Occupational exposure to pesticides and hematological alterations: A survey of farm residents in the South of Brazil

Piccoli, Camila; Cremonese, Cleber; Koifman, Rosalina; Koifman, Sérgio; Freire, Carmen

doi:10.1590/1413-81232018246.13142017

Acessibilidade / Reportar erro

Brasil

Español English

sumário « anterior atual seguinte »

Sumário

FREE THEMES • Ciênc. saúde colet. 24 (6) • June 2019 • https://doi.org/10.1590/1413-81232018246.13142017 copy

Occupational exposure to pesticides and hematological alterations: A survey of farm residents in the South of Brazil

Exposição ocupacional a agrotóxicos e alterações hematológicas: Estudo transversal em moradores rurais do Sul do Brasil

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

This study sought to investigate the association of exposure to organochlorine (OC) and non-persistent pesticides with hematological parameters in an agricultural population in Southern Brazil. A cross-sectional study was conducted with a random sample of 275 farm workers and their families in Farroupilha-RS. A questionnaire was used to collect information on sociodemographic and lifestyle factors, duration, frequency and type of pesticide used, among others. Blood samples were collected and analyzed for serum concentration of 24 OC pesticides and hematological parameters. Associations were explored through linear regression, controlling for confounders. Lifetime use of chemical classes other than organophosphates and dithiocarbamates were associated with decreased number of lymphocytes, while subjects sampled in the high pesticide use season showed higher number of erythrocytes and hemoglobin level. Detectable serum levels of many OC pesticides were associated with lower counts of white blood cells, particularly eosinophils. Although mostly null associations were observed between pesticide use and hematological parameters, findings may suggest that OC pesticides could lead to hematological alterations among agricultural workers.

Keywords
Agricultural workers; Non-persistent pesticides; Organochlorine pesticides; Hematotoxicity; Hematological alterations

	N (%)

	Total N = 275	Men N = 155	Women N = 120
Age (years)
18-30	77 (28.0)	48 (31.0)	29 (24.2)
31-45	67 (24.0)	33 (21.3)	34 (28.3)
46-60	98 (36.0)	54 (34.8)	44 (36.7)
> 60	33 (12.0)	20 (12.9)	13 (10.8)
Years of education
< 8	166 (60.0)	85 (54.8)	81 (67.5)
9-11	79 (29.0)	49 (31.6)	30 (25.0)
≥ 12	30 (11.0)	21 (13.5)	9 (7.5)
Marital status
Married	197 (71.6)	98 (63.2)	99 (82.5)
Single, divorced or widowed	78 (28.4)	57 (36.8)	21 (17.5)
Family income (x1.000 Brazilian reais per year)
≤ 10	39 (14.2)	18 (11.6)	21 (17.5)
11-20	77 (28.0)	40 (25.8)	37 (30.8)
21-50	96 (34.9)	59 (38.1)	37 (30.8)
> 50	63 (22.9)	38 (24.5)	25 (20.8)
Occupation
Farmer	239 (86.9)	142 (91.6)	97 (80.8)
Non farmer	36 (13.1)	13 (8.4)	23 (19.2)
Place of birth
Farroupilha	215 (78.2)	137 (88.4)	78 (65.0)
Other town	60 (21.8)	18 (11.6)	42 (35.0)
Cigarette smoking
Non-smoker	226 (82.2)	112 (72.3)	114 (95.0)
Ex-smoker	34 (12.4)	31 (20.0)	3 (2.5)
Current smoker	15 (5.5)	12 (7.7)	3 (2.5)
Alcohol intake in the last 30 days
No	95 (34.5)	36 (23.2)	59 (49.2)
Yes	180 (65.5)	119 (76.8)	61 (50.8)
Regular physical activity in the last 3 months
No	188 (68.4)	103 (66.5)	85 (70.8)
Yes	87 (31.6)	52 (33.5)	35 (29.2)
Body mass index (BMI)
Underweight or eutrophic (< 25 kg/m²)	110 (40.0)	66 (42.6)	44 (36.7)
Overweight or obese (≥ 25 kg/m²)	165 (60.0)	89 (57.5)	76 (63.3)
History of hematological disorder
No	274 (99.6)	155 (100)	119 (99.2)
Yes	1 (0.4)	0 (0.0)	1 (0.8)
Family history of hematological disorder in first-degree relatives
No	269 (97.8)	151 (97.4)	118 (98.3)
Yes	6 (2.2)	4 (2.6)	2 (1.7)

	N (%)
Years of agricultural work
< 1	29 (10.5)
1-10	40 (14.5)
11-25	60 (21.8)
26-50	114 (41.5)
> 50	32 (11.6)
Years mixing or applying pesticides
< 1	62 (22.5)
1-10	62 (22.5)
> 10	151 (54.9)
Days per year mixing or applying pesticides
< 5	73 (26.5)
5-39	50 (18.1)
40-59	51 (18.5)
≥ 60	101 (36.7)
Sampling season
Low pesticide use season (April-August)	140 (50.9)
High pesticide use season (September-March)	135 (49.1)
Use full personal protective equipment (PPE)	238 (86.5)
Current use of pesticides
All pesticides	132 (48.0)
Herbicides	118 (42.9)
Insecticides	40 (14.5)
Fungicides	63 (22.9)
OP insecticides	37 (13.5)
Dithiocarbamates	42 (15.3)
Other chemical classes^a	127 (46.2)
Total number of pesticides currently used
None	143 (52.0)
1	39 (14.2)
≥ 2	93 (33.8)
Total lifetime years of use
All pesticides
Never	70 (25.5)
1-20	86 (31.3)
> 20	119 (43.3)
Herbicides
Never	73 (26.5)
1-20	95 (34.5)
> 20	107 (38.9)
Insecticides
Never	106 (38.5)
1-20	110 (40.0)
> 20	59 (21.5)
Fungicides
Never	72 (26.2)
1-20	87 (31.6)
> 20	116 (42.2)
OP insecticides
Never	113 (41.1)
1-20	104 (37.8)
> 20	58 (21.1)
Dithiocarbamates
Never	71 (25.8)
1-20	92 (33.5)
>20	112 (40.7)
Other chemical classes^a
Never	185 (67.3)
1-20	62 (22.5)
> 20	28 (10.2)

	% > LOD	P25	Median	P75	N (%) < ref^a	N (%) > ref^b
Hematological parameters
Erythrocytes (m/mm³)	-	4.54	4.91	5.22	16 (5.8)	3 (1.1)
Hemoglobin (g/dL)	-	13.80	14.80	15.70	4 (1.5)	3 (1.1)
Hematocrit (%)	-	41.48	44.30	46.40	7 (2.6)	0 (0.0)
RDW (%)	-	12.20	12.70	13.10	80 (29.1)	3 (1.1)
MCV (fL)	-	86.80	89.95	92.40	1 (0.4)	6 (2.2)
MCH (pg)	-	29.30	30.20	31.20	2 (0.7)	25 (9.1)
MCHC (g/dL)	-	32.98	33.60	34.23	1 (0.4)	21 (7.6)
Leukocytes (u/µL)	-	5,700	6,700	7,900	3 (1.1)	8 (2.9)
Neutrophils (u/µL)	-	2,750	3,418	4,158	0 (0.0)	6 (2.2)
Lymphocytes (u/µL)	-	1,993	2,397	2,842	2 (0.7)	0 (0.0)
Monocytes (u/µL)	-	371	456	560	0 (0.0)	1 (0.04)
Eosinophils (u/µL)	-	118	201	285	0 (0.0)	25 (9.1)
Basophils (u/µL)	-	0	0	0	0 (0.0)	0 (0.0)
OC pesticides (ng/g)
α–HCH	30.9	<LOD	<LOD	10.10	-	-
β–HCH	41.3	<LOD	<LOD	29.48	-	-
γ–HCH	50.2	<LOD	3.71	12.36	-	-
HCB	28.0	<LOD	<LOD	11.53	-	-
Heptachlor	32.9	<LOD	<LOD	<LOD	-	-
Heptachlor epoxide A	1.8	<LOD	<LOD	21.07	-	-
Heptachlor epoxide B	5.5	<LOD	<LOD	<LOD	-	-
α–chlordane	0.0	-	-	-	-	-
γ–chlordane	10.3	<LOD	<LOD	<LOD	-	-
Trans-nonachlor	1.8	<LOD	<LOD	<LOD	-	-
o,p’-DDT	12.5	<LOD	<LOD	<LOD	-	-
p,p’-DDT	42.8	<LOD	<LOD	<LOD	-	-
o,p’-DDE	10.3	<LOD	<LOD	40.59	-	-
p,p’-DDE	39.5	<LOD	<LOD	<LOD	-	-
o,p’-DDD	3.7	<LOD	<LOD	30.27	-	-
p,p’-DDD	14.4	<LOD	<LOD	<LOD	-	-
Aldrin	2.6	<LOD	<LOD	<LOD	-	-
Endrin	30.6	<LOD	<LOD	<LOD	-	-
Dieldrin	6.6	<LOD	<LOD	<LOD	-	-
Endosulfan I	22.9	<LOD	<LOD	<LOD	-	-
Endosulfan II	2.2	<LOD	<LOD	<LOD	-	-
Methoxychlor	4.4	<LOD	<LOD	<LOD	-	-
Mirex	1.5	<LOD	<LOD	<LOD	-	-
Pentachloroanisole	26.6	<LOD	<LOD	0.71	-	-

Exposure variables	Erythrocytes	Hemoglobin	Leukocytes^b	Neutrophils^b	Lymphocytes^b	Monocytes^b	Eosinophils^b
Farmer (ref = non-farmer)	-0.08 (-0.22; 0.07)	-0.17 (-0.54; 0.18)	1.07 (0.96; 1.20)	1.12 (0.99; 1.26)	1.01 (0.91; 1.12)	1.04 (0.91; 1.19)	0.99 (0.76; 1.28)
High pesticide use season (ref = low use season)	0.10 (0.01; 0.19)	0.22 (0.00; 0.45)	0.98 (0.91; 1.05)	1.01 (0.93; 1.08)	1.02 (0.95; 1.08)	0.92 (0.85; 1.01)	0.98 (0.84; 1.16)
Years of agricultural work (ref = < 1)
1-10	0.09 (-0.12; 0.29)	0.28 (-0.21; 0.77)	0.94 (0.81; 1.09)	0.91 (0.78; 1.08)	0.98 (0.85; 1.13)	0.97 (0.81; 1.15)	0.99 (0.70; 1.43)
11-25	0.07 (-0.11; 0.26)	0.28 (-0.16; 0.72)	0.99 (0.86; 1.12)	1.03 (0.88; 1.19)	0.95 (0.84; 1.08)	0.94 (0.80; 1.10)	0.90 (0.66; 1.25)
26-50	0.14 (-0.07; 0.35)	0.41 (-0.10; 0.92)	0.96 (0.83; 1.12)	0.94 (0.79; 1.12)	1.01 (0.86; 1.16)	1.07 (0.88; 1.27)	0.88 (0.62; 1.30)
> 50	0.15 (-0.46; 0.46)	0.43 (-0.32; 1.18)	0.88 (0.70; 1.10)	0.94 (0.74; 1.21)	0.97 (0.78; 1.20)	1.10 (0.84; 1.46)	0.62 (0.36; 1.06)
p for trend	0.22	0.13	0.55	0.69	0.86	0.59	0.33
Years mixing/applying pesticides (ref = < 1)
1-10	0.03 (-0.12; 0.19)	0.05 (-0.33; 0.42)	0.94 (0.84; 1.05)	0.97 (0.86; 1.10)	0.92 (0.84; 1.03)	0.98 (0.85; 1.12)	0.82 (0.65; 1.13)
>10	0.10 (-0.05; 0.25)	0.32 (-0.04; 0.68)	1.01 (0.89; 1.12)	1.06 (0.94; 0.19)	0.99 (0.89; 1.09)	1.06 (0.92; 1.20)	0.93 (0.72; 1.20)
p for trend	0.16	0.92	0.85	0.25	0.89	0.36	0.65
Days/year mixing/applying pesticides (ref = < 5)
5-39	0.15 (-0.04; 0.30)	0.37 (0.02; 0.73)	1.01 (0.90; 1.13)	1.11 (0.99; 1.26)	0.98 (0.89; 1.08)	1.10 (0.96; 1.24)	1.07 (0.80; 1.35)
40-59	0.09 (-0.07; 0.26)	0.21 (-0.19; 0.61)	1.01 (0.90; 1.16)	1.05 (0.91; 1.20)	1.02 (0.90; 1.13)	1.02 (0.88; 1.19)	0.97 (0.74; 1.32)
≥ 60	0.03 (-0.12; 0.18)	0.17 (-0.19; 0.53)	0.99 (0.88; 1.11)	0.99 (0.89; 1.14)	1.01 (0.90; 1.11)	1.02 (0.89; 1.16)	0.89 (0.71; 1.21)
p for trend	0.86	0.67	0.75	0.55	0.78	0.12	0.39
No. of pesticides currently used (ref= none)
1	-0.08 (-0.22; 0.07)	-0.19 (-0.54; 0.16)	1.00 (0.89; 1.11)	0.94 (0.84; 1.05)	1.06 (0.95; 1.17)	1.05 (0.92; 1.20)	0.98 (0.76; 1.27)
≥ 2	-0.01 (-0.12; 0.11)	-0.11 (-0.39; 0.16)	1.03 (0.95; 1.13)	1.02 (0.92; 1.12)	1.01 (0.93; 1.09)	1.05 (0.94; 1.16)	0.99 (0.83; 1.24)
p for trend	0.89	0.41	0.38	0.71	0.80	0.38	0.90
Lifetime years of pesticide use (ref= none)
All pesticides
1-20	-0.10 (-0.23; 0.03)	-0.28 (-0.60; 0.03)	1.01 (0.12; 1.12)	0.95 (0.85; 1.05)	1.06 (0.97; 1.17)	0.92 (0.82; 1.04)	1.01 (0.80; 1.27)
> 20	-0.01 (-0.16; 0.15)	-0.06 (-0.44; 0.33)	1.05 (0.93; 1.18)	1.01 (0.88; 1.16)	1.04 (0.93; 1.16)	0.97 (0.84; 1.11)	0.94 (0.71; 1.24)
p-trend	0.80	0.63	0.45	0.98	0.40	0.59	0.68
Fungicides
1-20	0.11 (-0.03; 0.24)	0.28 (-0.03; 0.60)	0.99 (0.90; 1.09)	1.05 (0.95; 1.17)	0.94 (0.86; 1.03)	1.06 (0.94; 1.18)	1.02 (0.81; 1.28)
> 20	0.03 (-0.13; 0.19)	0.07 (-0.32; 0.45)	0.95 (0.85; 1.08)	1.01 (0.88; 1.14)	0.96 (0.86; 1.07)	1.01 (0.88; 1.16)	1.08 (0.82; 1.43)
p-trend	0.57	0.60	0.49	0.84	0.43	0.82	0.57
Insecticides
1-20	0.11 (-0.01; 0.22)	0.24 (-0.03; 0.51)	1.04 (0.96; 1.14)	1.07 (0.98; 1.17)	0.96 (0.89; 1.05)	1.07 (0.97; 1.18)	0.97 (0.80; 1.19)
> 20	0.07 (-0.08; 0.22)	0.06 (-0.29; 0.42)	1.01 (0.88; 1.11)	1.01 (0.88; 1.12)	0.91 (0.83; 1.01)	0.99 (0.87; 1.12)	0.99 (0.76; 1.28)
p-trend	0.21	0.49	0.74	0.41	0.08	0.84	0.89
Herbicides
1-20	0.06 (-0.07; 0.19)	0.17 (-0.15; 0.48)	0.96 (0.87; 1.06)	1.03 (0.93; 1.15)	0.96 (0.88; 1.05)	1.01 (0.90; 1.14)	0.94 (0.75; 1.19)
> 20	0.03 (-0.12; 0.19)	-0.03 (-0.41; 0.35)	0.94 (0.88; 1.07)	0.99 (0.88; 1.13)	0.99 (0.90; 1.10)	1.01 (0.88; 1.16)	0.93 (0.82; 1.42)
p-trend	0.66	0.99	0.48	0.98	0.85	0.85	0.63
OP insecticides
1-20	0.08 (-0.04; 0.19)	0.19 (-0.08; 0.46)	1.04 (0.95; 1.12)	1.07 (0.98; 1.17)	0.94 (0.89; 1.04)	1.05 (0.95; 1.16)	0.95 (0.78; 1.19)
> 20	0.01 (-0.13; 0.16)	-0.07 (-0.42; 0.28)	0.99 (0.89; 1.10)	1.01 (0.89; 1.13)	0.90 (0.83; 1.01)	0.98 (0.86; 1.11)	0.92 (0.71; 1.16)
p-trend	0.61	0.99	0.90	0.63	0.06	0.99	0.51
Dithiocarbamates
1-20	0.09 (-0.04; 0.22)	0.28 (-0.03; 0.60)	0.90 (0.89; 1.09)	1.05 (0.94; 1.16)	0.94 (0.86; 1.03)	1.08 (0.94; 1.21)	0.99 (0.79; 1.25)
> 20	0.01 (-0.16; 0.16)	0.14 (-0.25; 0.52)	0.95 (0.84; 1.07)	0.99 (0.88; 1.14)	0.96 (0.85; 1.06)	1.02 (0.88; 1.18)	1.01 (0.75; 1.32)
p-trend	0.85	0.40	0.44	0.95	0.38	0.65	0.99
Other chemical classes
1-20	0.03 (-0.09; 0.15)	0.25 (-0.03; 0.53)	1.01 (0.93; 1.10)	0.99 (0.89; 1.07)	1.03 (0.95; 1.11)	1.04 (0.93; 1.15)	1.01 (0.82; 1.24)
> 20	-0.11 (-0.27; 0.06)	-0.14 (-0.54; 0.25)	0.88 (0.79; 1.01)	0.88 (0.77; 1.01)	0.87 (0.78; 0.97)	0.90 (0.78; 1.05)	0.99 (0.74; 1.32)
p-trend	0.43	0.81	0.20	0.13	0.12	0.50	0.98

Levels > LOD (ref = undetected)	Erythrocytes	Hemoglobin	Leukocytes^b	Neutrophils^b	Lymphocytes^b	Monocytes^b	Eosinophils^b
α–HCH	0.06 (-0.09; 0.22)	0.03 (-0.07; 0.38)	0.97 (0.94; 0.99)	0.97 (0.94; 0.99)	0.97 (0.94; 0.99)	0.96 (0.93; 1.02)	0.94 (0.88; 1.01)
β–HCH	-0.04 (-0.20; 0.12)	0.11 (-0.13; 0.34)	1.03 (0.96; 1.11)	1.03 (0.96; 1.12)	1.01 (0.95; 1.08)	0.96 (0.87; 1.05)	1.09 (0.93; 1.31)
γ–HCH	0.02 (-0.14; 0.18)	0.04 (-0.19; 0.26)	1.01 (0.94; 1.07)	0.99 (0.92; 1.07)	1.03 (0.96; 1.09)	0.87 (0.81; 0.95)	0.81 (0.69; 0.96)
HCB	0.17 (-0.02; 0.32)	0.28 (-0.03; 0.53)	1.06 (0.98; 1.14)	1.06 (0.98; 1.15)	1.06 (0.98; 1.14)	0.98 (0.88; 1.07)	0.90 (0.75; 1.08)
Heptachlor	-0.04 (-0.19; 0.11)	-0.01 (-0.25; 0.23)	0.96 (0.89; 1.03)	0.96 (0.88; 1.03)	0.83 (0.91; 1.04)	0.83 (0.76; 0.91)	0.76 (0.63; 0.89)
Heptachlor epoxide A	-0.24 (-0.64; 0.16)	-0.43 (-1.26; 0.41)	0.83 (0.64; 1.07)	0.83 (0.64; 1.07)	0.84 (0.66; 1.06)	0.93 (0.68; 1.27)	1.15 (0.63; 2.11)
Heptachlor epoxide B	-0.21 (-0.47; 0.06)	-0.32 (-0.82; 0.18)	0.96 (0.83; 1.13)	0.96 (0.83; 1.13)	1.01 (0.87; 1.16)	0.91 (0.76; 1.09)	0.80 (0.56; 1.16)
γ–chlordane	-0.13 (-0.32; 0.06)	-0.40 (-0.77; -0.03)	0.96 (0.85; 1.07)	0.96 (0.85; 1.07)	0.95 (0.88; 1.09)	0.95 (0.83; 1.08)	0.76 (0.59; 1.01)
Trans-nonachlor	-0.13 (-0.60; 0.34)	-0.75 (-1.59; 0.08)	1.08 (0.84; 1.40)	1.08 (0.84; 1.40)	1.23 (0.94; 1.52)	1.23 (0.91; 1.68)	0.51 (0.28; 0.94)
o,p’-DDT	-0.05 (-0.23; 0.13)	-0.04 (-0.38; 0.30)	0.95 (0.86; 1.06)	0.95 (0.86; 1.06)	0.97 (0.88; 1.07)	0.97 (0.85; 1.09)	0.94 (0.73; 1.21)
p,p’-DDT	0.11 (-0.05; 0.26)	-0.01 (-0.24; 0.23)	0.97 (0.90; 1.05)	0.97 (0.91; 1.05)	0.95 (0.88; 1.01)	0.91 (0.84; 0.99)	0.93 (0.79; 1.10)
o,p’-DDE	-0.19 (-0.38; 0.01)	-0.12 (-0.49; 0.25)	0.93 (0.84; 1.05)	0.93 (0.84; 1.04)	0.94 (0.84; 1.04)	0.84 (0.74; 0.97)	0.77 (0.59; 1.01)
p,p’-DDE	-0.09 (-0.25; 0.07)	-0.09 (-0.33; 0.15)	0.97 (0.89; 1.05)	0.97 (0.90; 1.05)	0.95 (0.88; 1.02)	0.91 (0.84; 0.99)	0.85 (0.72; 1.02)
o,p’-DDD	-0.08 (-0.39; 0.24)	0.07 (-0.53; 0.67)	0.89 (0.75; 1.08)	0.89 (0.75; 1.08)	0.85 (0.72; 1.01)	0.83 (0.66; 1.03)	0.63 (0.41; 0.97)
p,p’-DDD	-0.10 (-0.28; 0.08)	-0.18 (-0.50; 0.15)	0.94 (0.86; 1.05)	0.97 (0.90; 1.05)	1.01 (0.91; 1.09)	0.93 (0.83; 1.05)	0.70 (0.55; 0.88)
Aldrin	0.21 (-0.20; 0.63)	0.22 (-0.49; 0.94)	0.91 (0.73; 1.14)	0.91 (0.73; 1.14)	0.79 (0.65; 0.97)	0.85 (0.66; 1.12)	0.87 (0.52; 1.46)
Endrin	-0.04 (-0.19; 0.11)	-0.06 (-0.30; 0.19)	0.97 (0.91; 1.05)	0.97 (0.89; 1.05)	1.01 (0.93; 1.07)	0.92 (0.84; 1.02)	0.73 (0.61; 0.87)
Dieldrin	0.04 (-0.18; 0.26)	0.07 (-0.38; 0.53)	0.96 (0.84; 1.10)	0.96 (0.84; 1.10)	0.99 (0.87; 1.13)	0.99 (0.84; 1.17)	0.80 (0.58; 1.11)
Endosulfan I	-0.13 (-0.28; 0.02)	-0.11 (-0.38; 0.16)	1.01 (0.93; 1.09)	1.01 (0.92; 1.09)	1.05 (0.97; 1.15)	0.99 (0.89; 1.09)	0.76 (0.63; 0.91)
Endosulfan II	-0.16 (-0.63; 0.31)	-0.39 (-1.15; 0.38)	0.98 (0.77; 1.24)	0.99 (0.77; 1.26)	0.94 (0.76; 1.18)	1.04 (0.79; 1.39)	1.30 (0.75; 2.27)
Methoxychlor	-0.18 (-0.49; 0.14)	0.15 (-0.09; 0.38)	0.91 (0.77; 1.09)	0.91 (0.77; 1.08)	0.91 (0.77; 1.06)	0.97 (0.79; 1.20)	0.66 (0.45; 0.98)
Mirex	-0.25 (-0.83; 0.33)	-0.13 (-1.06; 0.81)	0.99 (0.74; 1.38)	0.99 (0.73; 1.32)	0.91 (0.69; 1.19)	1.05 (0.74; 1.48)	1.07 (0.54; 2.11)
Pentachloroanisole	0.04 (-0.11; 0.19)	0.06 (-0.20; 0.31)	1.03 (0.95; 1.11)	1.03 (0.95; 1.10)	1.01 (0.94; 1.08)	0.95 (0.87; 1.05)	0.87 (0.72; 1.04)

ABRASCO - Associação Brasileira de Saúde Coletiva Av. Brasil, 4036 - sala 700 Manguinhos, 21040-361 Rio de Janeiro RJ - Brazil, Tel.: +55 21 3882-9153 / 3882-9151 - Rio de Janeiro - RJ - Brazil
E-mail: cienciasaudecoletiva@fiocruz.br

Acompanhe os números deste periódico no seu leitor de RSS

[1] Collaborations

C Piccoli has contributed to the acquisition, analysis and interpretation of data, and drafting the work. C Freire has contributed to analysis and interpretation of data, and drafting the work. C Cremonese has contributed to the conception of the study, and acquisition and analysis of data. R Koifman and S Koifman have contributed to the conception and design of the study, and interpretation of data. All of the authors revised the work critically and approved the submitted version of the manuscript.