Higher antioxidant and lower cadmium concentrations and lower incidence of pesticide residues in organically grown crops: a systematic literature review and meta-analyses

In the paper

“Most importantly, the concentrations of a range of antioxidants such as polyphenolics were found to be substantially higher in organic crops/crop-based foods, with those of phenolic acids, flavanones, stilbenes, flavones, flavonols and anthocyanins being an estimated 19 (95 % CI 5, 33) %, 69 (95 % CI 13, 125) %, 28 (95 % CI 12, 44) %, 26 (95 % CI 3, 48) %, 50 (95 % CI 28, 72) % and 51 (95 % CI 17,”

In the paper

“Most importantly, the concentrations of a range of antioxidants such as polyphenolics were found to be substantially higher in organic crops/crop-based foods, with those of phenolic acids, flavanones, stilbenes, flavones, flavonols and anthocyanins being an estimated 19 (95 % CI 5, 33) %, 69 (95 % CI 13, 125) %, 28 (95 % CI 12, 44) %, 26 (95 % CI 3, 48) %, 50 (95 % CI 28, 72) % and 51 (95 % CI 17,”

In the paper

“which also contained significantly higher concentrations of the toxic metal Cd”

In the paper

“Most importantly, the concentrations of a range of antioxidants such as polyphenolics were found to be substantially higher in organic crops/crop-based foods, with those of phenolic acids, flavanones, stilbenes, flavones, flavonols and anthocyanins being an estimated 19 (95 % CI 5, 33) %, 69 (95 % CI 13, 125) %, 28 (95 % CI 12, 44) %, 26 (95 % CI 3, 48) %, 50 (95 % CI 28, 72) % and 51 (95 % CI 17,”

In the paper

“Most importantly, the concentrations of a range of antioxidants such as polyphenolics were found to be substantially higher in organic crops/crop-based foods, with those of phenolic acids, flavanones, stilbenes, flavones, flavonols and anthocyanins being an estimated 19 (95 % CI 5, 33) %, 69 (95 % CI 13, 125) %, 28 (95 % CI 12, 44) %, 26 (95 % CI 3, 48) %, 50 (95 % CI 28, 72) % and 51 (95 % CI 17,”

In the paper

“Most importantly, the concentrations of a range of antioxidants such as polyphenolics were found to be substantially higher in organic crops/crop-based foods, with those of phenolic acids, flavanones, stilbenes, flavones, flavonols and anthocyanins being an estimated 19 (95 % CI 5, 33) %, 69 (95 % CI 13, 125) %, 28 (95 % CI 12, 44) %, 26 (95 % CI 3, 48) %, 50 (95 % CI 28, 72) % and 51 (95 % CI 17,”

In the paper

“In the present study, we carried out meta-analyses based on 343 peer-reviewed publications that indicate statistically significant and meaningful differences in composition between organic and non-organic crops/crop-based foods.”

In the paper

“Additionally, the frequency of occurrence of pesticide residues was found to be four times higher in conventional crops”

In the paper

“Most importantly, the concentrations of a range of antioxidants such as polyphenolics were found to be substantially higher in organic crops/crop-based foods”

In the paper

“Most importantly, the concentrations of a range of antioxidants such as polyphenolics were found to be substantially higher in organic crops/crop-based foods, with those of phenolic acids, flavanones, stilbenes, flavones, flavonols and anthocyanins being an estimated 19 (95 % CI 5, 33) %, 69 (95 % CI 13, 125) %, 28 (95 % CI 12, 44) %, 26 (95 % CI 3, 48) %, 50 (95 % CI 28, 72) % and 51 (95 % CI 17,”

In the paper

“Heterogeneity was extremely high (I 2>75 %) for most of the composition parameters, with I 2 ranging from 76 % for ascorbic acid to 100 % for carotenoids and DM (Fig. 3).”

In the paper

“For most of the minerals (including many plant marco- and micronutrients), the meta-analyses could not detect significant composition differences between organic and conventional crops (see online supplementary Table S12).”

In the paper

“Significantly higher frequencies of occurrence of pesticide residues in conventional crops were also detected when data reported for fruits, vegetables and processed crop-based foods were analysed separately (Fig. 5).”

In the paper

“while only a trend towards a significant difference (P= 0·06) was observed for vegetables”

In the paper

“The MPD for most of the compounds were between 18 and 69 % for most of the above-mentioned antioxidant compounds (Fig. 3).”

In the paper

“The meta-analyses did not detect significant differences for a range of other secondary metabolites with antioxidant activity. These included some individual carotenoids (α-carotene, lycopene, β-cryptoxanthin and zeaxanthin), vitamins (α-tocopherol, γ-tocopherol, vitamin B and vitamin B1), some specific phenolic acids (total hydroxycinnamic acids, caffeic acid, p-coumaric acid, ferulic acid, sinap”

In the paper

“For the toxic metals As and Pb, no significant differences could be detected in their concentrations between organic and conventional crops in the meta-analyses (see online supplementary Table S12).”

In the paper

“When data reported for fruits and vegetables were analysed separately, a significant difference was detected for fruits”

In the paper

“The unweighted meta-analysis also detected significantly higher concentrations of reducing sugars and DM in organic crops (Fig. 4).”

In the paper

“The unweighted meta-analysis also detected significantly higher concentrations of chlorogenic acid (5-O-caffeoylquinic acid) in organic crops (Fig. 3).”

In the paper

“Also, when data reported for carbohydrates in vegetables, fruits and cereals were analysed separately, no significant effects could be detected in their concentrations (Fig. 4).”

In the paper

“although there was no evidence of an interaction”

In the paper

“The standard meta-analyses showed that the frequency of occurrence of detectable pesticide residues was four times higher in conventional crops (46 (95 % CI 38, 55) %) than in organic crops (11 (95 % CI 7, 14) %) (Fig. 5).”

In the paper

“It should be pointed out that (1) there are only eleven studies in which the frequencies of occurrence of pesticide residues were compared, (2) eight of these studies focused on only one crop species, (3) no comparative studies for cereals, oilseeds and pulses were identified in the literature review, and (4) the data available did not allow scientifically robust comparisons of the concentrations”

In the paper

“The concentrations of proteins, amino acids and N (which are known to be positively correlated in plants) were found to be lower in organic crops, and this is consistent with the results of previous studies that have linked lower protein concentrations to lower N inputs and N availability in organic crop production systems( 61 , 62 ).”

In the paper

“It should be pointed out that (1) there are only eleven studies in which the frequencies of occurrence of pesticide residues were compared, (2) eight of these studies focused on only one crop species, (3) no comparative studies for cereals, oilseeds and pulses were identified in the literature review, and (4) the data available did not allow scientifically robust comparisons of the concentrations”

In the paper

“It should be pointed out that (1) there are only eleven studies in which the frequencies of occurrence of pesticide residues were compared, (2) eight of these studies focused on only one crop species, (3) no comparative studies for cereals, oilseeds and pulses were identified in the literature review, and (4) the data available did not allow scientifically robust comparisons of the concentrations”

In the paper

“For many composition parameters, the method of synthesis did not have large effects on results, in terms of both statistical significance and the magnitude of relative difference between organic and conventional crops.”

In the paper

“However, due to the lack of detailed information on agronomic and pedo-climatic background conditions in most of the available literature, it is currently not possible to quantify the relative contribution of genetic and environmental/agronomic sources of variation.”

In the paper

“The present study also identified variation between studies (1) carried out in countries with different pedo-climatic conditions and agronomic protocols (e.g. rotation designs, irrigated or non-irrigated crop production, and level and type of animal manures used) and/or (2) focused on different crop species.”

In the paper

“The on average 48 % lower Cd concentrations found in organic crops/crop-based foods in the meta-analyses carried out in the present study are therefore desirable, although the exact health benefits associated with reducing Cd intake levels via a switch to organic food consumption are difficult to estimate.”

In the paper

“The present study demonstrated that the prohibition of synthetic chemical pesticide use under organic farming standards results in a more than 4-fold reduction in the number of crop samples with detectable pesticide residues.”

In the paper

“It should be pointed out that (1) there are only eleven studies in which the frequencies of occurrence of pesticide residues were compared, (2) eight of these studies focused on only one crop species, (3) no comparative studies for cereals, oilseeds and pulses were identified in the literature review, and (4) the data available did not allow scientifically robust comparisons of the concentrations”

In the paper

“As has been mentioned in previous reviews( 19 – 21 ), pooling diverse information was necessary, because for most of the composition parameters, the number of published studies available was not sufficient to carry out separate meta-analyses for specific countries/regions and crop types and species.”

What the sources say

• Not checked yetcites [19] Dangour AD, Dodhia SK, Hayter A, et al. (2009) Nutritional quality of organic foods: a systematic review. Am J Clin Nutr 90, 680– 685 19640946 source
• Not checked yetcites [20] Brandt K, Leifert C, Sanderson R, et al. (2011) Agroecosystem management and nutritional quality of plant foods: the case of organic fruits and vegetables. Crit Rev Plant Sci 30, 177– 197 source
• Not checked yetcites [21] Smith-Spangler C, Brandeau ML, Hunter GE, et al. (2012) Are organic foods safer or healthier than conventional alternatives? A systematic review. Ann Intern Med 157, 348– 366 22944875 source

In the paper

“Consequently, heterogeneity was extremely high (I 2>75 %) for most of the composition parameters for which significant differences were detected.”

In the paper

“The considerably higher frequency of occurrence of detectable residues in conventional fruits (75 %) than in vegetables (32 %) may indicate higher levels of crop protection inputs being used in fruit crops, but could also have been due to the use of more persistent chemicals, different sprayer technologies used and/or pesticide applications being made closer to harvest.”

In the paper

“For other composition parameters (e.g. ferric reducing antioxidant power, oxygen radical absorbance capacity, Trolox equivalent antioxidant capacity, and levels of flavonoids, stilbenes, total carotenoids, l-ascorbic acid, proteins, and Cd), differences in methods had a large impact in terms of both significant effects being detected and/or estimates of the magnitude of difference based on MPD and”

In the paper

“Not all studies included in the meta-analyses used certified reference materials as a quality assurance measure for the accuracy of estimates of concentrations of compounds in crops.”

In the paper

“Also, in many studies, there was a lack of detailed information on (1) the geographical origin of samples in retail surveys and (2) agronomic (e.g. rotation, fertilisation, tillage and irrigation regimens), pedo-climatic and crop genetic backgrounds (in farm surveys and field experiments), which would allow potential sources of variation to be investigated.”

In the paper

“However, there is increasing evidence and more widespread acceptance that the consumption of organic foods is likely to reduce exposure to pesticide residues( 21 , 23 , 24 ).”

What the sources say

• Not checked yetcites [21] Smith-Spangler C, Brandeau ML, Hunter GE, et al. (2012) Are organic foods safer or healthier than conventional alternatives? A systematic review. Ann Intern Med 157, 348– 366 22944875 source
• Not checked yetcites [23] Curl C, Fenske RA & Elgethun K (2003) Organophosphorus pesticide exposure of urban and suburban preschool children with organic and conventional diets. Environ Health Perspect 111, 377– 382 12611667 PMC1241395 source
• Not checked yetcites [24] Leifert C, Ball K, Volakakis N, et al. (2008) Control of enteric pathogens in ready-to-eat vegetable crops in organic and ‘low input’ production systems: a HACCP-based approach. J Appl Microbiol 105, 931– 950 18397255 source

In the paper

“Many of these compounds have previously been linked to a reduced risk of chronic diseases, including CVD and neurodegenerative diseases and certain cancers, in dietary intervention and epidemiological studies.”

• Also stated in: § Abstract · boosted

  “There is particular interest in antioxidant activity/concentrations, as there is strong scientific evidence for health benefits associated with increased consumption of crops rich in (poly)phenolics and other plant secondary metabolites with antioxidant activity (e.g. carotenoids and vitamins C and E)( 16 – 18 ).”

What the sources say

• Not checked yetcites [16] Del Rio D, Rodriguez-Mateos A, Spencer JPE, et al. (2013) Dietary (poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid Redox Signal 18, 1818– 1892 22794138 PMC3619154 source
• Not checked yetcites [17] Wahlqvist ML (2013) Antioxidant relevance to human health. Asia Pac J Clin Nutr 22, 171– 176 23635359 source
• Not checked yetcites [18] Fardet A (2010) New hypotheses for the health-protective mechanisms of whole-grain cereals: what is beyond fibre? Nutr Res Rev 23, 65– 134 20565994 source

In the paper

“there were some statistically significant interactions between fertilisation and crop protection protocols with respect to gene and protein expression pattern”

What the sources say

• Not checked yetcites [10] Rempelos L, Cooper J, Wilcockson S, et al. (2013) Quantitative proteomics to study the response of potato to contrasting fertilisation regimes. Mol Breed 31, 363– 378 source
• Not checked yetcites [11] Lehesranta SJ, Koistinen KM, Massat N, et al. (2007) Effects of agricultural production systems and their components on protein profiles of potato tubers. Proteomics 7, 597– 604 17309105 source
• Not checked yetcites [12] Tetard-Jones C, Shotton PN, Rempelos L, et al. (2013) Quantitative proteomics to study the response of wheat to contrasting fertilisation regimes. Mol Breed 31, 379– 393 source
• Not checked yetcites [13] van Dijk JP, Cankar K, Scheffer SJ, et al. (2009) Transcriptome analysis of potato tubers – effects of different agricultural practices. J Agric Food Chem 57, 1612– 1623 19173602 source
• Not checked yetcites [14] van Dijk JP, Leifert C, Barros E, et al. (2010) Gene expression profiling for food safety assessment: examples in potato and maize. Regul Toxicol Pharmacol 58, Suppl. 3, S21– S25 20600454 source
• Not checked yetcites [15] van Dijk JP, Cankar K, Hendriksen PJM, et al. (2012) The identification and interpretation of differences in the transcriptomes of organically and conventionally grown potato tubers. J Agric Food Chem 60, 2090– 2101 22300527 source

In the paper

“Such large differences can be considered biologically implausible, and these ‘outlier’ data pairs were therefore omitted from the final standard meta-analyses”

In the paper

“Also, a switch from pesticide-based conventional to organic crop protection protocols has been shown to have a significant, but more limited effect than fertilisation regimens”

What the sources say

• Not checked yetcites [10] Rempelos L, Cooper J, Wilcockson S, et al. (2013) Quantitative proteomics to study the response of potato to contrasting fertilisation regimes. Mol Breed 31, 363– 378 source
• Not checked yetcites [11] Lehesranta SJ, Koistinen KM, Massat N, et al. (2007) Effects of agricultural production systems and their components on protein profiles of potato tubers. Proteomics 7, 597– 604 17309105 source
• Not checked yetcites [12] Tetard-Jones C, Shotton PN, Rempelos L, et al. (2013) Quantitative proteomics to study the response of wheat to contrasting fertilisation regimes. Mol Breed 31, 379– 393 source
• Not checked yetcites [13] van Dijk JP, Cankar K, Scheffer SJ, et al. (2009) Transcriptome analysis of potato tubers – effects of different agricultural practices. J Agric Food Chem 57, 1612– 1623 19173602 source
• Not checked yetcites [14] van Dijk JP, Leifert C, Barros E, et al. (2010) Gene expression profiling for food safety assessment: examples in potato and maize. Regul Toxicol Pharmacol 58, Suppl. 3, S21– S25 20600454 source
• Not checked yetcites [15] van Dijk JP, Cankar K, Hendriksen PJM, et al. (2012) The identification and interpretation of differences in the transcriptomes of organically and conventionally grown potato tubers. J Agric Food Chem 60, 2090– 2101 22300527 source

In the paper

“The finding of a four times higher frequency of occurrence of pesticide residues in conventional crops confirms the results of the study of Smith-Spangler et al. ( 21 ), in which a very similar set of studies (nine of the ten publications used in the present study) were used for analysis.”

What the sources say

• Not checked yetcites [21] Smith-Spangler C, Brandeau ML, Hunter GE, et al. (2012) Are organic foods safer or healthier than conventional alternatives? A systematic review. Ann Intern Med 157, 348– 366 22944875 source

In the paper

“The main reason for the inability of previous studies to detect composition differences was probably the highly limited number of studies/data sets available or included in analyses by these authors, which would have decreased the statistical power of the meta-analyses.”

In the paper

“This suggests that a switch from conventional to organic crop consumption may have impacts similar to those of an increase in the intake of foods with high antioxidant/(poly)phenolic contents.”

In the paper

“In contrast, there is increasing evidence that differences in fertilisation regimens between organic and conventional production systems (and, in particular, the non-use of high mineral N fertiliser inputs) are significant drivers for higher (poly)phenolic concentrations in organic crops( 20 , 49 – 52 ).”

What the sources say

• Not checked yetcites [20] Brandt K, Leifert C, Sanderson R, et al. (2011) Agroecosystem management and nutritional quality of plant foods: the case of organic fruits and vegetables. Crit Rev Plant Sci 30, 177– 197 source
• Not checked yetcites [49] Almuayrifi M (2013) Effect of fertilisation, crop protection, pre-crop and variety choice on yield of phenols content diseases severity and yield of winter wheat. PhD Thesis, Newcastle University.
• Not checked yetcites [50] Sander JF & Heitefuss R (1998) Susceptibility to Erysiphe graminis f. sp. tritici and phenolic acid content of wheat as influenced by different levels of nitrogen fertilization. J Phytopathol 146, 495– 507 source
• Not checked yetcites [51] Rühmann S, Leser C, Bannert M, et al. (2002) Relationship between growth, secondary metabolism, and resistance of apple. Plant Biol 4, 137– 143 source
• Not checked yetcites [52] Stewart AJ, Chapman W, Jenkins GI, et al. (2001) The effect of nitrogen and phosphorus deficiency on flavonol accumulation in plant tissues. Plant Cell Environ 24, 1189– 1197 source

In the paper

“Many of the antioxidants, including (poly)phenolics, found in higher concentrations in organic crops are known to be produced by plants in response to abiotic (e.g. wounding and heat, water and nutrient stress) and biotic (pest attacks and disease) stress and form part of the plants' constitutive and inducible resistance mechanisms to pests and diseases( 47 – 49 ).”

What the sources say

• Not checked yetcites [47] Nicholson RL & Hammerschmidt R (1992) Phenolic compounds and their role in disease resistance. Annu Rev Phytopathol 30, 369– 389 source
• Not checked yetcites [48] Bennett RN & Wallsgrove RM (1994) Secondary metabolites in plant defense mechanisms. New Phytol 127, 617– 633 33874382 source
• Not checked yetcites [49] Almuayrifi M (2013) Effect of fertilisation, crop protection, pre-crop and variety choice on yield of phenols content diseases severity and yield of winter wheat. PhD Thesis, Newcastle University.

In the paper

“For plant secondary metabolites, this confirms the results of the meta-analyses carried out by Brandt et al. ( 20 ), which indicated that there are significant composition differences between organic and conventional crops for a range of nutritionally relevant compounds.”

What the sources say

• Not checked yetcites [20] Brandt K, Leifert C, Sanderson R, et al. (2011) Agroecosystem management and nutritional quality of plant foods: the case of organic fruits and vegetables. Crit Rev Plant Sci 30, 177– 197 source

In the paper

“This estimated magnitude of difference would be equivalent to the amount of antioxidants/(poly)phenolics present in one to two of the five portions of fruits and vegetables recommended to be consumed daily and would therefore be significant/meaningful in terms of human nutrition, if information linking these plant secondary metabolites to the health benefits associated with increased fruit,”

What the sources say

• Not checked yetcites [16] Del Rio D, Rodriguez-Mateos A, Spencer JPE, et al. (2013) Dietary (poly)phenolics in human health: structures, bioavailability, and evidence of protective effects against chronic diseases. Antioxid Redox Signal 18, 1818– 1892 22794138 PMC3619154 source
• Not checked yetcites [17] Wahlqvist ML (2013) Antioxidant relevance to human health. Asia Pac J Clin Nutr 22, 171– 176 23635359 source
• Not checked yetcites [18] Fardet A (2010) New hypotheses for the health-protective mechanisms of whole-grain cereals: what is beyond fibre? Nutr Res Rev 23, 65– 134 20565994 source

In the paper

“Strong or moderate funnel plot asymmetry consistent with a publication bias was detected for approximately half of the parameters.”

In the paper

“However, there are several animal dietary intervention studies that have identified significant associations between organic feed consumption and animal growth and physiological (including immune and endocrine) parameters and/or biomarkers of health when compared with conventional feed consumption( 44 , 45 ).”

What the sources say

• Not checked yetcites [44] Huber M, van de Vijver LPL, Parmentier H, et al. (2010) Effects of organically and conventionally produced feed on biomarkers of health in a chicken model. Br J Nutr 103, 663– 676 19860984 source
• Not checked yetcites [45] Lauridsen C, Yong C, Halekoh U, et al. (2008) Rats show differences in some biomarkers of health when eating diets based on ingredients produced with three different cultivation strategies. J Sci Food Agric 88, 720– 732 source

In the paper

“Redundancy analysis identified total polyphenol concentrations in feeds as the strongest driver for the physiological/endocrinological parameters assessed in rats.”

What the sources say

• Not checked yetcites [46] Srednicka-Tober D, Baranski M, Gromadzka-Ostrowska J, et al. (2013) Effect of crop protection and fertilization regimes used in organic and conventional production systems on feed composition and physiological parameters in rats. J Agric Food Chem 61, 1017– 1029 23323826 source

In the paper

“However, it contradicts the results of the systematic reviews/meta-analyses by Dangour et al. ( 19 ) and Smith-Spangler et al. ( 21 ), which indicated that there are no significant composition differences between organic and conventional crops.”

What the sources say

• Not checked yetcites [19] Dangour AD, Dodhia SK, Hayter A, et al. (2009) Nutritional quality of organic foods: a systematic review. Am J Clin Nutr 90, 680– 685 19640946 source
• Not checked yetcites [21] Smith-Spangler C, Brandeau ML, Hunter GE, et al. (2012) Are organic foods safer or healthier than conventional alternatives? A systematic review. Ann Intern Med 157, 348– 366 22944875 source

In the paper

“The finding in the present study that organic crops have significantly lower N, and concentrations would support the theory that differences in antioxidant/(poly)phenolic concentrations between organic and conventional crops are driven by contrasting N supply patterns.”

In the paper

“However, a significant number of crop samples included in the regulatory European Food Safety Authority pesticide residue monitoring in Europe are still found to contain pesticide residues above the MRL( 57 ).”

What the sources say

• Not checked yetcites [57] European Food Safety Authority (2011) The 2009 European Union report on pesticide residues in food. EFSA 9, 2430 source

In the paper

“A range of other soil (e.g. pH) and agronomic (e.g. liming) factors are known to affect Cd concentrations in crops( 54 ), and these may explain the variability in results between individual comparative studies, crop species and crop types (see Fig. 4 and online supplementary Figs. S4 and S22).”

In the paper

“in antioxidant/(poly)phenolic concentrations between organic and conventional crops are driven by contrasting N supply patterns. This view is supported by previous studies that have suggested that under high N availability, plants allocate carbohydrates from photosynthesis to primary metabolism and rapid growth while producing less amounts of secondary metabolites involved in defence( 51 ).”

What the sources say

• Not checked yetcites [51] Rühmann S, Leser C, Bannert M, et al. (2002) Relationship between growth, secondary metabolism, and resistance of apple. Plant Biol 4, 137– 143 source

In the paper

“One of the main challenges to interpreting comparisons of organic and inorganic food production systems is the high heterogeneity arising from combinations of (1) crops, crop types and/or crop-based foods, (2) countries, and/or (3) pedo-climatic and agronomic background conditions.”

In the paper

“This indicates that there is now a sufficiently large body of published information to identify differences that are relatively consistent across study types, crops, and pedo-climatic and agronomic environments.”

In the paper

“However, data from studies that did not use reference materials are less reliable when used to estimate the concentrations of nutritionally relevant compounds in crops and total dietary intake levels of such compounds in crop-based foods.”

In the paper

“This is unlikely to have affected the estimates of relative differences between organic and conventional crops, as the same extraction and analytical methods were used for organic and conventional samples in all the studies included in the meta-analyses in the present study.”

In the paper

“There is little uncertainty surrounding this overall result, but further research is required to quantify more accurately the relative impacts of (1) crop types, species, and varieties/cultivars/hybrids and (2) agronomic and pedo-climatic background conditions on the relative difference between organic and conventional crop composition.”