogenic in humans, particularly in conjunction with chronic hepatitis B virus infection, and cause aflatoxicosis in episodic poisoning outbreaks. In animals, these toxins also impair growth and are immunosuppressive; the latter effects are of increasing interest in human populations. FB have been reported to induce liver and kidney tumours in rodents and are classified as Group 2B 'possibly carcinogenic to humans', with ecological studies implying a possible link to increased oesophageal cancer. Recent studies also suggest that the FB may cause neural tube defects in some maize-consuming populations. There is a plausible mechanism for this effect via a disruption of ceramide synthase and sphingolipid biosynthesis. Notwithstanding the need for a better evidence-base on mycotoxins and human health, supported by better biomarkers of exposure and effect in epidemiological studies, the existing data are sufficient to prioritize exposure reduction in vulnerable populations. For both toxins, there are a number of practical primary and secondary prevention strategies which could be beneficial if the political will and financial investment can be applied to what remains a largely and rather shamefully ignored global health issue.

Reduction in exposure to carcinogenic aflatoxins by postharvest intervention measures in west Africa: a community-based intervention study

Background Aflatoxins are fungal metabolites that frequently contaminate staple foods in much of sub-Saharan Africa, and are associated with increased risk of liver cancer and impaired growth in young children. We aimed to assess whether postharvest measures to restrict aflatoxin contamination of groundnut crops could reduce exposure in west African villages.

Methods We undertook an intervention study at subsistence farms in the lower Kindia region of Guinea. Farms from 20 villages were included, ten of which implemented a package of postharvest measures to restrict aflatoxin contamination of the groundnut crop; ten controls followed usual postharvest practices. We measured the concentrations of blood aflatoxin-albumin adducts from 600 people immediately after harvest and at 3 months and 5 months postharvest to monitor the effectiveness of the intervention.

Findings In control villages mean aflatoxin-albumin concentration increased postharvest (from 5.5 pg/mg [95% CI 4.7-6.1] immediately after harvest to 18.7 pg/mg [17.0-20.6] 5 months later). By contrast, mean aflatoxin-albumin concentration in intervention villages after 5 months of groundnut storage was much the same as that immediately postharvest (7.2 pg/mg [6.2-8.4] vs 8.0 pg/mg [7.0-9.2]). At 5 months, mean adduct concentration in intervention villages was less than 50% of that in control villages (8.0 pg/mg [7.2-9.2] vs 18.7 pg/mg [17.0-20.6], p<0.0001). About a third of the number of people had non-detectable aflatoxin-albumin concentrations at harvest. At 5 months, five (2%) people in the control villages had non-detectable adduct concentrations compared with 47 (20%) of those in the intervention group (p<0.0001). Mean concentrations of aflatoxin B1 in groundnuts in household stores in intervention and control villages were consistent with measurements of aflatoxin-albumin adducts.

Interpretation Use of low-technology approaches at the subsistence-farm level in sub-Saharan Africa could substantially reduce the disease burden caused by aflatoxin exposure.