Inequities in access to mammographic screening in Brazil

Our objectives with this study were to describe the spatial distribution of mammographic screening coverage across small geographical areas (micro-regions) in Brazil, and to analyze whether the observed differences were associated with spatial inequities in socioeconomic conditions, provision of health care, and healthcare services utilization. We performed an area-based ecological study on mammographic screening coverage in the period of 2010-2011 regarding socioeconomic and healthcare variables. The units of analysis were the 438 health micro-regions in Brazil. Spatial regression models were used to study these relationships. There was marked variability in mammographic coverage across micro-regions (median = 21.6%; interquartile range: 8.1%-37.9%). Multivariable analyses identified high household income inequality, low number of radiologists/100,000 inhabitants, low number of mammography machines/10,000 inhabitants, and low number of mammograms performed by each machine as independent correlates of poor mammographic coverage at the micro-region level. There was evidence of strong spatial dependence of these associations, with changes in one micro-region affecting neighboring micro-regions, and also of geographical heterogeneities. There were substantial inequities in access to mammographic screening across micro-regions in Brazil, in 2010-2011, with coverage being higher in those with smaller wealth inequities and better access to health care.

Keywords:
Health Inequalities; Breast Neoplasm; Health Services Accessibility

Variable /Brazilian regions *	Number of health micro-regions	Variable distribution per health micro-regions
Variable /Brazilian regions *	Number of health micro-regions	Mean	SD	Minimum value	Q1	Median	Q3	Maximum value
Outcome variable
Mammography ratio (per 100 women, %), 2010-2011
Brazil	438	24.15	17.96	0.05	8.06	21.58	37.87	84.15
Southeast	153	37.04	14.81	2.19	27.72	37.26	44.66	84.15
South	68	37.19	12.81	13.95	27.92	36.52	43.02	73.58
Northeast	133	13.40	10.70	0.05	5.94	12.15	17.48	51.55
Central	39	8.55	8.57	0.19	2.82	5.03	12.32	32.56
North	45	5.95	6.72	0.20	0.80	4.20	9.68	30.31
Socioeconomic conditions (distal variables)
Population size (x 1,000), 2010
Brazil	438	435.52	846.80	21.47	152.19	250.12	396.32	11253.50
Southeast	153	525.26	1272.24	44.27	128.29	236.19	393.43	11253.50
South	68	402.75	466.20	94.96	182.14	271.87	397.34	3223.84
Northeast	133	399.11	501.23	44.66	187.46	277.16	400.62	3908.76
Central	39	360.46	507.38	21.47	102.66	161.29	354.36	2570.16
North	45	352.54	421.38	41.34	137.53	214.88	377.47	2119.74
GDP per capita (x 1,000 BRL), 2010
Brazil	438	14.62	9.48	3.15	6.73	13.04	19.17	59.22
Southeast	153	19.01	10.35	4.48	12.15	17.76	23.43	59.22
South	68	20.08	6.55	10.04	15.53	18.84	22.89	43.10
Northeast	133	7.14	4.19	3.15	4.77	5.80	8.08	39.49
Central	39	18.01	8.81	7.08	12.99	15.59	21.86	58.33
North	45	10.61	5.40	3.18	6.07	10.39	12.45	30.83
Gini index of per capita household income (%), 2010
Brazil	438	50.92	5.11	38.00	48.00	51.00	54.00	71.00
Southeast	153	47.85	3.47	40.00	45.00	48.00	50.00	65.00
South	68	47.00	4.00	38.00	44.00	47.50	50.00	54.00
Northeast	133	53.68	2.92	48.00	51.00	54.00	56.00	63.00
Central	39	51.69	3.77	46.00	49.00	51.00	54.00	64.00
North	45	58.40	4.28	50.00	55.00	58.00	61.00	71.00
Population with secondary or higher education (%), 2010
Brazil	438	46.11	10.22	20.54	36.91	46.69	53.74	70.75
Southeast	153	51.11	8.94	26.63	46.57	52.90	57.87	66.90
South	68	51.38	6.10	39.79	47.66	50.08	54.66	67.74
Northeast	133	37.91	8.28	26.35	32.43	35.70	40.54	70.15
Central	39	48.76	6.96	38.30	43.80	46.88	52.13	70.75
North	45	43.08	10.41	20.54	36.11	40.35	48.84	65.79
Urbanization rate (%), 2010
Brazil	438	75.16	15.43	40.00	63.00	77.00	89.00	100.00
Southeast	153	84.86	12.30	42.00	80.00	89.00	94.00	100.00
South	68	78.68	10.94	55.00	70.50	80.00	85.25	99.00
Northeast	133	63.47	13.18	40.00	54.00	62.00	70.00	100.00
Central	39	79.87	10.91	58.00	69.00	81.00	89.50	98.00
North	45	67.31	13.95	43.00	57.00	65.00	77.00	98.00
Provision of health care (intermediate variables)
FHS coverage (%)
Brazil	438	78.42	22.65	13.01	64.92	86.50	98.11	100.00
Southeast	153	66.89	25.23	13.01	47.02	68.06	90.33	100.00
South	68	69.14	22.52	20.70	57.06	71.06	84.93	100.00
Northeast	133	94.53	9.62	40.63	92.76	98.13	100.00	100.00
Central	39	80.66	17.12	27.69	71.97	85.84	93.33	100.00
North	45	82.10	14.02	43.20	75.13	83.80	91.80	100.00
Physician ratio (per 1,000), 2010
Brazil	438	1.00	0.62	0.12	0.54	0.85	1.31	3.64
Southeast	153	1.35	0.63	0.30	0.93	1.24	1.64	3.64
South	68	1.27	0.54	0.63	0.87	1.14	1.44	2.99
Northeast	133	0.64	0.40	0.26	0.42	0.53	0.68	2.69
Central	39	0.92	0.54	0.42	0.58	0.85	0.96	2.73
North	45	0.59	0.38	0.12	0.33	0.47	0.72	1.47
Radiologist ratio (per 100,000), 2010
Brazil	438	2.93	2.59	0.00	1.00	2.00	4.00	20.00
Southeast	153	3.94	2.92	0.00	2.00	3.00	5.00	20.00
South	68	3.91	2.28	1.00	2.00	3.50	5.00	10.00
Northeast	133	1.79	1.85	0.00	1.00	1.00	2.00	11.00
Central	39	2.87	2.48	0.00	1.00	2.00	4.00	11.00
North	45	1.38	1.51	0.00	0.00	1.00	2.00	5.00
Mammography machines ratio (per 10,000), 2010
Brazil	438	1.19	0.86	0.00	0.63	1.14	1.66	7.70
Southeast	153	1.44	0.78	0.00	0.89	1.43	1.86	3.87
South	68	1.38	0.59	0.39	0.89	1.32	1.76	3.29
Northeast	133	0.84	0.70	0.00	0.43	0.71	1.18	3.31
Central	39	1.31	0.96	0.00	0.66	1.38	1.95	3.67
North	45	0.95	1.31	0.00	0.00	0.73	1.36	7.70
Healthcare services utilization (proximal variable)
Mammographic examinations per machine (x 100), 2010
Brazil	438	7.14	6.86	0.00	1.43	6.03	10.30	52.06
Southeast	153	9.66	6.58	0.00	5.38	8.21	12.48	30.39
South	68	11.94	6.42	3.80	7.89	9.75	13.79	34.33
Northeast	133	5.02	6.28	0.00	0.14	3.87	7.78	52.06
Central	39	2.24	2.66	0.00	0.11	1.59	3.67	10.52
North	45	1.82	3.06	0.00	0.00	0.22	2.41	12.42

Variables *	Step 1			Step 2			Step 3
	Impacts (p-value)			Impacts (p-value)			Impacts (p-value)
	Direct	Indirect	Total	Direct	Indirect	Total	Direct	Indirect	Total
Regions **
Southeast	Ref.	Ref.	Ref.	Ref.	Ref.	Ref.	Ref.	Ref.	Ref.
South	0.263 (0.859)	0.166 (0.863)	0.429 (0.860)	-0.103 (0.850)	-0.065 (0.859)	-0.167 (0.853)	-2.006 (0.100)	-0.859 (0.142)	-2.865 (0.108)
Northeast	-6.732 (0.001)	-4.241 (0.001)	-10.972 (< 0.001)	-6.793 (< 0.001)	-4.274 (< 0.001)	-11.067 (< 0.001)	-2.676 (0.078)	-1.145 (0.089)	-3.820 (0.075)
Central	-14.693 (< 0.001)	-9.257 (< 0.001)	-23.951 (< 0.001)	-14.811 (< 0.001)	-9.319 (< 0.001)	-24.130 (< 0.001)	-9.846 (< 0.001)	-4.214 (< 0.001)	-14.060 (< 0.001)
North	-8.500 (0.001)	-5.355 (0.002)	-13.856 (0.001)	-7.831 (0.001)	-4.927 (0.001)	-12.758 (0.000)	-2.641 (0.237)	-1.131 (0.261)	-3.772 (0.237)
Population (x 1,000, log)	1.985 (0.005)	1.251 (0.016)	3.236 (0.006)	1.668 (0.039)	1.050 (0.058)	2.718 (0.042)	-0.278 (0.734)	-0.119 (0.738)	-0.396 (0.734)
GDP per capita (x 1,000 BRL)	0.102 (0.106)	0.064 (0.115)	0.166 (0.106)	0.101 (0.144)	0.064 (0.150)	0.165 (0.142)	0.112 (0.152)	0.048 (0.188)	0.160 (0.156)
Gini index (%)	-0.648 (< 0.001)	-0.408 (0.002)	-1.056 (0.000)	-0.600 (0.000)	-0.378 (0.000)	-0.978 (0.000)	-0.562 (< 0.001)	-0.241 (< 0.001)	-0.803 (< 0.001)
Urbanization rate (%)	0.158 (0.002)	0.099 (0.009)	0.257 (0.002)	0.074 (0.363)	0.046 (0.382)	0.120 (0.368)	0.037 (0.421)	0.016 (0.457)	0.052 (0.429)
FHS coverage (%)				0.049 (0.120)	0.031 (0.126)	0.080 (0.117)	-0.004 (0.805)	-0.002 (0.815)	-0.006 (0.807)
Radiologists ratio per 100,000 inhabitants				0.870 (0.001)	0.548 (0.011)	1.418 (0.002)	0.919 (< 0.001)	0.393 (0.001)	1.312 (< 0.001)
Mammography machines ratio per 10,000 inhabitants				2.451 (< 0.001)	1.542 (0.001)	3.993 (< 0.001)	3.715 (< 0.001)	1.590 (< 0.001)	5.305 (< 0.001)
Mammograms per mammography machine (x 100)							0.948 (< 0.001)	0.406 (< 0.001)	1.353 (< 0.001)
Model diagnostics
AIC	3302.700			3278.900			3140.200
Breusch-Pagan test heterocedasticity	0.106			0.167			0.290
Test for residual autocorrelation	0.396			0.460			0.072

Regions/Variables	Step 1			Step 2			Step 3
	Impacts (p-value)			Impacts (p-value)			Impacts (p-value)
	Direct	Indirect	Total	Direct	Indirect	Total	Direct	Indirect	Total
Souheast
Population (x 1,000, log)	0.848 (0.395)	0.450 (0.408)	1.298 (0.394)	0.878 (0.562)	0.444 (0.569)	1.323 (0.561)	-1.566 (0.114)	-0.489 (0.154)	-2.055 (0.115)
GDP per capita (x 1,000 BRL)	0.146 (0.229)	0.077 (0.296)	0.224 (0.247)	0.153 (0.137)	0.077 (0.191)	0.231 (0.147)	0.144 (0.129)	0.045 (0.162)	0.189 (0.127)
Gini index (%)	-1.416 (< 0.001)	-0.751 (< 0.001)	-2.168 (< 0.001)	-1.373 (< 0.001)	-0.695 (0.001)	-2.067 (< 0.001)	-0.914 (< 0.001)	-0.285 (0.003)	-1.199 (< 0.001)
Urbanization rate (%)	-0.052 (0.230)	0.071 (0.250)	0.205 (0.230)	0.030 (0.614)	0.015 (0.675)	0.045 (0.632)	0.030 (0.919)	0.009 (0.924)	0.039 (0.919)
FHS coverage (%)				0.008 (0.906)	0.004 (0.900)	0.013 (0.903)	-0.061 (0.048)	-0.019 (0.083)	-0.080 (0.050)
Radiologists ratio per 100,000 inhabitants				0.598 (0.063)	0.303 (0.089)	0.901 (0.064)	0.692 (0.014)	0.216 (0.049)	0.908 (0.015)
Mammography machines ratio per 10,000 inhabitants				2.300 (0.008)	1.432 (0.031)	4.262 (0.011)	5.510 (< 0.001)	1.719 (0.001)	7.229 (< 0.001)
Mammograms per mammography machine (x 100)							0.965 (< 0.001)	0.301 (0.001)	1.266 (< 0.001)
South
Population (x 1,000, log)	9.210 (0.000)	4.885 (0.011)	14.095 (0.000)	7.710 (0.004)	3.902 (0.027)	11.613 (0.006)	5.946 (< 0.001)	1.856 (0.012)	7.802 (< 0.001)
GDP per capita (x 1,000 BRL)	-0.018 (0.975)	-0.010 (0.966)	-0.027 (0.972)	0.025 (0.991)	0.013 (1.000)	0.038 (0.994)	0.101 (0.698)	0.031 (0.726)	0.132 (0.703)
Gini index (%)	-1.275 (0.000)	-0.676 (0.006)	-1.951 (0.000)	-0.872 (0.011)	-0.441 (0.028)	-1.313 (0.012)	-0.899 (0.002)	-0.280 (0.008)	-1.179 (0.001)
Urbanization rate (%)	-0.223 (0.158)	-0.118 (0.216)	-0.341 (0.169)	-0.058 (0.737)	-0.029 (0.734)	-0.088 (0.734)	-0.114 (0.417)	-0.035 (0.442)	-0.149 (0.418)
FHS coverage (%)				0.203 (0.002)	0.103 (0.012)	0.306 (0.002)	0.072 (0.167)	0.022 (0.220)	0.094 (0.173)
Radiologists ratio per 100,000 inhabitants				1.259 (0.072)	0.637 (0.117)	1.896 (0.080)	1.127 (0.037)	0.352 (0.101)	1.478 (0.043)
Mammography machines ratio per 10,000 inhabitants				3.871 (0.071)	1.959 (0.115)	5.830 (0.078)	13.215 (< 0.001)	4.124 (0.001)	17.339 (< 0.001)
Mammograms per mammography machine (x 100)							1.311 (< 0.001)	0.409 (0.002)	1.720 (< 0.001)
Northeast
Population (x 1,000, log)	3.572 (0.012)	1.895 (0.027)	5.467 (0.013)	2.744 (0.049)	1.389 (0.059)	4.133 (0.047)	0.332 (0.741)	0.104 (0.740)	0.436 (0.739)
GDP per capita (x 1,000 BRL)	0.345 (0.156)	0.183 (0.207)	0.528 (0.167)	0.265 (0.272)	0.134 (0.301)	0.097 (0.276)	0.032 (0.956)	0.010 (0.958)	0.042 (0.956)
Gini index (%)	0.154 (0.557)	0.082 (0.599)	0.236 (0.569)	0.106 (0.586)	0.054 (0.604)	0.160 (0.588)	0.079 (0.885)	0.025 (0.891)	0.103 (0.886)
Urbanization rate (%)	0.096 (0.299)	0.051 (0.307)	0.148 (0.295)	0.020 (0.762)	0.010 (0.776)	0.030 (0.765)	0.094 (0.347)	0.029 (0.379)	0.123 (0.350)
FHS coverage (%)				-0.078 (0.570)	-0.040 (0.555)	-0.118 (0.562)	-0.069 (0.476)	-0.022 (0.489)	-0.091 (0.476)
Radiologists ratio per 100,000 inhabitants				0.514 (0.490)	0.260 (0.519)	0.774 (0.496)	0.757 (0.191)	0.236 (0.228)	0.994 (0.193)
Mammography machines ratio per 10,000 inhabitants				1.547 (0.192)	0.783 (0.202)	2.330 (0.188)	0.951 (0.336)	0.297 (0.382)	1.248 (0.340)
Mammograms per mammography machine (x 100)							1.036 (0.000)	0.323 (0.001)	1.360 (0.000)
Central
Population (x 1,000, log)	4.946 (0.049)	2.623 (0.103)	7.569 (0.059)	1.574 (0.644)	0.797 (0.676)	2.371 (0.652)	0.575 (0.712)	0.180 (0.726)	0.755 (0.714)
GDP per capita (x 1,000 BRL)	-0.008 (0.852)	-0.004 (0.877)	-0.012 (0.859)	-0.218 (0.284)	-0.110 (0.314)	-0.328 (0.288)	-0.277 (0.231)	-0.087 (0.265)	-0.364 (0.233)
Gini index (%)	-0.036 (0.895)	-0.019 (0.884)	-0.056 (0.891)	-0.110 (0.852)	-0.056 (0.855)	-0.166 (0.852)	-0.123 (0.647)	-0.038 (0.661)	-0.161 (0.648)
Urbanization rate (%)	-0.052 (0.883)	-0.028 (0.876)	-0.079 (0.880)	0.024 (0.869)	0.012 (0.865)	0.035 (0.867)	-0.122 (0.536)	-0.038 (0.541)	-0.160 (0.534)
FHS coverage (%)				0.107 (0.425)	0.054 (0.441)	0.161 (0.427)	0.050 (0.690)	0.015 (0.672)	0.062 (0.683)
Radiologists ratio per 100,000 inhabitants				2.767 (0.003)	1.400 (0.020)	4.167 (0.004)	2.293 (0.018)	0.716 (0.074)	3.008 (0.024)
Mammography machines ratio per 10,000 inhabitants				0.624 (0.810)	0.316 (0.797)	0.940 (0.805)	0.968 (0.434)	0.302 (0.434)	1.270 (0.430)
Mammograms per mammography machine (x 100)							1.848 (0.009)	0.577 (0.033)	2.425 (0.009)
North
Population (x 1,000, log)	1.912 (0.394)	1.014 (0.413)	2.926 (0.396)	1.122 (0.584)	0.568 (0.635)	1.690 (0.599)	-0.320 (0.803)	-0.100 (0.808)	-0.420 (0.803)
GDP per capita (x 1,000 BRL)	0.153 (0.629)	0.081 (0.654)	0.234 (0.635)	0.065 (0.791)	0.033 (0.785)	0.097 (0.788)	0.052 (0.883)	0.016 (0.900)	0.068 (0.886)
Gini index (%)	-0.063 (0.942)	-0.034 (0.982)	-0.097 (0.956)	0.012 (0.997)	0.006 (0.966)	0.018 (0.987)	-0.124 (0.810)	-0.039 (0.835)	-0.162 (0.815)
Urbanization rate (%)	0.246 (0.075)	0.130 (0.108)	0.376 (0.080)	0.152 (0.383)	0.077 (0.411)	0.230 (0.390)	0.036 (0.742)	0.011 (0.756)	0.047 (0.743)
FHS coverage (%)				-0.021 (0.938)	-0.011 (0.903)	-0.032 (0.925)	-0.069 (0.474)	-0.021 (0.526)	-0.090 (0.482)
Radiologists ratio per 100,000 inhabitants				0.777 (0.641)	0.393 (0.648)	1.170 (0.641)	0.672 (0.671)	0.210 (0.665)	0.881 (0.667)
Mammography machines ratio per 10,000 inhabitants				1.663 (0.135)	0.842 (0.171)	2.505 (0.140)	2.089 (0.037)	0.652 (0.091)	2.741 (0.040)
Mammograms per mammography machine (x 100)							1.148 (0.014)	0.358 (0.041)	1.507 (0.014)

Escola Nacional de Saúde Pública Sergio Arouca, Fundação Oswaldo Cruz Rua Leopoldo Bulhões, 1480 , 21041-210 Rio de Janeiro RJ Brazil, Tel.:+55 21 2598-2511, Fax: +55 21 2598-2737 / +55 21 2598-2514 - Rio de Janeiro - RJ - Brazil
E-mail: cadernos@ensp.fiocruz.br

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[1] Correspondence M. C. Nogueira Faculdade de Medicina, Universidade Federal de Juiz de Fora. Rua Alberto Vieira Lima 357, Juiz de Fora, MG 36050-070, Brasil. mario.cirio.nogueira@gmail.com