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. 2019 Mar 18;48(5):1519–1535. doi: 10.1093/ije/dyz017

Table 2.

Ever use of 14 pesticide chemical groups and 33 active ingredients and meta-risk estimates, fully adjusted, of non-Hodgkin lymphoid malignancies diagnosed during follow-up in farmers and farm workers in three cohort studies from France, Norway and the USA

Non-Hodgkin lymphoid malignancies (NHL)
Chronic lymphocytic leukaemia/small lymphocytic lymphoma (CLL/SLL)
Diffuse large B-cell lymphoma (DLBCL)
N a HRb 95% CI I2 P e N a HRb 95% CI I2 P e N a HRb 95% CI I2 P e
OP Insecticides 1417 0.90 (0.75–1.09) 0% 0.56 318 1.03 (0.64–1.65) 0% 0.65 256 0.90 (0.58–1.39) 0% 0.71
 Chlorpyrifos 453 0.99d (0.86–1.15) 0% 0.51 106 1.05d (0.77–1.42) 0% 0.84 86 0.99d (0.72–1.36) 0% 0.76
 Dichlorvos 523 1.10 (0.95–1.27) 0% 0.72 116 1.07 (0.78–1.46) 0% 0.39 81 0.94 (0.67–1.32) 0% 0.84
 Malathion 1208 0.98 (0.82–1.16) 0% 0.54 274 1.11 (0.76–1.64) 0% 0.89 209 0.84 (0.58–1.21) 0% 0.86
 Parathion 995 0.95 (0.81–1.11) 0% 0.58 210 0.99 (0.70–1.40) 0% 0.93 162 0.91 (0.63–1.31) 0% 0.92
 Terbufos 300 1.18d (1.00–1.39) 0% 0.53 76 1.28d (0.92–1.79) 0% 1.00 56 1.08d (0.74–1.57) 0% 0.57
Carbamate insecticides 1254 0.94 (0.81–1.08) 0% 0.97 283 1.06 (0.75–1.48) 0% 1.00 219 0.79 (0.56–1.11) 0% 0.77
 Aldicarb 526 1.09 (0.95–1.26) 0% 0.67 116 1.16 (0.84–1.60) 0% 0.93 82 0.88 (0.63–1.24) 0% 0.91
 Carbaryl 651 0.95 (0.83–1.10) 0% 0.52 148 0.97 (0.71–1.34) 0% 0.67 125 0.87 (0.64–1.19) 0% 0.96
 Carbofuran 254 1.00d (0.84–1.20) 0% 0.59 63 1.08d (0.75–1.56) 0% 0.40 44 0.84d (0.55–1.27) 0% 0.92
 Pirimicarb 796 0.90c (0.74–1.08) 0% 0.95 176 1.18c (0.77–1.82) 0% 0.51 123 0.71c (0.44–1.14) 0% 0.64
OC insecticides 1258 0.86 (0.74–0.99) 0% 0.77 288 1.08 (0.79–1.48) 0% 0.83 215 0.79 (0.52–1.20) 35% 0.21
 DDT 976 0.92 (0.81–1.04) 0% 0.71 220 1.00 (0.77–1.31) 0% 0.75 165 0.85 (0.63–1.14) 0% 0.74
 Lindane 953 0.89 (0.78–1.01) 0% 0.87 217 1.06 (0.79–1.41) 0% 0.60 160 0.94 (0.68–1.30) 0% 0.47
Pyrethroid insecticides 934 1.04 (0.90–1.19) 2% 0.36 211 1.29 (0.90–1.84) 15% 0.31 153 0.92 (0.66–1.28) 0% 0.72
 Deltamethrin 627 1.04c (0.82–1.33) 59% 0.12 148 1.48c (1.06–2.07) 0% 0.35 99 0.96c (0.68–1.37) 0% 0.64
 Esfenvalerate 549 1.15 (0.82–1.63) 69% 0.04 124 1.24c (0.79–1.94) 36% 0.21 89 1.03c (0.71–1.50) 0% 0.93
 Permethrin 812 1.01 (0.87–1.19) 0% 0.97 182 1.30 (0.85–2.00) 25% 0.26 131 0.89 (0.61–1.29) 0% 0.96
(Phenyl) urea herbicides 979 1.03 (0.89–1.19) 0% 0.48 209 1.07 (0.75–1.51) 0% 0.97 156 0.86 (0.61–1.21) 0% 0.87
 Isoproturon 453 1.03c (0.78–1.35) 55% 0.14 109 1.19c (0.79–1.78) 0% 0.54 73 0.82c (0.49–1.38) 21% 0.26
 Linuron 961 1.06 (0.90–1.24) 0% 0.46 204 1.05 (0.73–1.49) 0% 0.92 155 0.94 (0.67–1.33) 0% 0.88
Dicamba 815 1.04 (0.90–1.19) 10% 0.33 180 1.05 (0.80–1.38) 0% 0.83 142 0.95 (0.70–1.29) 0% 0.44
Chloroacetanilides 735 1.00 (0.87–1.14) 0% 0.79 161 0.96 (0.68–1.35) 21% 0.28 145 1.08 (0.79–1.47) 0% 0.68
 Alachlor 380 0.97d (0.81–1.15) 0% 0.45 85 0.92d (0.43–1.96) 68% 0.07 74 0.87d (0.60–1.24) 0% 0.87
 Metolachlor 358 0.99d (0.84–1.17) 0% 0.57 88 1.02d (0.72–1.43) 0% 0.45 71 0.95d (0.64–1.42) 0% 0.86
Dinitroaniline herbicides 506 0.94d (0.78–1.12) 0% 0.34 126 1.07d (0.74–1.56) 0% 0.42 101 0.91d (0.62–1.31) 0% 0.88
 Trifluralin 368 0.98d (0.72–1.33) 64% 0.10 90 0.92d (0.60–1.41) 15% 0.28 72 0.90d (0.62–1.32) 0% 0.66
Glyphosate 1131 0.95 (0.77–1.18) 57% 0.10 252 0.92 (0.69–1.24) 0% 0.38 221 1.36 (1.00–1.85) 0% 0.48
Phenoxy herbicides 1204 0.81 (0.67–0.98) 19% 0.29 272 0.89 (0.61–1.31) 0% 0.79 218 0.70 (0.32–1.52) 59% 0.09
 2, 4-D 1167 0.88 (0.75–1.04) 0% 0.87 262 0.92 (0.61–1.39) 19% 0.29 212 0.77 (0.46–1.30) 47% 0.15
 MCPA 775 0.81c (0.53–1.23) 65% 0.09 163 0.98c (0.54–1.77) 0% 0.83 125
 MCPP 776 0.94 (0.61–1.46) 65% 0.06 163 1.06c (0.57–1.98) 0% 0.63 124
Thiocarbamate herbicides 1015 0.93 (0.80–1.08) 0% 0.69 225 0.95 (0.63–1.45) 34% 0.22 171 0.88 (0.61–1.25) 0% 0.88
 Butylate 265 1.01d (0.85–1.19) 0% 0.52 60 0.96d (0.50–1.85) 56% 0.13 48 0.89d (0.61–1.32) 0% 0.92
 EPTC 606 1.04 (0.91–1.19) 0% 0.74 133 1.10 (0.76–1.60) 35% 0.21 101 1.12 (0.81–1.56) 0% 0.69
Triazine herbicides 1165 0.87 (0.74–1.02) 8% 0.34 269 0.85 (0.60–1.20) 0% 0.72 212 0.84 (0.60–1.18) 0% 0.40
 Atrazine 546 0.97d (0.79–1.18) 0% 0.99 131 0.96d (0.62–1.49) 0% 0.35 109 0.88d (0.59–1.31) 0% 0.54
 Simazine 303 0.92 (0.77–1.09) 0% 0.43 63 0.83 (0.53–1.31) 6% 0.35 54 0.91 (0.61–1.36) 0% 0.65
Triazinone herbicides 971 1.09 (0.85–1.40) 60% 0.08 215 1.22 (0.84–1.77) 21% 0.28 157 1.00 (0.73–1.36) 0% 0.67
 Metribuzin 971 1.09 (0.85–1.40) 60% 0.08 215 1.22 (0.84–1.77) 21% 0.28 157 1.00 (0.73–1.36) 0% 0.67
Dithiocarbamate fungicides 961 0.96 (0.83–1.11) 0% 0.96 196 0.86 (0.62–1.19) 0% 0.72 157 0.93 (0.66–1.31) 0% 0.60
 Mancozeb 932 0.94 (0.81–1.09) 0% 0.85 193 0.90 (0.64–1.26) 0% 0.66 149 0.87 (0.62–1.21) 0% 0.87
 Thiram 264 0.89c (0.73–1.07) 0% 0.35 54 0.82c (0.40–1.66) 50% 0.16 42 0.79c (0.50–1.25) 0% 0.54
Phthalimide fungicides 921 1.10 (0.80–1.52) 57% 0.10 193 1.13 (0.74–1.72) 0% 0.47 144 0.98 (0.65–1.47) 0% 0.94
 Captafol 800 1.12c (0.79–1.59) 69% 0.07 162 1.20c (0.71–2.03) 23% 0.25 121 0.93c (0.62–1.41) 0% 0.44
 Captan 481 0.90 (0.74–1.10) 0% 0.45 107 0.92 (0.59–1.44) 13% 0.32 74 0.83 (0.52–1.33) 0% 0.68
Arsenicals 272
0.97d

(0.79–1.18)

0%

0.71
60 1.04d (0.66–1.63) 0% 0.49 52 1.19d (0.73–1.95)
0%

0.64


Follicular lymphoma (FL)
Multiple myeloma/plasma-cell leukaemia (MM)
N a HRb 95% CI I2 P e N a HRb 95% CI I2 P e
OP insecticides 131 0.78 (0.34–1.76) 2% 0.36 313 0.85 (0.56–1.29) 0% 0.83
 Chlorpyrifos 46 1.08d (0.68–1.70) 0% 0.58 97 0.93d (0.66–1.32) 0% 0.73
 Dichlorvos 40 1.10 (0.69–1.76) 0% 0.95 111 0.98 (0.70–1.37) 22% 0.28
 Malathion 114 1.18 (0.66–2.10) 0% 0.64 269 0.95 (0.67–1.36) 0% 0.69
 Parathion 83 1.24 (0.72–2.15) 0% 0.44 230 0.84 (0.57–1.24) 18% 0.30
 Terbufos 35 1.33d (0.80–2.20) 0% 0.70 55 1.01d (0.69–1.49) 0% 0.64
Carbamate insecticides 115 1.03 (0.63–1.68) 0% 0.47 290 1.25 (0.89–1.75) 9% 0.33
 Aldicarb 38 0.94 (0.56–1.56) 0% 0.79 113 0.91 (0.68–1.22) 0% 0.58
 Carbaryl 67 1.27d (0.66–2.43) 27% 0.24 152 1.11 (0.71–1.74) 47% 0.15
 Carbofuran 26 0.91d (0.52–1.59) 0% 0.94 57 1.21d (0.83–1.78) 0% 0.70
 Pirimicarb 58 0.84c (0.41–1.71) 0% 0.96 185 1.01c (0.70–1.46) 0% 0.68
OC insecticides 114 0.87 (0.54–1.40) 0% 0.82 290 1.03 (0.76–1.40) 0% 0.97
 DDT 79 0.78 (0.45–1.37) 38% 0.20 230 0.96 (0.74–1.25) 0% 0.86
 Lindane 78 0.92 (0.61–1.38) 0% 0.57 216 0.97 (0.74–1.28) 0% 0.89
Pyrethroid insecticides 81 1.16 (0.75–1.79) 0% 0.87 210 1.07 (0.79–1.46) 0% 0.72
 Deltamethrin 46 1.09c (0.64–1.87) 0% 0.77 135 0.93c (0.69–1.24) 0% 0.97
 Esfenvalerate 41 1.04c (0.61–1.75) 0% 0.44 120 1.65 (0.61–4.41) 89% 0.00
 Permethrin 60 0.79 (0.42–1.50) 26% 0.26 187 1.18 (0.86–1.63) 0% 0.61
(Phenyl) urea herbicides 81 1.09 (0.65–1.82) 0% 0.84 227 1.08 (0.79–1.47) 0% 0.65
 Isoproturon 28 0.70c (0.36–1.36) 0% 0.90 100 1.04c (0.72–1.52) 0% 0.78
 Linuron 79 1.11 (0.66–1.87) 0% 0.76 224 1.13 (0.81–1.57) 0% 0.78
Dicamba 73 0.81 (0.53–1.23) 0% 0.63 179 1.21 (0.93–1.59) 0% 0.92
Chloroacetanilides 78 1.00 (0.63–1.58) 0% 0.92 147 0.94 (0.71–1.25) 0% 0.88
 Alachlor 43 0.86d (0.47–1.56) 0% 0.96 78 1.06d (0.73–1.54) 0% 0.94
 Metolachlor 43 1.05d (0.59–1.86) 0% 0.90 71 1.05d (0.71–1.53) 0% 0.71
Dinitroaniline herbicides 57 0.99d (0.56–1.74) 0% 0.71 95 0.82d (0.42–1.61) 69% 0.07
 Trifluralin 39 0.80d (0.47–1.35) 0% 0.66 70 0.89d (0.60–1.32) 0% 0.44
Glyphosate 105 0.79 (0.52–1.21) 0% 0.56 240 0.87 (0.66–1.15) 0% 0.95
Phenoxy herbicides 115 1.02 (0.60–1.75) 0% 0.95 257 0.77 (0.49–1.22) 43% 0.18
 2, 4-D 113 1.14 (0.67–1.96) 0% 0.91 250 0.90 (0.65–1.26) 0% 0.53
 MCPA 60 1.21c (0.53–2.80) 6% 0.30 174 0.69c (0.29–1.64) 64% 0.10
 MCPP 59 0.96c (0.25–3.61) 58% 0.13 175 0.82c (0.25–2.67) 82% 0.02
Thiocarbamate herbicides 88 0.81 (0.52–1.26) 0% 0.68 225 0.99 (0.73–1.34) 0% 0.80
 Butylate 31 1.06d (0.63–1.77) 0% 0.94 54 1.04d (0.70–1.53) 0% 0.69
 EPTC 49 0.86 (0.42–1.73) 51% 0.13 138 1.19 (0.90–1.59) 0% 0.87
Triazine herbicides 115 1.45 (0.62–3.39) 56% 0.10 246 0.82 (0.50–1.35) 56% 0.10
 Atrazine 65 1.28d (0.69–2.38) 0% 0.79 108 0.98d (0.62–1.55) 0% 0.54
 Simazine 23 0.91 (0.48–1.70) 0% 0.88 66 0.83 (0.52–1.32) 35% 0.22
Triazinone herbicides 86 0.85 (0.54–1.36) 0% 0.41 221 1.20 (0.73–1.97) 51% 0.13
 Metribuzin 86 0.86 (0.54–1.36) 0% 0.41 221 1.20 (0.74–1.97) 51% 0.13
Dithiocarbamate fungicides 75 0.88 (0.52–1.49) 0% 0.98 229 1.11 (0.80–1.52) 0% 0.74
 Mancozeb 71 0.80 (0.46–1.39) 0% 0.90 222 1.07 (0.78–1.48) 0% 0.64
 Thiram 17 0.84c (0.40–1.79) 0% 0.72 58 0.80c (0.40–1.61) 60% 0.12
Phthalimide fungicides 71 0.73d (0.37–1.44) 0% 0.84 216 1.05 (0.71–1.54) 0% 0.81
 Captafol 62 1.11c (0.51–2.42) 10% 0.29 192 1.13c (0.76–1.68) 0% 0.45
 Captan 36 0.90 (0.47–1.72) 0% 0.59 97 0.73 (0.39–1.37) 48% 0.15
Arsenicals 17 65 0.91d (0.59–1.40) 0% 0.84

AGRICAN: Cox regression adjusted for: sex, livestock, retirement status, number of selected types of crops for which pesticide treatment personally applied.

CNAP: Cox regression adjusted for: sex, livestock, dichlorvos, aldicarb, lindane, DDT, deltametrin, mancozeb, linuron, glyphosate.

AHS: Cox regression adjusted for: sex, state, livestock, terbufos, lindane, DDT, permethrin, dicamba, parathion, carbaryl.

mHR estimates for DLBCL in association with MCPA and MCPP not available because statistical models did not converge.

mHR estimate for FL in association with arsenicals not available because an estimate could be computed in only one (AGRICAN) of three cohorts. OC, organochlorine; OP, organophosphate; I2 (I-squared, variation in meta-estimate attributable to heterogeneity).

aNumber of cancer cases.

bHazard ratio: random effects meta-analysis (fully adjusted models).

cMeta-analysis based on AGRICAN and CNAP only. For esfenvalerate, AHS contributed to mHR of NHL and multiple myeloma.

dMeta-analysis based on AGRICAN and AHS only.

e P-value for heterogeneity.