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. 2021 Sep 5;13(17):4477. doi: 10.3390/cancers13174477

Table 1.

Summary of studies included in meta-analysis of farming and brain cancer.

First Author Publication Year Source of Article Region (Location) Study Type Study Population Type of Farmer Subcohort with Higher Exposure Number of Exposed Brain Cancer Cases or Deaths Measure of Association Brain Cancer Risk Estimate (95% CI) Risk Estimate among More Highly Exposed Sucohort (95% CI) All-Cancer Risk Estimate (95% CI)
Alberghini [40] 1991 Khuder Europe
(Italy)
Cohort deaths among 4580 male farmers licensed to buy and use pesticides in the Emilia Romagna region of Italy during 1974–1987; both regional and national populations were used as a reference crop no 11 SMR 1.39 (0.69, 2.46) - 0.68 (0.60,0.78)
Blair [41] 1993 Khuder US (multiple states) PMR deaths in 23 US states during 1984–1988 among farmers (n = 135,560) compared with non-farmers mixed no 473 PMR 1.14 (1.04, 1.24) - 0.87 (0.81,0.93)
Brownson [34] 1990 Khuder US
(Missouri)
Case-control 312 histologically confirmed brain and other CNS cancer cases and 1248 frequency-matched controls (patients with other cancers) in white males from the Missouri Cancer Registry during January 1984–1988 not specified no 21 OR 1.10 (0.60, 1.70) - -
Burmeister [42] 1981 Khuder US (Iowa) Cohort 121,101 deaths among white males aged >20 in Iowa during 1971–1978; Iowa population was used as a reference not specified no 111 SMR 1.13 (0.66, 1.82) - 1.12;
p < 0.01
Cerhan [43] 1998 Pubmed US (Iowa) PMR 88,090 deaths among white males 20 years or older in Iowa during 1987–1993; deaths among farmers (n = 5552) were compared to those among non-farmers (n = 82,538) not specified age 65+ (assumed longer exposure) 117 PMR 1.10 (0.92, 1.32) 1.09
(0.88, 1.36)
0.92
(0.90, 0.94)
Corrao [44] 1989 Acquavella Europe (Piedmont, Italy) Cohort hospitalizations for a malignant neoplasm among 25,945 male farmers licensed to purchase and use pesticides between 1970 and 1974 crop cluster of villages with the greatest arable land 25 SIR 1.0 (0.6, 1.4) 0.7
(0.3, 1.3)
0.7
(0.6, 0.8)
Dean [45] 1994 Khuder Europe (Ireland) Cohort deaths caused by brain cancers among farmers in Ireland between 1971 and 1987; the general population was used as a reference not specified no 240 SMR 0.91 (0.62, 0.98) - -
Decoufle [46] 1977 Acquavella US (New York) Case-control 25,416 cancer patients admitted to a cancer treatment center in New York between 1956 and 1965 and non-cancer patients mixed no 2 OR 6.53 (0.57, 74.24) - -
Delzell [10] 1985 Khuder US (North Carolina) PMR 74,041 deaths among black and white male residents of North Carolina during 1976–1978 aged ≥15 years livestock, crop level of agricultural activity (non-whites only); age at death ≥65 years 27 SMR 1.21 (0.38, 3.88) 0.91
(0.34, 2.48)
0.90
(0.81, 1.0)
Demers [47] 1991 Khuder US (Washington) Case-control (cancer deaths) white males aged 20 years and older who died in Washington state between 1969 and 1971 from a brain tumor (n = 904) and from a cause other than brain cancer, CNS tumor, or leukemia (n = 904) as identified from death certificates not specified farmers and farm managers 63 OR 1.05 (0.75, 1.47) 1.0
(0.7, 1.6)
-
Faustini [48] 1993 Acquavella Europe (Aprilia, Italy) Cohort deaths among 2127 registered farmers aged 30 years or older who were residents of Aprilia between 1971 and 1988; the population of Italy was used as a reference crop no 3 SMR 1.38 (0.44, 4.35) - 0.81 (0.58,1.12)
Fincham [49] 1992 Khuder Canada (Alberta) Case-control 1130 male farmers and 3563 men in other occupations between 25 and 74 years of age from the Alberta Cancer Registry during 1983–1988 diagnosed with their first neoplasm not specified no 8 OR 0.33 (0.16, 0.68) - -
Forastiere [50] 1993 Khuder Europe (Italy) Case-control (cancer deaths) 2154 deaths (1674 cancer deaths and 480 referent deaths of all causes) among men aged 35–80 in rural areas surrounding the Viterbo Province between 1980 and 1986 crop employed > 10 years 10 OR 0.67 (0.29, 1.50) 1.04
(0.43, 2.44)
-
Gallagher [51] 1989 Acquavella Canada (British Columbia) PMR deaths among persons aged 20 and older in British Columbia recorded during 1950 and 1984; 35,668 deaths among male farmers, managers, and laborers compared with all other deaths among the 536,636 mixed no 111 PMR 0.98 (0.81, 1.18) - 0.84
(0.68, 1.02)
Gandhi [11] 2014 Agricola US Case-control (cancer deaths) 26 brain cancer deaths during 1990–2003 and randomly sampled controls from 43,904 poultry and nonpoultry workers who were members of the United Food and Commercial Worker union between 1949 and 1989 in the US livestock, crop no 6 OR 1.6 (0.3, 8.4) - -
Gunnarsdottir [52] 1991 Khuder Europe (Iceland) Cohort 5922 men registered with the Farmers’ Pension Fund between 1971 and 1980; Icelandic male population was used as a reference livestock no 11 SIR 1.28 (0.73, 2.52) - 0.72
(0.63, 0.82)
Heineman [53] 1995 Khuder Asia (Shanghai, China) Cohort 276 cases of brain cancer among women age 30 years or older in the Shanghai Cancer Registry during 1980–1984; the 1982 census and a sample of retirees from the same urban districts were used a reference crop grain farmers (higher probability of exposure to pesticides) 3 SIR 2.8 (0.6, 8.0) 6.5
(1.3, 19.1)
-
Howe [54] 1983 Khuder Canada Cohort deaths among 415,201 males in Canada from 1965 to 1969 with data documented on occupation; the Canadian population and the occupational cohort as a whole were used as a reference not specified no 4 SMR 1.77 (0.59, 4.22) - 0.88
(0.79, 0.98)
Inskip [55] 1996 Khuder Europe (England and Wales) PMR all deaths among England and Wales at ages 20–74 during 1979–80 and 1982–90; 62,780 deaths among farmers were compared with those of the general working population not specified no 495 PCMR 1.12 (1.03, 1.22) - 0.96
(0.91, 1.02)
Keller [56] 1994 Khuder US (Illinois) Case-control 9514 cancer cases reported to the Illinois state cancer registry between 1986 and 1988 with information on both employment and tobacco use mixed no 30 OR 1.39 (0.86, 2.24) - -
Kristensen [12] 1996 Khuder Europe (Norway) Cohort cancer occurrence among 246,104 farm holders and spouses in Norway identified through the agricultural census in 1969–1989; the total rural population of Norway was used as reference livestock, crop those who purchased pesticides 122 SIR 0.91 (0.77, 1.08) 1.24
(0.89, 1.73)
0.84
(0.71, 1.0)
Lee [57] 2002 Pubmed US (26 states) PMR deaths among from 26 states during 1984–1993; deaths among crop and livestock industry farmers (n = 267,479) were compared to all deaths (~5.7 million) livestock, crop no 869 PMR 1.08 (0.93, 1.25) - 0.90
(0.86, 0.95)
Lee [13] 2005 Pubmed US (Nebraska) Case-control White male cases of histologically confirmed incident cases of glioma aged 21 and older diagnosed between 1988 and 1993 from the Nebraska Cancer Registry or from 11 hospitals (n = 251) and population-based controls either from the general population via random digit dialing or from Medicare files or death certificates (n = 498) not specified ≥ 55 years farmed 89 OR 1.51 (1.01, 2.27) 3.9
(1.8, 8.6)
-
Mallin [58] 1989 Khuder US (Illinois) Case-control (cancer deaths) deaths from seven cancer sites (n = 10,013) and randomly sampled non-cancer deaths (n = 3198) among black and white men aged 35–74 in Illinois during 1979–1984 not specified no 70 OR 1.70 (1.23, 2.38) - -
Mastrangelo [59] 1996 Khuder Europe (Padova, Italy) Cohort deaths among 2283 male dairy cattle and crop/orchard farmers in Veneto during 1970–1992; the Italian male population was used as a reference livestock, crop no 7 SMR 2.36 (1.12, 4.98) - -
McLaughlin [60] 1987 Khuder Europe (Sweden) Cohort 3394 intercranial gliomas among Swedish malesg,r employed in 1960 and followed from 1961 to 1979; the Swedish population was used as a reference not specified no 621 SIR 1.10 (1.02, 1.19) - -
Menegoz [61] 2002 Pubmed Multi-national study Case-control histologically confirmed meningiomas (n = 330) aged 20–80 years and diagnosed during 1980–1991; 2229 matched (age group, gender, and study center) controls livestock, crop no 63 OR 1.05 (0.76, 1.45) - -
Milham [62] 1983 Acquavella US (Washington) PMR deaths among 429,926 men during 1950–1979 and 25,066 women excluding homemakers during 1974–1979 in Washington livestock, crop yes 69 PMR 1.11 (0.87, 1.40) - -
Mills [63] 2006 Pubmed US (California) PMR deaths (n = 3977) among current and former farmworkers who were members of the UFW in California during 1973–2000; the US and Hispanic California populations were used as a reference not specified no 18 PMR 0.57 (0.34, 0.90) - 0.79
(0.73,0.84)
Miranda-Filho [14] 2011 Pubmed Brazil (Rio de Janeiro) Case-control (cancer deaths) brain cancer deaths (n = 2040) among adults aged 18 years and older who resided in Rio de Janeiro during 1996–2005, controls (n = 4140) were selected from among all other causes mixed per capita of pesticide sales as an indicator of potential exposure to pesticides 95 OR 1.82 (1.21, 2.71) 1.15
(0.90, 1.47)
-
Musicco [64] 1982 Khuder Europe (Milan, Italy) Case-control patients with glioma (n = 47) and controls (n = 201) with non-neoplastic diseases or benign tumors hospitalized at a neurological institute in Milan, Italy during January 1979 to March 1980; analyzed as matched pairs not specified farmers who worked after 1960 when the use of pesticides and fertilizers was higher 17 OR 1.9 (1.23, 4.66) 5.7
(1.66, 25.78)
-
Musicco [15] 1988 Khuder Europe (Milan, Italy) Case-control patients with glioma brain tumors (n = 240) and hospital controls with non-neoplastic neurological diseases without severe psychiatric disorders (n = 742) aged 20–74 years old hospitalized at a neurological institute in Milan between January 1983 and December 1984 not specified chemical users 61 OR 1.60 (1.06, 2.42) 1.6
(1.04, 2.53)
-
Preston-Martin [37] 1993 Khuder New Zealand Case-control adult male brain cancer patients (n = 1619) and non-brain cancer controls (n = 12,010) obtained from the New Zealand cancer registry between 1972 and 1988 livestock, mixed no 48 OR 3.23 (2.29, 4.57) - -
Rafnsson [65] 1989 Acquavella Europe (Iceland) Cohort 5923 farmers registered in the Farmers’ Pension Fund in Iceland between 1977 and 1984; the Icelandic male population was used as a reference livestock those born between 1934 and 1945, presumably more pesticide use 7 SMR 1.23 (0.49, 2.53) 1.49
(0.04, 8.32)
0.72
(0.58, 0.89)
Rodvall [66] 1996 Khuder Europe (Sweden) Case-control 192 newly diagnosed histologically confirmed cases of glioma and 343 matched controls between the ages 25–74 in central Sweden during 1987–1990 mixed those with self-estimated exposure to pesticides or weedkillers 33 OR 1.12 (0.65, 1.93) 1.92
(0.81, 4.56)
-
Ronco [39] 1992 Khuder Europe (Denmark) Cohort 1970 farmers 15–74 years old registered in the Danish Occupational Cancer Register in 1970; Danish employed population was used as a reference not specified no 291 SIR 1.00 (0.90, 1.13) - -
Ronco [39] 1992 Khuder Europe (Italy) Cohort cancer deaths in Italian farmers aged 18–74 years between 1981 and 1982; deaths from other causes used as a reference not specified no 23 OR 0.54 (0.37, 0.78) - -
Ruder [16] 2009 Pubmed US (Iowa, Michigan, Minnesota, Wisconsin) Case-control 798 cases ages 18 to 80 years of histologically confirmed glioma diagnosed between 1989 and 1992 residing in Iowa, Michigan, Minnesota, and Wisconsin and identified through medical offices, and 1175 controls without glioma were identified through States’ driver’s license and Medicare data livestock, crop pesticides used on farm as child and adult 481 OR 0.85 (0.71, 1.02) 0.61
(0.41, 0.91)
-
Saftlas [17] 1987 Khuder US (Wisconsin) PMR deaths during 1968–1976 among 35,972 white male farmers aged ≥18 years who resided in 69 of 70 Wisconsin counties; US and Wisconsin populations used as a reference livestock, crop youngest cohort with a high level of agricultural production herbicide and insecticide exposure 119 PMR 1.10 (0.92, 1.31) 1.15
(0.90, 1.47)
0.92
(0.90, 0.94)
Salerno [18] 2016 Pubmed Europe (Vercelli, Italy) Case-control first hospital admissions for cancer among adults aged 25 to 79 in Vercelli during 2002–2009 (n = 887); controls did not have cancer or had a different type of cancer from the case (n = 11,491) crop no 6 OR 4.03 (1.22, 11.89) - 1.46
(1.23, 1.73)
Schlehofer [67] 2004 Pubmed International Case-control histologically confirmed incident cases (n = 1169) of glioma aged between 20 and 80 years diagnosed during 1980–1991 recruited from either neurosurgical clinics or cancer registries and population-based controls (n = 1981) not specified exposure to pesticides 115 OR 0.82 (0.48, 1.40) 1.03
(0.67, 1.57)
-
Schwartz [68] 1986 Acquavella US (New Hampshire) PMR deaths among white males aged 20 years or older in specific occupations between 1975 and 1985 (n = 37,500); the national population was used as a reference livestock, crop no 4 PMR 1.33 (0.50, 3.53) - 0.94
(0.87, 1.01)
Stark [69] 1987 Khuder US (New York) Cohort deaths among 20,833 male farm owners and operators aged 18 and older registered in the Farm Bureau in New York from 1973 to 1984; the census population was used as a reference mixed no 12 SMR 1.03 (0.56, 1.75) - 0.61
(0.55, 0.68)
Stubbs [70] 1984 Khuder US (California) PMR deaths among farm workers and farm owners/managers (n = 14,908) compared with deaths in California during 1978–1979 not specified no 26 PCMR 1.67 (1.11, 2.41) - -
Une [71] 1987 Khuder US (South Carolina) PMR deaths (n = 25,949) among male farmers and non-farmers aged 35 to 84 in South Carolina between 1983 and 1984 not specified no 9 PMR 0.79 (0.37, 1.70) - 0.82
(0.74, 0.90)
Walrath [72] 1985 Acquavella US Cohort deaths among 293,958 white males aged 31 to 81 with an active US government life insurance policy in January 1954 in specific occupations compared with all other occupations not specified no 27 SMR 1.04 (0.70,1.49) - 0.90
(0.83, 0.97)
Wigle [73] 1990 Khuder Canada (Saskatchewan) Cohort deaths among 69,513 male farmers in Saskatchewan aged ≥35 years during 1971–1985m mixed no 96 SMR 1.03 (0.84, 1.25) - 0.81
(0.78, 0.84)
Wiklund [38] 1986 Acquavella Europe (Sweden) Cohort cancer incidence among 604,103 men and women working in agriculture or forestry in Sweden during 1961–1979 mixed no 819 RR 1.04 (0.96,1.12) - 0.82
(0.81, 0.83)
Wiklund [19] 1994 Khuder Europe (Sweden) Cohort 50,682 women who worked at least 20 h per week in agriculture as reported in the 1970 Swedish Census, followed from 1971 to 1987 mixed birth cohort 1935+ with the rationale that younger persons tended to use more pesticides 189 SIR 1.05 (0.91, 1.22) 0.85
(0.43, 1.5)
0.85
(0.82, 0.87)
Wiklund [74] 1995 Khuder Europe (Sweden) Cohort 140,208 men who worked at least 20 h per week in agriculture as reported in the 1970 Swedish Census, followed from 1971 to 1987 mixed birth cohort 1935+ with the rationale that younger persons tended to use more pesticides 488 SIR 1.00 (0.91, 1.09) 1.07
(0.77, 1.46)
0.80
(0.78, 0.81)
Wingren [75] 1992 Khuder Europe (Sweden) Case-control (cancer deaths) 570,979 deaths among men age 45 and older in Sweden during 1950–1982; brain cancer deaths compared with deaths from nonmalignant cancers and noncardiovascular disorders not specified no 11 OR 4.80 (2.70, 8.50) - -
Zheng [76] 2001 Pubmed US (Iowa) Case-control 412 histologically confirmed cases of glioma aged 40–85 years identified by the Iowa state health registry during 1984–1987, 2434 population-based controls without a previous cancer diagnosis identified through drivers licenses and Medicare records not specified ≥10 years duration of employment 111 OR 1.33 (1.05, 1.70) 1.27
(0.92, 1.76)
-