Hospitalization and ambulatory costs related to breast cancer due to physical inactivity in the Brazilian state capitals

Diego Augusto Santos Silva

doi:10.1371/journal.pone.0261019

. 2022 Jan 19;17(1):e0261019. doi: 10.1371/journal.pone.0261019

Hospitalization and ambulatory costs related to breast cancer due to physical inactivity in the Brazilian state capitals

Diego Augusto Santos Silva ^1,^*

Editor: Muhammad Shahzad Aslam²

PMCID: PMC8769291 PMID: 35045087

Abstract

The aim of this study was to estimate the hospitalization and ambulatory costs related to breast cancer due to physical inactivity in the female population from Brazilian capitals over a three-year period (2015 to 2017). This study was carried out with data from the Brazilian health system and had as metrics incidence of breast cancer, total and standardized rate hospitalizations by breast cancer, hospitalization and ambulatory costs by breast cancer and prevalence of physical inactivity. The Population Attributable Fraction (PAF) calculation was used. The total hospitalization cost by breast cancer in women aged ≥ 20 years in Brazil from 2015 to 2017 was US$ 33,484,920.54. Of this total, US$ 182,736.76 was due to physical inactivity. Outpatient expenses related to breast cancer in the Brazilian female population from 2015 to 2017 was US$ 207,993,744.39. Of this total, US$ 1,178,841.86 was due to physical inactivity. Outpatient and hospitalization expenses were higher in the states of Southeastern, Southern and Northeastern regions. Physical inactivity has contributed to the high number of hospitalizations for breast cancer in Brazil, which resulted in economic burden for health services (inpatient and outpatient) of more than US$ 1,300,000.00 from 2015 to 2017.

Introduction

Breast cancer is the type of cancer most commonly diagnosed in the female population and in 2015, it accounted for 523,000 deaths worldwide [1, 2]. Breast cancer has multifactorial cause in which genetic and lifestyle aspects stand out [1]. Among modifiable lifestyle aspects, physical inactivity plays an important role in the prevention and treatment of this neoplasm because the regular practice of physical exercise is associated with lower concentrations of female sex hormones and lower levels of body fat [1]. Both factors (high concentrations of female sex hormones and high levels of body fat) are associated with increased risk of breast cancer, especially in postmenopausal women [1, 2]. Epidemiological surveys on breast cancer mortality due to physical inactivity estimated 29,605 deaths in 1990 and 46,720 deaths in 2015 around the world [3].

In addition to mortality estimates presented in literature, the analysis of the economic burden of breast cancer can serve to assess public policies and for governments to prioritize preventive measures in order to reduce the economic cost of this disease [4]. Data from Spain published in 2020 reported that the total cost of breast cancer in that country over a five-year period was € 469,92.73 (US$ 557,43.01) [4] (€ 1.00 = US$ 1.19 in June 18, 2021). In Mexico, cost projection of US$ 245 million was estimated for procedures related to breast cancer throughout the lives of women born in 2012 [5]. In the United States of America, 2007 data have shown total cost of US$ 12.2 billion with procedures related to breast cancer [6]. In Brazil, cost of approximately US$ 5.8 million was estimated in 2013 for hospitalizations due to breast cancer [7].

In addition to information on the global economic burden of the disease, which can be analyzed by metrics related to cost related to hospitalizations, medicines and procedures in general [6, 7], studies have prioritized making estimates by risk factors [8]. These risk factor estimates allow managers and society to become aware of how much each action in a specific risk factor would result in savings. A systematic review developed with studies published until 2014 found 24 articles that estimated the cost of physical inactivity related to various non-communicable diseases and reported that physical inactivity had high economic impact for the health sector, regardless of economic analysis metric [8]. Ding et al. [9] estimated costs of physical inactivity related to various non-communicable diseases around the world and found that in 2013, this cost was US$ 53.8 billion, of which US$ 31.2 billion were paid by the public sector. In relation to breast cancer, a survey highlighted the impact of physical inactivity on hospitalizations for breast cancer and estimated an approximate expenditure of US$ 1.2 million in a single country [7].

Brazil has continental dimensions, with evident social and economic discrepancies among states [3, 10]. These discrepancies are reflected in living conditions, lifestyles and in the quality and access to health services [10], which, in turn, reflect in the amount of care for breast cancer and the cost of each state with the treatment of the disease [3]. Thus, the estimate of the economic burden of breast cancer due to physical inactivity by Brazilian state can provide information on how each state has faced the problem of breast cancer related to physical inactivity and also can provide information on the health inequality in Brazil.

The aim of this study was to estimate the hospitalization and ambulatory cost related to breast cancer due to physical inactivity in the female population from Brazilian capitals over a three-year period (2015 to 2017).

Materials and methods

Study design

This is a cost-of-illness study to estimate the direct costs of breast cancers attributable to lack of physical activity from the perspective of the Brazilian health services. The study’s analysis units are the states of Brazil. This study was carried out with data from the Brazilian Unified Health System accessed via Department of Informatics (DATASUS) of free access and charge. For all Brazilian states, the quality of data from DATASUS is considered high and close to high-income countries [11, 12]. In addition, this study used information collected by the Ministry of Health of Brazil entitled “Surveillance System of Risk and Protection Factors of Noncommunicable Disease by Telephone Survey—VIGITEL”. This system aims to monitor health indicators of the Brazilian population aged ≥ 18 years through telephone survey and was carried out in 26 Brazilian capitals and the Federal District. Free and informed consent was obtained from all participants at the time of data collection. The VIGITEL study in Brazil protocol was approved by National Ethics Committee on Research with Human Beings (CONEP/BRAZIL), and has been conducted in full accordance with ethical principles, including provisions of the World Medical Association Declaration of Helsinki (Ethical Application Ref: 65610017.1.0000.0008).

Hospitalizations and ambulatory costs data

For the present study, malignant breast cancer was characterized according to the latest International Classification of Diseases, 10^th Revision (ICD-10). ICD-10 categories for malignant breast cancer analyzed were C50, C50.0, C50.1, C50.2, C50.3, C50.4, C50.5, C50.6, C50.8, C50.9 [13].

From the access to the DATASUS system (i.e, SIH—Hospital Admission System), information from years 2015, 2016 and 2017 on the total number of hospitalizations and the cost of these hospitalizations in the Brazilian female population aged ≥20 years was extracted [14, 15]. Outpatient procedures related to breast cancer were extracted from Outpatient Information System from DATASUS (SIA/SUS) of the years 2015, 2016 and 2017. The total cost of outpatient procedures related to breast cancer in 2015, 2016 and 2017 were related to Brazilian capitals and the Federal District. For outpatient estimates, the procedures recommended by DATASUS were considered. All outpatient procedures related to breast cancer with the respective DATASUS codes can be found in the S1 Table.

From values of years 2015, 2016 and 2017, the mean cost of hospitalizations in these three years (with standard deviation estimate) and the total cost were calculated from the sum of annual values. For international comparison, estimates in reais (R$—Brazilian currency) were converted into US dollars (US$). For this purpose, the mean value of the dollar quotation in the three years of the survey was considered (US$ 1.0 = R$ 3,33) [16].

Prevalence of physical inactivity

For estimates on the prevalence of physical inactivity in Brazilian women (aged ≥20 years), national surveys of the Surveillance System for Risk and Protective Factors for Chronic Diseases by Telephone Survey (VIGITEL) for years 2015, 2016 and 2017 were used [17–19]. Such a system was implemented in Brazil in 2006 and is consolidated as a health surveillance and management system. The sampling procedures used in this survey aim to obtain, in each capital of the 26 Brazilian states and the Federal District, probabilistic samples of the population of adults living in households served by at least one fixed telephone line. The system establishes minimum sample size of approximately 2 thousand individuals in each city to estimate, with 95% confidence coefficient and maximum error of two percentage points, the frequency of any risk factor in the adult population. Maximum errors of three percentage points are expected for specific estimates, according to sex, assuming similar proportions of men and women in the sample [17–19]. Smaller samples are accepted in locations where fixed telephone coverage is less than 40% of households and where the absolute number of households with a telephone line is less than 50 thousand. In this case, estimates for the adult population will have maximum error of three percentage points, being of four percentage points the same error for sex-specific estimates [17–19].

In 2015, 54,174 individuals were evaluated, of which 33,806 were women (n = 730 women aged 18–19 years; n = 33,076 women aged ≥ 20 years). In 2016, 53,210 individuals were evaluated, 32,952 of which were women (n = 757 women aged 18–19 years; n = 32,195 women aged ≥ 20 years). In 2017, 53,034 individuals were evaluated, of which 33,530 were women (n = 674 women aged 18–19 years; n = 32,856 women aged ≥ 20 years).

In the present study, estimates of physical inactivity were considered in all domains (leisure, transport, occupation and domestic activities). Such information is obtained through standardized questionnaire validated for the Brazilian population [20, 21]. Physically inactive were subjects who did not practice any free-time physical activity in the last three months of the interview and those who did not make intense physical efforts at work, did not commute to work or school and were not responsible for heavy cleaning of the house, as recommended in literature (e.g., they are those who have energy expenditure < 600 METS minutes/week) [22]. For these estimates, sampling weight and sampling strata were considered.

Data analysis

To estimate hospitalizations and ambulatory costs for breast cancer due to physical inactivity, the Population Attributable Fraction (PAF) calculation strategy was used, which is also used in studies on the global burden of diseases attributable to risk factors [2, 3] and in other studies that estimate the cost of physical inactivity [7–9]. This metric identifies the percentage reduction in the disease, in a given year, if the risk factor (physical inactivity) was not present. That is, if the population met the guidelines for physical activity [22]. For this, the following equation was used: PAF = {[p * (RR -1)] / [p * (RR—1) + 1]}, where ‘p’ refers to the prevalence of exposure, ‘RR’ refers to the relative risk attributed to the exposure. RR of the relationship between physical activity and breast cancer was obtained from meta-analysis that analyzed the dose-response between these variables with the inclusion of adjustment covariates based on studies with good methodological quality [23]. Kyu et al. [23] reported that women who practiced physical activity in an amount ≥ 600 MET minutes/week of total physical activity had at least a reduced risk of breast cancer by 3% compared to those who reported lower amounts of physical activity (< 600 MET minutes/week). In the present study RR considered was 1.03, which indicated the risk of breast cancer in women who did not meet physical activity recommendations of ≥ 600 METs minutes/week [22].

Information on the breast cancer was presented in absolute terms and at standardized rates by age. For the calculation of rates, the most current data from estimates of the female population aged ≥ 20 years in each of the Brazilian states and Federal District in 2015, 2016 and 2017 [24] were used. Rates were presented for a population of 100,000 inhabitants. The reference population for the calculation of standardized rates was the estimates of the Ministry of Health of Brazil according to Brazilian capitals and Federal District from 2000 to 2020 [24]. The information on the breast cancer incidence and number and age-standardized rate of hospitalizations (per 100,000 inhabitants) due to breast cancer in Brazilian women are in the S2 and S3 Tables.

All maps were built using TABNET® software (public domain software developed by the Ministry of Health of Brazil) and all images are in the public domain. All cost analyzes were performed using Microsoft Windows Excel® software (Redmond, USA).

Results

The prevalence of physical inactivity in 2015 among Brazilian women aged ≥ 20 years was 19.5%, 18.5% in 2016, and 19.0% in 2017. Table 1 shows this information according to each Brazilian state capital and Federal District.

Table 1. Prevalence of physical inactivity in women aged ≥ 20 years in 2015, 2016 and 2017, in Brazilian capitals and Federal District.

	Prevalence of physical inactivity
	2015		2016		2017
	n	%	n	%	n	%
Brazil	6,436	19.5	5,962	18.5	6,245	19.0
Aracaju	220	17.9	243	20.0	218	16.9
Belém	189	16.5	238	19.4	212	18.5
Belo Horizonte	180	15.0	184	14.9	182	15.5
Boa Vista	192	16.3	146	14.5	139	14.6
Brasília	280	23.3	199	17.2	235	20.3
Campo Grande	207	17.3	233	18.9	299	22.9
Cuiabá	261	19.6	189	15.4	243	18.6
Curitiba	169	14.7	240	19.0	266	19.1
Florianópolis	298	23.3	242	20.3	291	22.8
Fortaleza	250	20.2	248	20.3	257	20.2
Goiânia	281	20.9	190	15.5	254	19.2
João Pessoa	344	27.2	292	23.2	295	23.0
Macapá	239	20.2	201	18.2	146	17.4
Maceió	251	20.5	266	21.3	307	23.0
Manaus	213	17.6	211	18.3	164	16.4
Natal	265	21.3	275	21.9	276	22.0
Palmas	155	14.4	161	15.1	158	13.7
Porto Alegre	243	20.1	241	19.1	269	20.0
Porto Velho	189	16.1	176	16.2	142	13.5
Recife	275	21.7	284	22.0	286	21.5
Rio Branco	273	21.6	154	15.5	198	18.0
Rio de Janeiro	247	19.6	246	20.7	267	22.4
Salvador	243	19.2	215	18.0	222	17.3
São Luís	246	19.6	216	18.7	244	19.1
São Paulo	190	16.2	193	15.8	164	13.1
Teresina	229	19.1	233	19.6	247	19.8
Vitória	307	23.6	246	18.8	264	20.1

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In women aged ≥ 20 years (Fig 1), 0.56% of hospitalizations by breast cancer were attributable to physical inactivity. The highest PAF values were found in Brazilian states capitals of Northeastern region, indicating that such locations would prevent greater number of hospitalizations by breast cancer if the population practiced physical activity regularly.

The total hospitalization cost by breast cancer in women aged ≥ 20 years in Brazil from 2015 to 2017 was US$ 33,484,920.54. Of this total, US$ 182,736.76 was due to physical inactivity. The cities of São Paulo (US$ 35,299.72) and Rio de Janeiro (US$ 22,312.10) were those with the highest hospitalization costs by breast cancer due to physical inactivity (Table 2).

Table 2. Cost of hospitalizations for breast cancer in women aged ≥ 20 years in Brazil and in the Brazilian state capitals in 2015, 2016 and 2017.

Total cost of hospitalizations by breast cancer (US$)					Total cost of hospitalizations by breast cancer due to physical inactivity (US$)
US$	2015	2016	2017	Total	2015	2016	2017	Total
Brazil	10,687,409.88	11,160,469.79	11,637,040.87	33,484,920.54	59,139.83	60,474.44	63,122.49	182,736.76
Aracaju	24,433.87	41,704.48	51,028.93	117,167.27	130.51	248.73	257.41	636.66
Belém	137,356.49	145,082.04	171,264.34	453,702.87	676.57	839.49	945.27	2,461.33
Belo Horizonte	723,850.97	827,838.24	949,217.32	2,500,906.54	3,242.74	3,683.97	4,393.43	11,320.14
Boa Vista	17,373.53	22,365.80	17,984.40	57,723.73	84.54	96.87	78.43	259.84
Brasília	269,751.76	317,052.65	351,963.39	938,767.80	1,872.48	1,627.59	2,130.48	5,630.55
Campo Grande	223,031.22	290,247.48	275,857.40	789,136.11	1,151.56	1,636.42	1,882.21	4,670.19
Cuiabá	105,468.38	113,445.33	102,924.48	321,838.20	616.53	521.71	571.13	1,709.37
Curitiba	376,940.91	492,409.52	571,581.44	1,440,931.87	1,655.01	2,790.83	3,256.50	7,702.34
Florianópolis	63,258.25	77,592.75	55,494.16	196,345.16	439.11	469.68	377.00	1,285.79
Fortaleza	740,583.44	711,142.95	790,174.54	2,241,900.93	4,460.90	4,304.65	4,759.61	13,525.16
Goiânia	286,867.08	425,047.94	453,219.55	1,165,134.58	1,787.45	1,967.32	2,595.59	6,350.37
João Pessoa	189,502.17	184,655.63	261,043.64	635,201.44	1,533.82	1,276.32	1,788.86	4,599.00
Macapá	9,766.56	11,210.53	19,530.33	40,507.42	58.83	60.88	101.42	221.12
Maceió	153,443.99	158,188.56	272,727.25	584,359.80	937.91	1,004.41	1,868.92	3,811.24
Manaus	127,671.93	155,408.36	193,623.29	476,703.59	670.57	848.53	947.96	2,467.06
Natal	285,511.46	224,746.88	278,327.82	788,586.16	1,812.83	1,466.95	1,824.92	5,104.70
Palmas	30,588.30	25,251.58	27,157.71	82,997.59	131.57	113.87	111.16	356.61
Porto Alegre	421,819.56	416,269.32	462,820.66	1,300,909.54	2,528.33	2,371.63	2,760.36	7,660.32
Porto Velho	91,802.98	81,444.69	77,610.60	250,858.27	441.28	393.91	313.06	1,148.24
Recife	470,599.54	554,286.63	569,218.83	1,594,105.00	3,043.79	3,634.31	3,647.93	10,326.03
Rio Branco	17,565.87	17,162.55	28,558.37	63,286.79	113.09	79.44	153.39	345.92
Rio de Janeiro	1,169,287.67	1,249,706.18	1,163,136.18	3,582,130.03	6,835.22	7,712.78	7,764.10	22,312.10
Salvador	1,366,024.00	1,394,854.46	1,256,897.95	4,017,776.41	7,823.24	7,491.76	6,489.62	21,804.61
São Luís	276,954.14	319,646.21	391,882.16	988,482.51	1,618.97	1,783.21	2,232.69	5,634.87
São Paulo	2,788,745.33	2,566,806.08	2,478,585.57	7,834,136.97	13,487.75	12,109.26	9,702.71	35,299.72
Teresina	194,228.08	212,597.46	232,800.02	639,625.56	1,106.59	1,242.77	1,374.67	3,724.02
Vitória	124,982.35	124,305.50	132,410.56	381,698.41	878.65	697.15	793.65	2,369.46

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Note. US$: US American Dollar; US$ 1.00 = R$ 0.30 (R$ = Brazilian currency; mean of Brazilian currency from the values of 2015, 2016 and 2017).

The total ambulatory cost by breast cancer in women aged ≥ 20 years in Brazil from 2015 to 2017 was US$ 207,993,744.39. Of this total, US$ 1,178,841.86 was due to physical inactivity. The cities of São Paulo (US$ 188,863.22) and Rio de Janeiro (US$ 108,470.77) were those with the highest ambulatory costs by breast cancer due to physical inactivity (Table 3).

Table 3. Ambulatory costs by breast cancer in women aged ≥ 20 years in Brazil and in the Brazilian state capitals in 2015, 2016 and 2017.

Total ambulatory costs by breast cancer (US$)					Total ambulatory costs by breast cancer due to physical inactivity (US$)
	2015	2016	2017	Total	2015	2016	2017	Total
Brazil	66,547,706.20	69,002,663.12	72,443,375.07	207,993,744.39	387,039.90	380,851.06	410,586.89	1,178,841.86
Aracaju	731,229.11	736,308.54	615,406.45	2,082,944.10	3,905.73	4,391.50	3,104.37	11,352.02
Belém	1,248,804.85	1,319,497.61	1,544,688.94	4,112,991.40	6,151.14	7,635.04	8,525.71	22,253.08
Belo Horizonte	4,972,864.31	4,921,002.28	5,010,042.61	14,903,909.20	22,277.64	21,898.99	23,188.87	67,357.85
Boa Vista	67,924.96	22,979.44	34,476.93	125,381.33	330.54	99.53	150.35	566.65
Brasília	1,078,406.68	1,086,120.73	1,606,007.16	3,770,534.57	7,485.74	5,575.61	9,721.38	22,784.24
Campo Grande	859,786.03	937,151.23	940,776.37	2,737,713.63	4,439.25	5,283.69	6,419.03	16,083.48
Cuiabá	892,048.62	980,317.14	1,016,485.73	2,888,851.49	5,214.58	4,508.24	5,640.52	15,400.87
Curitiba	2,674,829.92	2,908,246.71	3,041,053.24	8,624,129.87	11,744.21	16,483.05	17,325.96	45,293.03
Florianópolis	1,253,623.04	1,233,554.91	1,147,228.79	3,634,406.74	8,702.00	7,466.88	7,793.74	23,972.73
Fortaleza	5,200,153.99	5,587,967.46	6,134,968.34	16,923,089.79	31,323.12	33,824.73	36,953.97	102,103.38
Goiânia	2,151,199.73	2,298,807.51	2,377,009.61	6,827,016.84	13,403.98	10,639.98	13,613.16	37,745.26
João Pessoa	1,805,978.56	2,005,025.13	2,157,376.76	5,968,380.46	14,617.51	13,858.52	14,783.89	43,486.74
Macapá	111,748.00	142,659.86	178,204.74	432,612.61	673.11	774.69	925.40	2,400.53
Maceió	1,407,712.73	1,485,944.45	1,693,152.97	4,586,810.15	8,604.52	9,434.90	11,602.70	29,530.73
Manaus	891,367.71	1,082,569.23	1,176,336.00	3,150,272.94	4,681.70	5,910.85	5,759.24	16,390.03
Natal	2,106,787.06	2,046,843.62	2,154,155.01	6,307,785.69	13,376.89	13,359.99	14,124.20	40,860.30
Palmas	266,723.25	253,058.84	254,619.66	774,401.76	1,147.29	1,141.19	1,042.20	3,331.00
Porto Alegre	4,043,633.64	4,123,004.19	4,037,748.02	12,204,385.85	24,236.96	23,490.22	24,082.00	71,824.54
Porto Velho	152,735.42	132,343.52	171,541.64	456,620.58	734.17	640.08	691.94	2,081.72
Recife	4,887,193.05	5,372,720.77	5,862,159.59	16,122,073.42	31,609.85	35,227.46	37,568.61	104,434.94
Rio Branco	197,607.49	185,564.56	224,504.01	607,676.06	1,272.25	858.88	1,205.81	3,329.61
Rio de Janeiro	5,423,314.09	5,930,128.16	6,055,319.38	17,408,761.63	31,702.68	36,598.82	40,420.12	108,470.77
Salvador	4,523,782.30	4,357,461.56	4,918,953.59	13,800,197.45	25,907.76	23,403.91	25,397.56	74,802.65
São Luís	1,644,602.43	1,907,067.35	2,051,813.91	5,603,483.70	9,613.73	10,638.96	11,689.91	31,980.36
São Paulo	14,111,844.97	13,831,915.51	14,123,226.21	42,066,986.69	68,251.86	65,253.98	55,287.00	188,863.22
Teresina	1,541,923.70	1,807,941.17	1,696,560.69	5,046,425.56	8,784.89	10,568.55	10,018.06	29,349.85
Vitória	2,299,880.55	2,306,461.65	2,219,558.71	6,825,900.90	16,168.68	12,935.49	13,303.72	42,394.42

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Note. US$: US American Dollar; US$ 1.00 = R$ 0.30 (R$ = Brazilian currency; mean of Brazilian currency from the values of 2015, 2016 and 2017).

The mean hospitalization cost for breast cancer due to physical inactivity in the period from 2015 to 2017 among women aged ≥ 20 years was US$ 69,912.25 (± 2,027.11) and this cost was higher in the Brazilian states of Southeastern, Southern and Northeastern regions (Fig 2).

Fig 2 — All maps were built using TABNET® software (public domain software developed by the Ministry of Health of Brazil) and all images are in the public domain. US$: US American Dollar; US$ 1.00 = R$ 0.30 (R$ = Brazilian currency; mean of Brazilian currency from the values of 2015, 2016 and 2017).

The mean ambulatory cost for breast cancer due to physical inactivity in the period from 2015 to 2017 among women aged ≥ 20 years was US$ 386,201.63 (± 12,553.33) and this cost was higher in the Brazilian states of Southeastern, Southern and Northeastern regions (Fig 3).

Fig 3 — All maps were built using TABNET® software (public domain software developed by the Ministry of Health of Brazil) and all images are in the public domain. US$: US American Dollar; US$ 1.00 = R$ 0.30 (R$ = Brazilian currency; mean of Brazilian currency from the values of 2015, 2016 and 2017).

Discussion

The economic burden of physical inactivity was studied by authors from different countries who found high costs for health systems due to physical inactivity [25–27]. Most of these studies associated physical inactivity to costs due to cardiovascular disease or diabetes [25–27] and few estimated costs due to breast cancer [7, 9]. The few studies that associated costs to breast cancer were focused on leisure-time physical inactivity [7] and not with physical inactivity in all domains (leisure, transport, domestic activities, work), as was the case in the present study. The estimate of physical inactivity in all domains is important because depending on contextual and social characteristics, the population can be physically active in one domain and not in another [28, 29]. In this sense, estimates of physical inactivity in only one domain may overestimate the economic burden of physical inactivity due to a given chronic disease.

The present study found that from 2015 to 2017, US$ 182,736.76 (annual mean value of US$ 69,912.25) were spent on hospitalizations for breast cancer due to physical inactivity in women aged ≥ 20 years. The ambulatory cost for breast cancer due to physical inactivity from 2015 to 2017 was US$ 1,178,841.86 (average annual value of US$ 386,201.63). These values reflected a total cost of more than US$ 1,361,578.62 in three years due to physical inactivity in Brazil. The Brazilian government developed the “Academia da Saúde” Program, which is a community program whose objective is to promote physical activity, healthy eating, health education, contributing to the production of care and healthy and sustainable ways of life for the population. To this end, the Program promotes the implementation of public spaces with infrastructure, equipment and qualified professionals [30]. The practice of physical activity is one of the main actions of the program and the entire Brazilian population living in cities where the program has been implemented can participate free of charge [30]. The cost for the implementation of this program varies from R$ 80,000.00 (US$ 15,822.49) to R$ 180.000,00 (US$ 35,600.60) and has the capacity to serve the entire population of cities [30]. That is, the cost for cities to implement community-based programs to promote physical activity is lower than the hospitalization cost for breast cancer due to physical inactivity shown in the present study.

The discussion on the costs of physical inactivity must be done in different countries and about the different contexts of physical activity. The development of programs to promote physical activity in workplaces can also be effective in increasing the levels of physical activity in the population, especially in the adult population that spends most of the day at work [31] and thus can be a strategy for governments to lower the costs of physical inactivity. Lutz et al. [31] developed a systematic review of programs aimed at promoting physical activity in the workplace and estimated the costs of these programs. Of the 16 studies that estimated the costs of implementing this type of program, an average cost per person of € 174.00 was reported, which is equivalent to approximately US$ 206.40 (€ 1.00 = US$ 1.19 in June 18, 2021). In other words, with estimated cost of US$ 206.40 per person in the work environment, physical activity promotion programs can be implemented, which will prevent breast cancer and other non-communicable diseases and conditions and will consequently reduce the economic burden of hospitalizations due to physical inactivity.

The present study found that in Brazilian women aged ≥ 20 years, 0.56% of hospitalizations for breast cancer could be avoided with the regular practice of physical activities. These results reinforce the beneficial effect of the practice of physical activity for the prevention of breast cancer in all age groups, mainly because the practice of physical activity causes changes in female sex hormones (estrogens and progesterone) and in body fat, factors that are related to higher risk of breast cancer [32].

The Brazilian capitals of Northeastern region showed the highest PAF values, indicating that such locations would prevent greater number of hospitalizations by breast cancer if the population practiced physical activity on a regular basis. This information is useful in terms of public health because these capitals are those with the worst economic and social indicators, which also reflects in worse levels of quality and access to health services [3]. In addition, all the Brazilian capitals could save inpatient and outpatient resources if the population were physically active. Thus, increasing the level of physical activity of the population across the country would have a beneficial effect in reducing hospitalizations by breast cancer, which would bring important economic results to these locations, also preventing women from being hospitalized.

The present study developed an analysis of the hospitalization and ambulatory cost by breast cancer. This analysis is one of the possible analyzes for estimating the economic burden of a disease [7]. The cost analysis can only be estimated from variables with measurable values and, therefore, can be accounted for, as is the case with hospitalization. However, regular physical activity can provide numerous health benefits, such as its effects on the reduction in the use of medications [33], and in recovering from some illnesses [34]. Therefore, higher levels of physical activity in the population promote positive effects on economy and health.

There is a lot of debate in the literature about the effect of physical activity on the prevention of breast cancer before and after menopause [35–37]. All health agencies reinforce that the effect of physical activity in preventing breast cancer is more evident after menopause. However, before menopause there is a theoretical discussion that still needs consensus. The World Cancer Research Fund report describes that the strongest evidence that exists in the relationship between physical activity and breast cancer prevention is for women after menopause [35]. Physical activity guidelines describe that there is strong evidence that physical activity prevents breast cancer before and after menopause [36, 37]. The present study adopted the recommendations of the physical activity guidelines because they were the most recent on the subject. In addition, in the present study was used a reference for PAF that which investigated adult and older adults women [23].

This study has several limitations, such as the estimation of hospitalization and ambulatory costs only for breast cancer. Physical inactivity is associated with other health problems that were not investigated in the present study [23], that is, the cost of physical inactivity for the health sector is significantly higher than that estimated in this research. Thus, the results of this study on the economic burden of physical inactivity are much more worrying. Another limitation of this study is the non-stratification of hospitalizations by types of breast cancer and the non-exclusion of hospitalizations due to genetic mutations, as there are types of breast cancer that are more related to lifestyle than others [38]. This study developed analyses at level of Brazilian capitals, and not at level of states. The strategy used in the present study limits the identification of which states or other cities of the Brazil have high hospitalization and ambulatory costs due to physical inactivity and which would need to invest more in physical activity programs in primary care. The decision to analyze the capitals of Brazil and the Federal District was made because the survey of physical activity that is carried out in Brazil annually is carried out in Brazilian capitals and in the Federal District [17–19]. In addition, another limitation is the temporal difference between exposure to the risk factor and the outcome. We used a RR to estimate the attributable fraction from a systematic review that led to studies conducted in developed countries and this is another limitation. The study of ecological design is not free from the ecological fallacy. Finally, estimates of physical inactivity in the present study came from surveys that used self-reported physical activity measures, which are less accurate than objective measures [39].

Conclusions

It could be concluded that physical inactivity has contributed to high number of hospitalizations by breast cancer in Brazilian female population, which resulted in cost of more than US$ 182,700.00 from 2015 to 2017 for health services. In addition, the ambulatory cost for breast cancer due to physical inactivity from 2015 to 2017 was US$ 1,178,841.86. These values reflected a total cost of more than US$ 1,300,000.00 in three years due to physical inactivity in Brazil. Thus, the promotion of physical activity in the Brazilian female population would bring economic benefits for all geographic regions.

Supporting information

S1 Table. Description of outpatient procedures on breast cancer applied in Brazil.

DATASUS (2015, 2016 and 2017).

(DOC)

Click here for additional data file.^{(31.5KB, doc)}

S2 Table. Incidence of breast cancer among women in Brazilian state capitals and Federal District (aged ≥ 20 years).

*rate per 100,000 inhabitants. Reference population: Reference population: women residing in each capital for each year (aged ≥ 20 years).

(DOC)

Click here for additional data file.^{(66KB, doc)}

S3 Table. Number and age-standardized rate of hospitalizations (per 100,000 inhabitants) due to breast cancer in women aged ≥ 20 years in 2015, 2016 and 2017, in Brazil and in the Brazilian state capitals.

*Age-standardized (per 100,000 inhabitants).

(DOC)

Click here for additional data file.^{(59KB, doc)}

Data Availability

All data are publicly available by Brazilian Unified Health System accessed via Department of Informatics (DATASUS) of free access and charge: https://datasus.saude.gov.br/informacoes-de-saude-tabnet/. The authors did not have any special access privileges that others would not have.

Funding Statement

The author(s) received no specific funding for this work.

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PLoS One. doi: 10.1371/journal.pone.0261019.r001

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The economic burden of breast cancer due to physical inactivity in Brazil

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Reviewer #1: The manuscript "The economic burden of breast cancer due to physical inactivity in Brazil" study the economic impact of physical inactivity and breast cancer to Brazilian healthcare system. The study has merit and was written. However, I have some comments to the author.

Major comments:

1) There is only one author in the study? If is true, the sentence “These authors contributed equally to this work” in the first page make no sense.

2) The correlation between mean hospitalization cost and healthcare quality and access index is weak both in women aged 20-59 years and in those aged ≥60 years (rho = 0.37, p = 0.04 and rho = 0.43, p = 0.02) (figure 1 and 2). Besides some Brazilian estates showed a higher cost and higher access index, this is not direct correlated in the country. This should be clear in results and discussion.

3) In the discussion, lines 353 to 355 “The cost for the implementation of this program varies from R$ 80.000,00 (US$ 266,400.00) to R$ 180.000,00 (US$ 599,400.00) and ….”. The values in Real and Dollar should be revised in this sentence and perhaps in all text.

Minor comments:

1) Values of rho and p should be corrected. For instance: rho = .37, p = .04 to rho= 0.37, p = 0.04

Reviewer #2: I found that the article is well written. The content is interesting and well elaborated.

I found same minor errors that should be seen.

LIne 62 probably the number in euros is wrongly written.

Line 185 the term PAF was used in line 251 the term FAP was used for the same meaning

Line 342 is this phrase correct?

would be € 133,074, which is equivalent to approximately US$ 151,000,000

Line 354

implementation of this program varies from R$ 80.000,00 (US$ 266,400.00) to R$ 354 180.000,00 (US$ 599,400.00)

Reviewer #3: The study is important to added the information about the correlation about a breast cancer and economic costs in populous country such as brazil. The Datasus is a main source of data health from Brazilian`s population. This study have not study design, and the authors did not declare the conflict of interest.

Please see attachment.

Reviewer #4: General comments: The article has an exciting and very current theme. Economic analyzes in low- and middle-income countries are always welcome. Three methodological issues are central. The first question refers to the option of the authors to use a survey of the prevalence of risk factors that is not nationally representative to build a fraction attributable to be applied nationally. The second question concerns using only direct hospital expenses and highlighting in the title that an analysis of the economic burden is a broad concept. The third and last concerns the questionable contribution of the correlation analysis between attributable expenditure and the Healthcare Access and Quality (HAQ) Index.

Specific comments: 1. Although the article's title refers to economic burden in Brazil, data from Vigitel were used, which is a telephone survey with representation only for the 26 capitals and DF and not for Brazil; 2. The economic burden seems a broad term. The author only analyzed the hospital expenses of the public health system; 3. It was unclear why choosing the analysis period between 2015 and 2017; 4. It was also unclear why analyzing the correlation between expenditures and conditions of access and quality of services (HAQ) in the states; 4. It seems that the approval of CONEP was from the telephone survey research (Vigitel) and not from the study carried out; 5.What is the purpose of calculating the standardized rate of hospitalization for breast cancer; 6. the value of RR 1.40 used was not found in the reference text; 7. The example used in the discussion (lines 336-344) does not seem suitable for the discussion section once it was a foreign factual experience; 8. Review the dollar amounts in lines 352-355; 9. The reference used in lines 358-370 also does not seem adequate since an analysis of the attributable fraction of expenses by type (recreational, occupational, transport, at home) was not performed. The values marked in the article were not found in the original 10. Clarify the justification pointed out in lines 408-412; 11. The quality of life and mental well-being are considered non-measurable; why? Lines 412-416; 12. In the study's limitations, there was no mention of the issue of temporal GAP between exposure to the risk factor and the outcome. This question has not been considered, although other research groups on attributable fraction consider it very relevant; 13. I could not access reference #38, review doi; 14. Lines 425-426 reinforce that attributable expenditures were carried out using prevalence data from the state's capitals. Wouldn't that be a limitation? 15. No analysis was made of the correlation between expenditure attributable to physical inactivity and the HAQ index. Why? since the rho values are relatively low.

Reviewer #5: The introduction section is so long. Along the stretch between 62 and 81 lines are highlighted some studies with cost estimates widely different, limiting the cross-countries comparison. Sugiro excluir a maior parte e/ou transferir uma parte para a discussão. I suggest deleting most of this and/or transferring a part to the discussion.

It is not clear which is the study design.

The authors argue that “For all Brazilian states, the quality of data from DATASUS is considered high and close to high-income countries”. However, several authors suggest which coverage and quality of the North Brazilian region datasets is poor in regard south region, for example (Please, check this manuscripts: https://pubmed.ncbi.nlm.nih.gov/31800858/; https://pubmed.ncbi.nlm.nih.gov/31859881/).

Please consider exclude the following stretch “All DATASUS information follows the ethical precepts of the Declaration of Helsinki, so that users' anonymity is respected.”, because the study is based in secondary data.

How the authors dealt with the number of readmissions?

If the quality of data from DATASUS is considered high in Brazil why the authors did not use the breast cancer Brazilian estimates?

The Healthcare Access and Quality (HAQ) Index may have been influenced by the poor-quality data of the north region cities. Are the north region estimates reliable?

Reviewer #6: This study highlights an important topic on the impact of physical inactivity on hospitalization costs due to breast cancer, through secondary analysis of national databases. The study aimed “to estimate the economic burden of breast cancer due to physical inactivity in the Brazilian female population over a three-year period (2015 to 2017) and to relate these costs to conditions of access and quality of health services in Brazilian states”.

I have several major and some minor observations.

1) A first concern is using the VIGITEL database to estimate the prevalence of physical inactivity of Brazilians. This database is restricted to the Brazilian population aged ≥ 18 years living in households served by at least one fixed telephone line in 26 Brazilian capitals and the Federal District. Then, it is not representative of the Brazilian population, primarily because the exposure investigated (physical activity) can differ significantly between female residents of capitals and other cities in the country. The title, abstract, analyses, results, and conclusion should be revised to attend to this particularity.

2) In the Abstract, the author stated that the “Population Attributable Fraction” (PAF) was calculated but did not present the results, an important result of this study.

3) In the Introduction (lines 61-67), it stated some cost estimates of breast cancer in different countries and, importantly, in different points of time (from 2007 to 2020). This difference in time could be influencing in the estimates presented. I suggest considering presenting more current data and standardize the values in dollars.

4) In the Methods (lines 97-112), the databases used in the present study should be presented more clearly. Which data were obtained from DATAUS (SIH?) and which data were obtained from VIGITEL surveys? Are DATASUS and VIGITEL different databases with specific aims?

5) In lines 99-100, the author stated that “the quality of data from DATASUS is considered high and close to high-income countries”, but the references used to support this claim (11,12) deal whit mortality statistics' information, not included in this study. Please review this claim and references.

6) In lines 129-132, it is stated the data extracted from the DATASUS (total number of hospitalizations and the cost of these hospitalizations in the Brazilian female population aged 20-59 years and ≥60 years, according to year). In lines 325-326, the author informs that analyses were conducted at the country's geographic region and states and not at municipality level. It is unclear to me why the analyses were not restricted to 26 Brazilian capitals and the Federal District?

7) The RR used to estimate the attributable fraction was taken from a systematic review (Kyu 2013) (lines 192-195) that led to studies conducted in developed countries with populations different from the Brazilian one (United States, Canada, European countries, Japan and China). This limitation should be pointed out in the discussion.

8) Please consider presenting the results by capitals and Federal District, not by Brazilian states.

9) Lines 299-300. The statistic used (Spearman's correlation coefficient) was not described in the Method.

10) In lines 320-321, it is stated that “few estimated costs due to breast cancer [7]”. Please consider to cite other studies, such as Ding, 2016 (ref 9).

11) In lines 366-370, the author stated that “[…] physical activity promotion programs can be implemented, which will prevent breast cancer and other non-communicable diseases and conditions.” Despite the recognized importance of these programs, they do not guarantee the prevention of all breast cancer cases, given the existence of other risk factors for the disease.

12) It would be great if the author could include a limitation about the susceptibility of the analysis conducted in the present study to ecological fallacy.

13) Please change FAP (lines 251 and 379) by PAF.

**********

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Reviewer #1: No

Reviewer #2: Yes: João Pedreira Duprat Neto

Reviewer #3: Yes: Jonas Baltazar Daniel ( Biologist, MSc Nutrition Food & Health, PhD candidate -Public Health)

Reviewer #4: No

Reviewer #5: No

Reviewer #6: No

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Attachment

Submitted filename: PONE-D-21-09895_reviewer_19.05.21 to send.pdf

Click here for additional data file.^{(1.3MB, pdf)}

PLoS One. 2022 Jan 19;17(1):e0261019. doi: 10.1371/journal.pone.0261019.r002

Author response to Decision Letter 0

24 Jun 2021

Reviewer #1:

The manuscript "The economic burden of breast cancer due to physical inactivity in Brazil" study the economic impact of physical inactivity and breast cancer to Brazilian healthcare system. The study has merit and was written. However, I have some comments to the author.

Authors: We really appreciate your comments on the article.

Reviewer #1:

Major comments:

1) There is only one author in the study? If is true, the sentence “These authors contributed equally to this work” in the first page make no sense.

Authors: The article has only one author. In the new version of the article the sentence was corrected to "This author contributed to all the work”.

Reviewer #1:

Authors: We really appreciate your comments. In the new version of the article we only added information about Brazilian capitals as suggested by other reviewers. These new data demonstrated that there was no relationship between mean hospitalization cost and healthcare quality and access index. In addition, in discussion section we added the information: “The Brazilian states of Northern and Northeastern regions showed the highest PAF values, indicating that such locations would prevent greater number of hospitalizations by breast cancer if the population practiced physical activity on a regular basis. In addition, the present study found that Brazilian capitals with lower values of Healthcare Quality and Access index had a higher percentage of hospitalizations by breast cancer due to physical inactivity. This information is useful in terms of public health because these geographical regions are those with the worst economic and social indicators, which also reflects in worse levels of quality and access to health services [3]. Thus, increasing the level of physical activity of the population in these geographic regions would have a beneficial effect in reducing hospitalizations by breast cancer, which would bring important economic results to these locations, also preventing women from being hospitalized and not having the adequate care and treatment for breast cancer, as these locations are those with poor infrastructure and fewer health professionals to serve the population compared to other Brazilian regions [3]”.

Reviewer #1:

Authors: The change was made: “…The cost for the implementation of this program varies from R$ 80,000.00 (US$ 15,822.49) to R$ 180.000,00 (US$ 35,600.60)…”.

Reviewer #1:

Minor comments:

1) Values of rho and p should be corrected. For instance: rho = .37, p = .04 to rho= 0.37, p = 0.04

Authors: The change was made.

Reviewer #2: I found that the article is well written. The content is interesting and well elaborated.

I found same minor errors that should be seen.

Authors: We really appreciate your comments on the article.

Reviewer #2:

Line 62 probably the number in euros is wrongly written.

Authors: The change was made

Reviewer #2:

Line 185 the term PAF was used in line 251 the term FAP was used for the same meaning

Authors: In the new version of the paper we put all terms as “PAF”.

Reviewer #2:

Line 342 is this phrase correct?

would be € 133,074, which is equivalent to approximately US$ 151,000,000

The authors estimated different cost scenarios and reported that the highest estimated cost would be € 133,074.00, which is equivalent to approximately Authors: In the new version of the paper we correct the information: “…The authors estimated different cost scenarios and reported that the highest estimated cost would be € 133,074.00, which is equivalent to approximately US$ 162,040.00 [33] (€ 1.00 = US$ 1.22 in June 10, 2021)…”.

Reviewer #2:

Line 354

implementation of this program varies from R$ 80.000,00 (US$ 266,400.00) to R$ 354 180.000,00 (US$ 599,400.00)

Authors: In the new version of the paper we correct the information: “…The cost for the implementation of this program varies from R$ 80,000.00 (US$ 15,822.49) to R$ 180.000,00 (US$ 35,600.60) and has the capacity to serve the entire population of cities…”.

Reviewer #3:

The study is important to added the information about the correlation about a breast cancer and economic costs in populous country such as brazil. The Datasus is a main source of data health from Brazilian`s population. This study have not study design, and the authors did not declare the conflict of interest.

Please see attachment.

Authors: We really appreciate your comments on the article.

Reviewer #4:

General comments: The article has an exciting and very current theme. Economic analyzes in low- and middle-income countries are always welcome. Three methodological issues are central. The first question refers to the option of the authors to use a survey of the prevalence of risk factors that is not nationally representative to build a fraction attributable to be applied nationally. The second question concerns using only direct hospital expenses and highlighting in the title that an analysis of the economic burden is a broad concept. The third and last concerns the questionable contribution of the correlation analysis between attributable expenditure and the Healthcare Access and Quality (HAQ) Index.

Authors: We really appreciate your comments on the article. We agree that it is a limitation of the article to investigate only Brazilian capitals. This information was added in the discussion section as a limitation: “…This study developed analyses at level of Brazilian states capitals, and not at level of states. The strategy used in the present study limits the identification of which states or other cities of the Brazil have high hospitalization costs due to physical inactivity and which would need to invest more in physical activity programs in primary care...”.

In the new version of the paper we changed the title and the aim of this study.

Title: Hospitalization cost related to breast cancer due to physical inactivity in the Brazilian state capitals; Objective: to estimate the hospitalization cost related to breast cancer due to physical inactivity in the Brazilian states capitals over a three-year period (2015 to 2017) and to relate these costs to conditions of access and quality of health services in Brazilian states.

Reviewer #4:

Authors: We really appreciate your comments on the article. We agree that it is a limitation of the article to investigate only Brazilian capitals. Because of that we changed all the results. In addition, this information was added in the discussion section as a limitation: “…This study developed analyses at level of Brazilian states capitals, and not at level of states. The strategy used in the present study limits the identification of which states or other cities of the Brazil have high hospitalization costs due to physical inactivity and which would need to invest more in physical activity programs in primary care...”.

Reviewer #4:

2. The economic burden seems a broad term. The author only analyzed the hospital expenses of the public health system;

Authors: In the new version of the paper we changed the title and the aim of this study.

Reviewer #4:

3. It was unclear why choosing the analysis period between 2015 and 2017;

Authors: We chose these years because they are the years with data consolidated in DATASUS. The most recent data available in DATASUS (2018, 2019 and 2020) are still in the process of consolidation by the national system.

Reviewer #4:

4. It was also unclear why analyzing the correlation between expenditures and conditions of access and quality of services (HAQ) in the states;

Authors: In the new version of the article we added new correlations between percentage of hospitalizations for breast cancer due to physical inactivity and the Healthcare Quality and Access index. The information allowed progress in the discussions of the article.

Reviewer #4:

4. It seems that the approval of CONEP was from the telephone survey research (Vigitel) and not from the study carried out;

Authors: The data collected directly from people was from VIGITEL, because of that the Ethics Committee was referring to this research. DATASUS data are secondary and free to access.

Reviewer #4:

5.What is the purpose of calculating the standardized rate of hospitalization for breast cancer;

Authors: It is important to calculate the standardized rate because the standardized rate takes into account the population of the city. If the rate is not standardized, the information will not be real for the population of interest (Please visit:

https://www.cdc.gov/cancer/uscs/technical_notes/stat_methods/rates.htm#:~:text=Crude%20rates%20are%20influenced%20by,cancers%20increase%20with%20increasing%20age).

Reviewer #4:

6. the value of RR 1.40 used was not found in the reference text;

Authors: In the new version of the paper we changed the RR. RR of the relationship between physical activity and breast cancer was obtained from meta-analysis that analyzed the dose-response between these variables with the inclusion of adjustment covariates based on studies with good methodological quality (Kyu et al, 2016). Kyu et al. (2016) reported that women who practiced physical activity in an amount ≥ 600 MET minutes/week of total physical activity had at least a reduced risk of breast cancer by 3% compared to those who reported lower amounts of physical activity. In the present study RR considered was 1.03, which indicated the risk of breast cancer in women who did not meet physical activity recommendations of 600 METs minutes/week.

Reviewer #4:

7. The example used in the discussion (lines 336-344) does not seem suitable for the discussion section once it was a foreign factual experience;

Authors: In the new version of the paper we removed the Germany article from the discussion.

Reviewer #4:

8. Review the dollar amounts in lines 352-355;

Authors: The change was made.

Reviewer #4:

9. The reference used in lines 358-370 also does not seem adequate since an analysis of the attributable fraction of expenses by type (recreational, occupational, transport, at home) was not performed. The values marked in the article were not found in the original

Authors: In the new version of the paper we kept the article in the discussion section because it brings a debate about the implementation of physical activity programs in other contexts, which can be a strategy to be used in Brazil.

The value marked in our research is in the pag. 135 of the paper of Lutz et al. (2020).

- Lutz N, Clarys P, Koenig I, Deliens T, Taeymans J, Verhaeghe N. Health economic evaluations of interventions to increase physical activity and decrease sedentary behavior at the workplace: a systematic review. Scand J Work Environ Health. 2020;46(2):127-42. doi: https://doi.org/10.5271/sjweh.3871

Reviewer #4:

10. Clarify the justification pointed out in lines 408-412; 11. The quality of life and mental well-being are considered non-measurable; why? Lines 412-416;

Authors: We really appreciate your comments on the article. In the new version of the paper we changed this paragraph: “...The present study developed an analysis of the hospitalization cost by breast cancer. This analysis is one of the possible analyzes for estimating the economic burden of a disease [7]. The cost analysis can only be estimated from variables with measurable values and, therefore, can be accounted for, as is the case with hospitalization. However, regular physical activity can provide numerous health benefits, such as its effects on the reduction in the use of medications [38], and in recovering from some illnesses [39]. Therefore, higher levels of physical activity in the population promote positive effects on economy and health…”.

Reviewer #4:

12. In the study's limitations, there was no mention of the issue of temporal GAP between exposure to the risk factor and the outcome. This question has not been considered, although other research groups on attributable fraction consider it very relevant.

Authors: In the new version of the paper we added this limitation.

Reviewer #4:

13. I could not access reference #38, review doi

Authors: The change was made.

Reviewer #4:

14. Lines 425-426 reinforce that attributable expenditures were carried out using prevalence data from the state's capitals. Wouldn't that be a limitation?

Authors: In the new version of the paper all the information was from state’s capitals.

Reviewer #4:

15. No analysis was made of the correlation between expenditure attributable to physical inactivity and the HAQ index. Why? since the rho values are relatively low.

Reviewer #5:

The introduction section is so long. Along the stretch between 62 and 81 lines are highlighted some studies with cost estimates widely different, limiting the cross-countries comparison. Sugiro excluir a maior parte e/ou transferir uma parte para a discussão. I suggest deleting most of this and/or transferring a part to the discussion.

Authors: The different reviewers of the paper have debated the different sections of the research. We have chosen to keep the introduction information because, along with other reviewers, we understand that it is important for the reader to bring information from previous studies about the costs of physical inactivity.

Reviewer #5:

It is not clear which is the study design.

Authors: Our paper is an ecological study. We added the information on the method section.

Reviewer #5:

Authors: The quality of data from DATASUS is considered high and close to high-income countries. I understand that some information still needs further improvement and it does need to improve. However, DATASUS is a quality system whose data is important for Brazil.

Reviewer #5:

Authors: The change was made.

Reviewer #5:

How the authors dealt with the number of readmissions?

Authors: We do not consider this information in the article.

Reviewer #5:

If the quality of data from DATASUS is considered high in Brazil why the authors did not use the breast cancer Brazilian estimates?

Authors: In the new version of the paper we added all the information from DATASUS (included breast cancer estimates). “…Information regarding the incidence of breast cancer in the Brazilian female population aged 20-59 years and aged ≥ 60 years over 2015, 2016 and 2017 was taken from estimates of the DATASUS (i.e., Panel-Oncology), which analyzes estimates and makes information available free of charge”.

Reviewer #5:

The Healthcare Access and Quality (HAQ) Index may have been influenced by the poor-quality data of the north region cities. Are the north region estimates reliable?

Reviewer #6:

This study highlights an important topic on the impact of physical inactivity on hospitalization costs due to breast cancer, through secondary analysis of national databases. The study aimed “to estimate the economic burden of breast cancer due to physical inactivity in the Brazilian female population over a three-year period (2015 to 2017) and to relate these costs to conditions of access and quality of health services in Brazilian states”.

I have several major and some minor observations.

Authors: We really appreciate your comments. In the new version of the article we only added information about Brazilian capitals as suggested.

Reviewer #6:

2) In the Abstract, the author stated that the “Population Attributable Fraction” (PAF) was calculated but did not present the results, an important result of this study.

Authors: The change was made.

Reviewer #6:

Authors: The change was made for all information.

Reviewer #6:

Authors: We used the information of the SIH for hospitalization due to breast cancer. The information about physical activity were from Vigitel. In the new version of the paper we added the information.

Reviewer #6:

Authors: The mortality statistics' information are from DATASUS. Because of that we kept the reference.

Reviewer #6:

Authors: We really appreciate your comments. In the new version of the article we only added information about Brazilian capitals. We changed all the results. In the new version of the article we added new correlations between percentage of hospitalizations for breast cancer due to physical inactivity and the Healthcare Quality and Access index. The information allowed progress in the discussions of the article.

Reviewer #6:

Authors: We really appreciate your comments. We added this limitation.

Reviewer #6:

8) Please consider presenting the results by capitals and Federal District, not by Brazilian states.

Authors: In the new version of the article we only added information about Brazilian capitals. We changed all the results. In the new version of the article we added new correlations between percentage of hospitalizations for breast cancer due to physical inactivity and the Healthcare Quality and Access index. The information allowed progress in the discussions of the article.

Reviewer #6:

9) Lines 299-300. The statistic used (Spearman's correlation coefficient) was not described in the Method.

Authors: In the new version of the article we added the information.

Reviewer #6:

10) In lines 320-321, it is stated that “few estimated costs due to breast cancer [7]”. Please consider to cite other studies, such as Ding, 2016 (ref 9).

Authors: The changed was made.

Reviewer #6:

Authors: In the new version of the article we added others information.

Reviewer #6:

12) It would be great if the author could include a limitation about the susceptibility of the analysis conducted in the present study to ecological fallacy.

Authors: In the new version of the article we added this limitation.

Reviewer #6:

13) Please change FAP (lines 251 and 379) by PAF.

Authors: The changed was made.

Attachment

Submitted filename: Response to Reviewers.doc

Click here for additional data file.^{(73KB, doc)}

PLoS One. doi: 10.1371/journal.pone.0261019.r003

Decision Letter 1

Muhammad Shahzad Aslam

13 Jul 2021

PONE-D-21-09895R1

Hospitalization cost related to breast cancer due to physical inactivity in the Brazilian state capitals

PLOS ONE

Dear,

Please read the reviewer comments given below

Please submit your revised manuscript by12th August 2021. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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Kind regards,

Muhammad Shahzad Aslam, Ph.D.,M.Phil., Pharm-D

Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #4: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #1: Yes

Reviewer #4: Partly

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #4: N/A

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #1: Yes

Reviewer #4: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #1: Yes

Reviewer #4: Yes

**********

6. Review Comments to the Author

Reviewer #1: (No Response)

Reviewer #4: Thanks to the author for his availability to answer the questions asked by the reviewers. As for the manuscript, essential questions remain that still need to be clarified.

1. When re-reading the manuscript, after adjustments, it is not clear to the reader the reason for analyzing only hospital expenses and only expenses in capitals and DF. For most cancers, including breast cancer, ambulatory (outpatient) costs are much higher than hospital (inpatient) costs. Why not analyze both expenses? Why analyze only spending in capitals and DF? Wouldn't the expenses in the UF be more significant than in the capitals? Was the choice made for greater ease, convenience, or the availability in data collection, or is there any other reason?

2. The usefulness of presenting breast cancer incidence (number and raw rate) and hospitalization (number and age-standardized rate) data are not convincing. Where was this data used in the manuscript? What is the need for four tables to present unused data?

3. It is unclear what is the usefulness of using the HAQ Index. There is no mention of a theoretical or empirical association between this indicator and the prevalence of physical inactivity in the introduction. What premise or assumption motivated the author to include this analysis?

4. In the reference article by Kyu et al. (2016), the RR varies according to activity level. Compared with less active women (reporting less than 600 MET minutes/week of total physical activity), the risk of breast cancer among those in the low active (600-3999 MET minutes), moderately active (4000-7999 MET minutes), and highly active (≥8000 MET minutes) categories were, respectively, reduced by 3%, 6%, and 14%. The author used Vigitel's physically inactive women as a category of prevalence analysis. This category corresponds to how many METs/minutes/week? The impression is that the correct category of choice for Vigitel would be "insufficient physical activity" and not "physically inactive." Clarify this question, please.

5. According to the 2018 WCRF report on physical activity and cancer risk, physical activity has been associated with postmenopausal breast cancer (C50 for women 50 years or older). Why were all women included?

6. The methodology section needs to be better organized and written. The suggestion is to divide the section into four subsections: study design, hospital cost data, RR and prevalence of physical inactivity, and data analysis. The study design is a cost-of-illness study to estimate the direct costs of breast cancers attributable to lack of physical activity from the perspective of the Brazilian SUS. This approach uses aggregated disease costs, and attributable population fraction (PAF) estimates to calculate the costs attributable to a given risk factor. Hospital cost data should inform the data source and how they were collected (this information is already contained in the latest version of the manuscript). The RR and prevalence subsection should inform where the values were taken from. In the case of prevalence, the data source, the eligible population, and how the METS of the selected population were calculated need to be precise. Data analysis should inform how the PAF (equation) was calculated, the variables included in the equation, how the PAF was applied to expenses, and which software was used to calculate the final amounts.

7. Results must prioritize spending.

8. The reason for separating expenditures into 20-59 years and ≥ 60 years does not seem adequate. There are no restrictions on physical activity for those over 65s in the latest version of the WHO physical activity guide (2020). Therefore, any policy, program, or action involving physical activity will have the same recommendation regardless of premenopausal or postmenopausal women.

It is appropriate to analyze spending only in postmenopausal women since, according to WCRF, physical activity is related to postmenopausal breast cancer.

9. The discussion and conclusion sections should be rewritten in light of the above recommendations.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #4: No

PLoS One. 2022 Jan 19;17(1):e0261019. doi: 10.1371/journal.pone.0261019.r004

Author response to Decision Letter 1

11 Aug 2021

Reviewer #4:

Thanks to the author for his availability to answer the questions asked by the reviewers. As for the manuscript, essential questions remain that still need to be clarified.

Authors: We really appreciate your comments. In the new version of the article we have added most of your suggestions. In other suggestions, we provide explanations based on the literature to exemplify our decisions.

Reviewer #4:

Authors: We really appreciate your comments. In the new version of the article we added outpatient costs. Thus, this article presents hospitalization costs and outpatient costs.

The decision to analyze the capitals of Brazil and the Federal District was made because the survey of physical activity that is carried out in Brazil annually (e.g., VIGITEL) is carried out in Brazilian capitals and in the Federal District. Therefore, making estimates for all municipalities in Brazil based on physical activity information from Brazilian capitals would not be appropriate. We emphasize that there are no annual physical activity surveys covering all Brazilian states. These surveys only cover the capitals. In the new version of the paper we added this limitation: “This study developed analyses at level of Brazilian capitals, and not at level of states. The strategy used in the present study limits the identification of which states or other cities of the Brazil have high hospitalization and ambulatory costs due to physical inactivity and which would need to invest more in physical activity programs in primary care. The decision to analyze the capitals of Brazil and the Federal District was made because the survey of physical activity that is carried out in Brazil annually is carried out in Brazilian capitals and in the Federal District [17-19]”.

Reviewer #4:

Authors: We really appreciate your comments. In the new version of the article we removed this information from the article. This information was presented as supplementary documents, as if readers want to know general information about breast cancer in Brazil, they can consult the supplementary files.

Reviewer #4:

Authors: We agree with the reviewer. In the new version of the article we removed the information about HAQ Index. This information really was without theoretical support.

Reviewer #4:

Authors: We really appreciate your comments. In the new version of the article we added this information in the method section: “... Physically inactive were subjects who did not practice any free-time physical activity in the last three months of the interview and those who did not make intense physical efforts at work, did not commute to work or school and were not responsible for heavy cleaning of the house, as recommended in literature (e.g., they are those who have energy expenditure < 600 METS minutes/week) [22]”.

In 2017, a consensus was released (Tremblay et al., 2017) in which the concepts related to physical activity and sedentary behavior were defined. In this consensus was defined that physical inactivity is an insufficient physical activity level to meet present physical activity recommendations (i.e., < 600 METS minutes/week). For that reason, we used the term physical inactivity in our paper.

Reference:

Tremblay MS, Aubert S, Barnes JD, Saunders TJ, Carson V, Latimer-Cheung AE, Chastin SFM, Altenburg TM, Chinapaw MJM; SBRN Terminology Consensus Project Participants. Sedentary Behavior Research Network (SBRN) - Terminology Consensus Project process and outcome. Int J Behav Nutr Phys Act. 2017 Jun 10;14(1):75. doi: 10.1186/s12966-017-0525-8.

Reviewer #4:

Authors: In the new version of the paper we analyzed information from adult and older adult women in Brazil (aged ≥ 20 years) without stratifying by age. I respect the reviewer's opinion that the WCRF reports that physical activity is related to postmenopausal breast cancer. However, in the present study we used a reference for PAF that provided evidence for the female population over 20 years of age. In addition, the guidelines of physical activity make it clear that there is sufficient evidence of the relationship between physical activity and breast cancer in women adults and older adults (before and after menopause). For this reason, in the present study we made this methodological decision. The following paragraph was added to the discussion section: “There is a lot of debate in the literature about the effect of physical activity on the prevention of breast cancer before and after menopause [39-41]. All health agencies reinforce that the effect of physical activity in preventing breast cancer is more evident after menopause. However, before menopause there is a theoretical discussion that still needs consensus. The World Cancer Research Fund report describes that the strongest evidence that exists in the relationship between physical activity and breast cancer prevention is for women after menopause [39]. Physical activity guidelines describe that there is strong evidence that physical activity prevents breast cancer before and after menopause [40, 41]. The present study adopted the recommendations of the physical activity guidelines because they were the most recent on the subject. In addition, in the present study was used a reference for PAF that which investigated adult and older adults women [24]”.

Reviewer #4:

Authors: The change was made.

Reviewer #4:

7. Results must prioritize spending.

Authors: In the new version of the paper we prioritize spending information.

Reviewer #4:

It is appropriate to analyze spending only in postmenopausal women since, according to WCRF, physical activity is related to postmenopausal breast cancer.

9. The discussion and conclusion sections should be rewritten in light of the above recommendations.

Authors: We really appreciate your comments on the article. The change was made.

Attachment

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PLoS One. doi: 10.1371/journal.pone.0261019.r005

Decision Letter 2

Muhammad Shahzad Aslam

29 Sep 2021

PONE-D-21-09895R2Hospitalization and ambulatory costs related to breast cancer due to physical inactivity in the Brazilian state capitalsPLOS ONE

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6. Review Comments to the Author

Reviewer #4: I have only a final commentary. The author said that periodic exams prevent breast cancer (lines 315-316): "it is necessary that cities invest in other initiatives for the prevention of breast cancer, such as periodic exams." It's not true. Periodic exams such as mammography, contrary to routine cervical cancer exams that lower cervical cancer cases, increase the number of breast cancers.

Reviewer #7: The topic is of great public health importance. But it only focused on description of the situation. It should be very informative to the reader and policy makers. So, higher order statistics should be included. Sound study participants categorization should be include.

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PLoS One. 2022 Jan 19;17(1):e0261019. doi: 10.1371/journal.pone.0261019.r006

Author response to Decision Letter 2

28 Oct 2021

Reviewer #4:

I have only a final commentary. The author said that periodic exams prevent breast cancer (lines 315-316): "it is necessary that cities invest in other initiatives for the prevention of breast cancer, such as periodic exams." It's not true. Periodic exams such as mammography, contrary to routine cervical cancer exams that lower cervical cancer cases, increase the number of breast cancers.

Authors: We really appreciate your comments. In the new version of the article we have removed that sentence.

Reviewer #7:

The topic is of great public health importance. But it only focused on description of the situation. It should be very informative to the reader and policy makers. So, higher order statistics should be included. Sound study participants categorization should be include.

Authors: We really appreciate your comments. This is a cost-of-illness study to estimate the direct costs of breast cancers attributable to lack of physical activity from the perspective of the Brazilian health services. The study's analysis units are the states of Brazil. Thus, in the article we are not working with data from individuals, but with data from the states of Brazil. In the new version of the article, we've added this information more explicitly: “The study's analysis units are the states of Brazil”.

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PLoS One. doi: 10.1371/journal.pone.0261019.r007

Decision Letter 3

Muhammad Shahzad Aslam

23 Nov 2021

Hospitalization and ambulatory costs related to breast cancer due to physical inactivity in the Brazilian state capitals

PONE-D-21-09895R3

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PLoS One. doi: 10.1371/journal.pone.0261019.r008

Acceptance letter

Muhammad Shahzad Aslam

7 Jan 2022

PONE-D-21-09895R3

Hospitalization and ambulatory costs related to breast cancer due to physical inactivity in the Brazilian state capitals

Dear Dr. Silva:

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 Table. Description of outpatient procedures on breast cancer applied in Brazil.

DATASUS (2015, 2016 and 2017).

(DOC)

Click here for additional data file.^{(31.5KB, doc)}

S2 Table. Incidence of breast cancer among women in Brazilian state capitals and Federal District (aged ≥ 20 years).

*rate per 100,000 inhabitants. Reference population: Reference population: women residing in each capital for each year (aged ≥ 20 years).

(DOC)

Click here for additional data file.^{(66KB, doc)}

*Age-standardized (per 100,000 inhabitants).

(DOC)

Click here for additional data file.^{(59KB, doc)}

Attachment

Submitted filename: PONE-D-21-09895_reviewer_19.05.21 to send.pdf

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Attachment

Submitted filename: Response to Reviewers.doc

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Submitted filename: Response to Reviewers 3.doc

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Attachment

Submitted filename: review II.doc

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Submitted filename: Response to Reviewers 5.doc

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Data Availability Statement

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PERMALINK

Hospitalization and ambulatory costs related to breast cancer due to physical inactivity in the Brazilian state capitals

Diego Augusto Santos Silva

Roles

Abstract

Introduction

Materials and methods

Study design

Hospitalizations and ambulatory costs data

Prevalence of physical inactivity

Data analysis

Results

Table 1. Prevalence of physical inactivity in women aged ≥ 20 years in 2015, 2016 and 2017, in Brazilian capitals and Federal District.

Fig 1. Population attributable fraction indicating the percentage of hospitalizations for breast cancer due to physical inactivity in women aged ≥ 20 years (Fig 1) from the Brazilian states capitals and Federal District.

Table 2. Cost of hospitalizations for breast cancer in women aged ≥ 20 years in Brazil and in the Brazilian state capitals in 2015, 2016 and 2017.

Table 3. Ambulatory costs by breast cancer in women aged ≥ 20 years in Brazil and in the Brazilian state capitals in 2015, 2016 and 2017.

Fig 2. Average cost of hospitalizations for breast cancer due to physical inactivity in the period of 2015, 2016 and 2017 in the Brazilian states capitals in women aged ≥ 20 years.

Fig 3. Average ambulatory cost for breast cancer due to physical inactivity in the period of 2015, 2016 and 2017 in the Brazilian states capitals in women aged ≥ 20 years.

Discussion

Conclusions

Supporting information

Data Availability

Funding Statement

References

Decision Letter 0

Muhammad Shahzad Aslam

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Author response to Decision Letter 0

Decision Letter 1

Muhammad Shahzad Aslam

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Author response to Decision Letter 1

Decision Letter 2

Muhammad Shahzad Aslam

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Author response to Decision Letter 2

Decision Letter 3

Muhammad Shahzad Aslam

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Acceptance letter

Muhammad Shahzad Aslam

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Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

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