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East Tennessee State University

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8-2016

Geographical Location and Stage of Breast Cancer

Diagnosis: A Systematic Review of the Literature

Faustine Williams

East Tennessee State University, williamsf2@etsu.edu

Aimee S. James

Washington University in St. Louis School of Medicine

Stephen Jeanetta

University of Missouri

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Williams, Faustine; James, Aimee S.; and Jeanetta, Stephen. 2016. Geographical Location and Stage of Breast Cancer Diagnosis: A Systematic Review of the Literature.Journal of Health Care for the Poor and Underserved. Vol.27(3). 1357-1383.https://doi.org/ 10.1353/hpu.2016.0102ISSN: 1548-6869

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Geographical Location and Stage of Breast Cancer Diagnosis: A

Systematic Review of the Literature

Copyright Statement

Copyright © 2017 Meharry Medical College. This article first appeared inJournal of Health Care for the Poor

and Underserved27:3 (2016), 1357-1384. Reprinted with permission by Johns Hopkins University Press.

Comments

Errata of article published inJournal of Health Care for the Poor and Undeserved, 28(1), February 2017:

https://muse.jhu.edu/article/648782

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Geographical Location and Stage of Breast Cancer Diagnosis: A Systematic Review

of the Literature

Faustine Williams, Stephen Jeanetta, Aimee S. James

Journal of Health Care for the Poor and Underserved, Volume 27, Number

3, August 2016, pp. 1357-1383 (Article)

Published by Johns Hopkins University Press

DOI:

For additional information about this article

Access provided by East Tennessee State University (27 Apr 2017 19:13 GMT)

https://doi.org/10.1353/hpu.2016.0102

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© Meharry Medical College Journal of Health Care for the Poor and Underserved 27 (2016): 1357–1383.

Geographical Location and Stage of Breast Cancer

Diagnosis: A Systematic Review of the Literature

Faustine Williams, PhD, MPH, MS

Stephen Jeanetta, PhD Aimee S. James, PhD, MPH

Abstract: Objective: To examine systematically the literature on the effect of geographical location variation on breast cancer stage at diagnosis, race/ ethnicity, and socioeconomic status. Methods. Eight electronic databases were searched using combination of key words. Of the 312 articles retrieved from the search, 36 studies from 12 countries were considered eligible for inclusion. Results. This review identified 17 (47%) of 36 studies in which breast cancer patients residing in geographically remote/ rural areas had more late- stage diagnosis than urban women. Ten (28%) studies reported higher proportions of women diagnosed with breast cancer resided in urban than rural counties. Nine (25%) studies reported no statistically significant association between place of residence and stage at diagnosis for breast cancer patients residing in rural and urban areas. Conclusions. Cancer patients residing in rural and disadvantaged areas were more likely to be diagnosed with distant breast metastasis. Efforts to reduce these inequalities and subsequent mortality are needed.

Key words: Breast neoplasm, staging at diagnosis, rural- urban, rural population, urban population, place of residence.

E

xcept for skin cancer, breast cancer is the most frequent malignancy among women in the United States, affecting women across all racial and ethnic groups. In 2015 it was projected that 231,840 new cases of invasive breast cancer were expected to occur among women in the United States (U.S.), and about 2,350 new cases were expected in men. In addition to invasive breast cancer, 60,290 new cases of in situ breast cancer were expected to occur among women in 2015.1,2

Studies have indicated that disparities in access to primary care, especially access to screening services such as mammogram and Papanicolaou smear, exist throughout the United States primarily due to uneven distribution of health facilities.3,4 Disparities in

the prevention and early detection of cancer lead to disparities in cancer outcomes and LITERATURE REVIEW

FAUSTINE WILLIAMS is affiliated with the College of Public Health, Department of Health Services Management and Policy, at East Tennessee State University. AIMEE S. JAMES is affiliated with the Division of Public Health Science, Department of Surgery, at Washington University in St. Louis School of Medicine. STEPHEN JEANETTA is affiliated with the Department of Rural Sociology, Community Development Program and the University of Missouri. Please send correspondence to Faustine Williams, Ph.D., MPH, MS, College of Public Health, Department of Health Services Management and Policy, East Tennessee State University Box 70264 Johnson City, TN 37614-1700; email: FaustineWilliams@ gmail.com; phone: (423) 439-6637; fax: (423) 439-6710.

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1358 Location and stage of breast cancer diagnosis

survival. Much of the disparity in mortality can be attributed to the stage of diagnosis at the time of cancer detection. Research shows that certain groups of people, namely those who are poor, less educated, uninsured, and/or immigrants, are more likely to be diagnosed at a later stage of disease, more likely to receive substandard care, and are more likely to die from cancer.5 Nationally, 61% of White women but only 51%

of Black women were diagnosed with breast cancer at the local stage.6 The five- year

survival rate for White women diagnosed with breast cancer between 2002 and 2008 was 90% while the survival rate for Black women was just 78%.6

Other studies on cancer survival from cancer in various countries have noted that geographical location is strongly associated with survival and that could also reflect stage at diagnosis and the kind of treatment patients are likely to receive.7– 13 In contrast,

some studies have reported that no significant difference exists between breast cancer stage at diagnosis and place of residence or travel time/ distance travel to the nearest mammography facility.14– 22 The aim of this review was to examine systematically the

literature on the effect of geographical location variation on breast cancer stage at diagnosis, race/ ethnicity, and socioeconomic status rather than rural- urban differences in mammography use or risk factors for breast cancer development.

Methods

In the process of identifying studies, searches were conducted in the following biblio-graphic databases: Academic Search Complete (1984– 2013), CINAHL (1982– 2013), Compendex and GEOBASE (1969– 2013), Medline (1966– 2013), PubMed (1951– 2013), EMBASE (1947– 2013), Cochrane (1993– 2013) and Scopus (1960– 2013) using key words and phrases. The key words and phrases: breast neoplasm or cancer, staging at diagnosis, rural- urban, rural population, urban population, or place of residence. Addi-tionally, we systematically searched the references sections of all articles retrieved to identify additional citation. There was no limitation of publication date in the search; however, the earliest eligible article was published in 1992. Inclusion criteria were studies comparing the differences in breast cancer stage at diagnosis and geographical place of residence, and were published in English. Based on the inclusion criteria, studies that focus solely on access to health care services, influence of socioeconomic status and race on stage at diagnosis, and geographic differences in treatment and/or survival of breast cancer were excluded.

Results

Based on the selection criteria established, 36 out of 312 studies from 12 countries remained eligible.11,14– 49 Figure 1 shows the summary of criteria used for inclusion of

eligible studies in this review. Of the eligible papers selected, 23 were from the United States, two each from Australia and New Zealand, and one each from Canada, Den-mark, Egypt, Estonia, Italy, Poland, South Africa, Switzerland, and the United King-dom. Tables 1 and 2 list studies included in this review. Table 1 identifies the type of cancer registry database used and findings, whereas Table 2 focuses on the primary factors addressed and the major conclusions reached by the authors. For the purpose

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1359 Williams, Jeanetta, and James

of this review, we began analysis by summarizing all of the findings in each study. Second, common themes that emerged in these findings were identified, and finally, the review was structured according to three major general themes. These include: (1) variation by geographic location; (2) variation by race/ ethnicity; and (3) variation by socioeconomic status.

Variation by geography or location. Geographic barriers are important for breast cancer patients, especially those who live in rural areas. Over the past decades, numerous studies have confirmed that patients residing in rural and medically underserved areas are more likely to have unstaged tumors and advanced stage breast cancer diagnosis than their urban counterparts.11,23– 38 However, we found inconsistency in the definition of

rural and/or urban. For example, all 23 studies11,16– 21,23,25,26,29– 32,34,35,38– 40,43– 46,49 from the U.S.

used different definitions and measurements for rural and urban. Six studies11,17,18,21,39,40

used the rural urban commuting area (RUCA) codes measurement and definition. The RUCA codes classify all census tracts in the U.S. using measures of population density, urbanization, and daily commuting.50 The rural urban continuum or Beale code system

was used in four studies.20,23,43,46 Other definitions such as the urban influence code,

U.S. Census Bureau rural urban classification, population density, state- specific minor division, ZIP code and census tract, and federally designated medically underserved Figure 1. Flow diagram for literature search results and application of eligibility criteria.

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Au th or D ata ba se/S our ce Sa mp le P opu la tio n a nd D ata Y ea r Siz e (N) C ou nt ry Rur al- U rb an D efini tio n Prim ar y F in din g A m ey et  al . 1997 (23) Flo rid a C an cer D at a S ys te m a nd A re a R es our ce Fi le A ll w om en r es idin g in t he st at e o f F lo ri da b et w ee n 1981 a nd 1989 w ho w er e di ag no se d w ith b re as t can ce r 79,946 U .S.A. Rura l U rb an C on tin uum C od e (R UC C) cl as sifi ca tio n— M et ro po lit an a nd N on- m et ro po lit an c oun tie s Rura l b la ck w om en a re di ag no se d w ith b re as t c an -ce r m uc h l at er t ha n b la ck ur ba n w om en o r w hi te s of ei th er re siden ce . A rms tr ong & Bo rm an 1996 (14) N at io na l C an cer Re gi str y Pe rs on s di ag no se d a s h av -in g c an ce r o f t he b re as t th ro ug h t he N at io na l C an ce r R eg ist ry b et w ee n 1978 a nd 1992 20,090 Ne w Z ea -lan d Ba se d on R eg ion al H ea lth A ut hor ity re -gi on s. R ura l c en te rs a s p op ul at io n ra ng in g fr om 10,000 t o 30,000 a nd ur ba n a re as a s w ith p op ul at io n g re at er t ha n 30,000 St ud y b ut n o s ig nifi ca nt diff er en ce b et w ee n s ta ge a t di ag no sis a nd r ura l- ur ba n p la ce o f r es id en ce . Baa de et  al . 2011 (24) Q ue en slan d C an -ce r R eg ist ry W om en a ge d 30 –79 y ea rs di ag no se d a s h av in g br ea st c an ce r b et w ee n 1997 a nd 2006 18,658 A us tra lia A cc es sib ili ty/R em ot en es s in de x o f A us tra lia cl as sifi ca tio n in to fi ve a re as b as ed o n di st an ce t o t he c lo set s er vi ce c en te r (M aj or Ci ty , I nn er R eg io na l, O ut er R eg io na l, R e-m ot e a nd V er y R em ot e a re as) Th e ra te s o f a dva nc ed b re as t c an ce r w er e s ig nifi -ca nt ly h ig he r f or w om en r es idin g in O ut er R eg io na l ar ea s (O R 1.13, 95% CI = 1.02, 1.24) a nd t ho se w ho liv ed in t he m os t di sa dva nt ag ed a re as (O R 1.16, 95% CI = 1.02, 1.32). Ba rr y & Br ee n 2005 (25) Sur ve ill an ce , Ep idem io log y, an d E nd R es ul ts (S EER) C an ce r d at a f ro m 1989 to 1990 12,395 U .S.A. Fed er all y d es ign at ed m ed ic all y u nd er se rv ed ar ea d ev el op ed b y H ea lth R es our ce s a nd Se rv ic es A dm in ist ra tio n Re sid en ce in a n un de rc la ss n eig hb or ho od o r a n ext re m el y p oo r n eig hb or ho od a lso c on tr ib ut es t o a la te s ta ge di ag no sis. Be nn et t et  al . 2007 (15) N ew Z ea la nd C an ce r R eg ist ry W om en di ag no se d w ith br ea st c an ce r b et w ee n Ja nu ar y 1998 a nd 31 D ec em be r 2002 11,340 Ne w Z ea -lan d St at ist ics N ew Z ea la nd C la ss ifi ca tio n, b as ed o n p op ul at io n s iz e. U rb an a re as: (i) M ain ur ba n a re as ≥30,000 po pu la tio n, (ii) S ec on da ry ur ba n a re as (10 –29,999 p op ul at io n, a nd (iii) M in or ur ba n a re as 1000 –9999 p op ul at io n. R ura l ar ea s <1000 p op ul at io n U rb an/r ura l r es id en ce , h ow ev er c la ss ifi ed , di d n ot ha ve a ny s ig nifi ca nt e ffe ct o n t he o dd s o f l at e s ta ge at di ag no sis f or w om en di ag no se d w ith b re as t ca nc er in N ew Z ea la nd . A lso n o t re nd t o in cr ea sin g od ds w ith in cr ea sin g r ura lit y o r di st an ce . ( Co nt in ue d o n p . 1361 )

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Au th or D ata ba se/S our ce Sa mp le P opu la tio n a nd D ata Y ea r Siz e (N) C ou nt ry Rur al- U rb an D efini tio n Prim ar y F in din g Bl air et  al . 2006 (16) Th e C alif or ni a C an ce r R eg ist ry Pa tie nts w ith b re as t, mel ano m a, a nd c ol on ca nc er f ro m 1988 t o 2003 59,615 (b re as t can ce r) U .S.A. C alif or ni a R ura l H ea lth C om m iss io n d efin i-tio n. R ura l c oun tie s r ep re se nt a p op ul at io n d en sit y o f 250 p eo pl e/l es s p er sq ua re m ile a nd n o in co rp ora te d c om m un i-tie s o f m or e t ha n 50,000 p eo pl e Th er e wa s n o diff er en ce in p er ce nt ag e o f p at ie nts pr es en tin g w ith e ar ly s um m ar y s ta ge di se as e bet w ee n r ura l a nd ur ba n d w el le rs. F or e xa m pl e, in 2003, 70% o f ur ba n p at ie nts p re se nt ed w ith e ar ly st ag e di se as e a nd 69% o f ur ba n p at ie nts w er e di ag -no se d w ith e ar ly s um m ar y s ta ge b re as t c an ce r. C el aya et  al . 2010 (17) N ew H am ps hir e St at e C an ce r Re gi str y Fem ale re siden ts o f N ew H am ps hir e di ag no se d w ith b re as t c an ce r bet w ee n J an ua ry 1, 1998 an d D ec em be r 31, 2004 5,966 U .S.A. Rura l U rb an C om m ut in g A re a (R UCA) cl as sifi ca tio n s ch em e. G ro up in g: ur ba n, la rg e r ura l, a nd s m al l r ura l N o s ig nifi ca nt a ss oci at io n b et w ee n r ura l r es id en ce an d s ta ge o f di ag no sis wa s f oun d. C ho et  al . 2011 (26) Illin oi s S ta te C an ce r R eg ist ry in co nj un ct io n 1990 an d 2000 C en su s tr ac t W om en di ag no se d w ith br ea st c an ce r in C oo k C oun ty b et w ee n 1994 an d 2003 42,714 U .S.A. U ni te d S ta te s (U .S.) C en su s t ra ct Re sidin g in p oo r c on ce nt ra te d im m ig ra tio n n eig h-bo rh oo ds wa s a ss oci at ed w ith b ein g di ag no se d w ith la te b re as t c an ce r. C ut hb er ts on et  al . 2009 (27) Tr en t C an cer Re gi str y W om en di ag no se d w ith in va siv e b re as t c an ce r fr om 1998 t o 2006 31,551 U .K. Pr im ar y C ar e T ru st b oun da ri es d er iv ed fr om p os tc ode W om en r es id en t in n in e T re nt p rim ar y c ar e t ru sts (PCT s) h av e s ig nifi ca nt h ig he r r isk di ag no sis w ith la te s ta ge b re as t c an ce r t ha n t ho se r es id en t in N ot -tin gh am Ci ty PCT . D al to n et  al . 2006 (28) D an ish B re as t Ca nc er C oo pe ra -tive W om en w ith a p rim ar y in va siv e b re as t c an ce r di ag no se d b et w ee n 1983 an d 1999 28,765 D en m ar k D eg re e o f ur ba ni ci ty : c ap ita l a re as, s ub ur bs, pr ov in ci al ci tie s a nd r ura l a re as Th er e wa s a n ur ba n- rura l g ra di en t, w ith h ig he r ri sk a m on g r ura l w om en (O R 1.10; 95 % CI = 1.02, 1.18) a nd l ow er r isk a m on g w om en in t he c ap ita l su bur bs (O R, 0.85; 95% CI = 0.78, 0.93) a nd c ap ita l ar ea (O R, 0.93; 95% CI = 0.84, 1.02). ( Co nt in ue d o n p . 1362 )

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Au th or D ata ba se/S our ce Sa mp le P opu la tio n a nd D ata Y ea r Siz e (N) C ou nt ry Rur al- U rb an D efini tio n Prim ar y F in din g D ey et  al . 2010 (42) Gha rb ia h po pul ati on - ba sed ca nce r R eg ist ry W om en di ag no se d w ith p rim ar y b re as t ca nc er w ith k no w n es tr og en r ec ep to r p os iti ve (ER+) o r p ro ge st er on e re cep to rs(P R) s ta tu s fo r a p er io d o f 6 y ea rs (2001 –2006) 3,673 Eg ypt C en tra l A ge nc y f or P ub lic M ob iliza tio n a nd St at ist ics c odin g o f ur ba n a nd r ura l a re as. U rb an a re as c on sis te d o f c ap ita l ci tie s, a nd rura l c on sis te d o f v ill ag es s ur ro un din g t he ca pit al c iti es U rb an ER+ in ci de nc e ra te (p er 100,000 w om en) wa s 2 –4 t im es (IRR = 3.36, 95% CI = 4.84, 2.34) h ig he r t ha n r ura l in ci de nc e ra te . ER - in ci de nc e ra te wa s 2 –3 t im es (IRR = 1.86, 95% CI = 2.38, 1.45) h ig he r in ur ba n a re as t ha n in rura l a re as. El lio tt et  al . 2004 (29) La ke S up er ior Rura l C an ce r C ar e Pr ojec t A ll e lig ib le c an ce r c as es di ag no se d b et w ee n 1993 an d 1997 831 U .S.A. U .S. C en su s B ur ea u r ura l a nd ur ba n c la s-sific at io n U rb an p at ie nts w er e m or e li ke ly t o b e di ag no se d a t ea rli er s ta ge t ha n r ura l. Es s et  al . 2010 (30) Se ve n S w iss Po pul ati on ba sed C an cer R eg ist rie s W om en di ag no se d w ith in va siv e b re as t c an ce r bet w ee n J an ua ry 1, 2003 an d D ec em be r 31, 2005 4,820 Sw itz erl and Re gi on s - un de fin ed C on sid era bl e diff er en ce s in t he d et ec tio n a nd m an ag em en t o f b re as t c an ce r a cr os s a ll t he s ev en re gi on s w ith r eg ar ds t o ur ba ni ty a nd a ffl ue nc e. Fr ie de ll et  al . 2003 (43) K en tuc ky C an cer Re gi str y In ci de nc e a nd m or ta lit y of b re as t c an ce r a m on g w om en f or t he p er io d 1995 –2000 18,205 U .S.A. Be al e c od e/R ura l U rb an C on tin uum C od e co un tie s c la ss ifi ca tio n U sin g B ea le c od e 0 –3 f or “ ur ba n” a nd 4 –9 f or r ura l, in ci de nc e ra te s f or e ar ly s ta ge c as es a re s lig ht ly hig he r in t he ur ba n a re as. I nci de nc e ra te s f or l at e st ag e c as es a re s lig ht ly h ig he r f or ur ba n c om pa re d to r ura l a re as o ve r t he r ep or tin g p er io d. Gr ego ri o et  al . 2002 (44) C on ne ct ic ut T u-m or R egi str y W om en di ag no se d w ith br ea st c an ce r b et w ee n 1991 t o 1995 10,601 inva siv e a nd 1,814 in s itu br ea st ca nce rs U .S.A. C on ne ct ic ut c en su s b lo ck g ro ups Th e m os t p ro ba bl e l oc at io n o f l ow in ci de nc e wa s rura l n or th ea st er n C on ne ct ic ut w he re r isk o f di se as e, r el at iv e t o e lse w he re a ro un d t he s ta te , wa s 0.70 (p=.0001); t he m os t p ro ba bl e p la ce o f el eva te d in ci de nc e wa s n or th c en tra l C on ne ct ic ut w he re a r el at iv e r isk o f 1.34 (p=.002) wa s o bs er ve d. In ciden ce o f in s itu d ise as e w as e sti m at ed t o b e sig ni fic an tly h ig h f or n or th c en tr al C on ne ct icu t (RR = 1.84; p=.0001). ( Co nt in ue d o n p . 1363 )

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Au th or D ata ba se/S our ce Sa mp le P opu la tio n a nd D ata Y ea r Siz e (N) C ou nt ry Rur al- U rb an D efini tio n Prim ar y F in din g H al l et  al . 2005 (45) N or th C ar olin a C en tra l C an ce r Re gi str y W om en w ith a fir st c as e of in va siv e o r in sit u b re as t c an ce r di ag -no se d b et w ee n J an ua ry 1995 a nd D ec em be r 1999 27,989 U .S.A. U rb an I nfl ue nc e C od e: (i) M et ro po lit an, (ii) N on- M et ro po lit an – a dj ac en t t o a m et ro po lit an a re a, (iii) N on- M et ro po lit an – no n- ad ja ce nt t o m et ro po lit an a re a Fo r w hi te w om en, in ci de nc e ra te ra tio s (IRRs) co m -pa rin g t he m os t ur ba n w ith t he m os t r ura l c oun tie s w er e 1.60 f or in s itu a nd 1.18 f or in va siv e c an ce r. Fo r n on- w hi te w om en, IRRs w er e 1.27 a nd 0.99, re sp ec tiv ely . H au sau er et  al . 2009 (46) N or th A m er ic an A ss oci at io n o f C en tra l C an ce r Re gi st ri es re so urc e In va siv e a nd in s itu b re as t ca nc er in ci de nc e d at a f or th e y ea rs 1997 t o 2004 475,523 inva siv e a nd 111,885 in situ U .S.A. 2003 U .S. D ep ar tm en t o f A gr ic ul tur e n in e- po in t r ura l/ur ba n c odifi ca -tio n s ch em e, w hi ch di st in gui sh es c oun tie s by p op ul at io n s iz e, d eg re e o f ur ba niza tio n, an d a dj ac en cy t o a m et ro po lit an a re a O ve ra ll p at te rn s o f in va siv e b re as t c an ce r w er e co m pa ra bl e a m on g w om en li vin g in b ot h ur ba n an d s ub ur ba n c oun tie s b ut diff er ed f or w om en in rura l c oun tie s. H en ry et  al . 2011 (18) 10 st at e- w id e po pul ati on ba sed ca nc er re gi st rie s (A rk an sa s, C alif or -ni a, I da ho , I owa, K en tuc ky , N or th C ar olin a, N ew H am ps hir e, N ew Yo rk, N ew J er se y, an d O re go n W om en a ge d 40 y ea rs a nd older , d ia gn os ed b et w een Ja nu ar y 1, 2004 a nd D ec em be r 31, 2006, 161,619 U .S.A. Rura l U rb an C om m ut in g A re a c od es b as ed on U .S. C en su s B ur ea u ur ba niz ed a re a a nd w or k c om m ut in g p at te rn s. U rb an (c en tra l pl ac es >50,000 p op ul at io n), s m al l t ow n (c en tra l p la ce s o f 10,000 –49,000 p op u-la tio n), a nd s m al l r ura l t ow n (<10,000 popu la tio n) Pr op or tio n o f l at e s ta ge wa s n ea rly i de nt ic al a m on g w om en li vin g in s m al l r ura l t ow ns (31%) c om pa re d to w om en li vin g in ur ba n a re as (30%). R ura l/ur ba n re sid en ce t yp e wa s n ot a s ig nifi ca nt p re di ct or o f br ea st c an ce r s ta ge a t di ag no sis. H ig gi nb ot ha m et  al . 2001 (31) M iss iss ip pi S ta te D ep ar tm en t o f H ea lth C en tra l C an ce r R eg ist ry A ll p at ie nts w ho w er e di ag no se d a nd/o r t re at ed fo r c an ce r in 1996 9,685  U .S.A. U .S. C en su s B ur ea u r ura l ur ba n c la ss ifi ca -tion Th er e wa s a s ig nifi ca nt diff er en ce b et w ee n r ura l an d ur ba n r es id en ts f or s ta ge o f di se as e a t in iti al di ag no sis. S ec on dl y, t he p ro po rt io n o f t um or s un st ag ed a t di ag no sis i s g re at er f or r ura l c om pa re d to ur ba n r es id en ts. Ho ffm an et  al . 2000 (47) So ut h A fr ic an C an ce r R eg ist ry W om en un de r t he a ge o f 50 di ag no se d w ith b re as t can ce r 485 So ut h Af ri ca U nd efi ne d Th e o dd s o f b ein g di ag no se d w ith l oc aliz ed s ta ge br ea st c an ce r wa s m or e t ha n t w ic e f or w om en in ur ba n a re as. ( Co nt in ue d o n p . 1364 )

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Au th or D ata ba se/S our ce Sa mp le P opu la tio n a nd D ata Y ea r Siz e (N) C ou nt ry Rur al- U rb an D efini tio n Prim ar y F in din g H ow e et  al . 1992 (32) Illin oi s S ta te C an -ce r R eg ist ry A ll f em al e b re as t c an ce r ca se s di ag no se d in 1986 –87 781 U .S.A. 1990 U .S. C en su s p op ul at io n c oun ts. R ura l – p op ul at io n d en sit y o f <100 p er so ns/s qu ar e m ile a nd ur ba n 210 p er so ns/s qu ar e m ile C om pa re d w ith ur ba n c as es, r ura l c as es di ag no se d in r ura l h os pi ta ls w er e l es s li ke ly t o h av e a s ta ge d tum or s a nd m or e li ke ly t o h av e n od e di ss ec tio ns. H ua ng et  al . 2009 (19) K en tuc ky C an cer Re gi str y Fe m al e di ag no se d w ith br ea st c an ce r b et w ee n 1999 a nd 2003 12,322 U .S.A. Re sid en ce in ur ba n/r ura l c oun tie s wa s ca te go riz ed a s m et ro po lit an o r n on m et ro -po lit an Th er e wa s n o s ig nifi ca nt a ss oci at io n b et w ee n r ura l/ ur ba n r es id en ce a nd p ov er ty a t C en su s t ra ct l ev el . In no s et  al . 2011 (33) Es to ni a C an ce r Re gi str y Fe ma le b re as t c an -ce r c as es r ep or te d in 1995 –2006 6,936 Es ton ia C oun ty a nd r eg io n - un de fin ed Sig nifi ca nt diff er en ce s in t he n um be r o f p at ie nts di ag no se d w ith l at e s ta ge c an ce r a cr os s r eg io ns o f re sid en ce (T al lin n, T ar tu , I da- V ir u C oun ty). K le in et  al . 2011 (20) Sur ve ill an ce , Ep idem io log y, an d E nd R es ul ts (S EER) P ro gra m of t he N at io na l C an ce r I ns tit ut e M al e p at ie nts di ag no se d w ith b re as t c an ce r f ro m 1988 t o 2006 4,222 U .S.A. Rura l U rb an C on tin uum C od e – M et ro po li-ta n a nd N on m et ro po lit an c oun tie s A s ig nifi ca nt diff er en ce wa s n ot f oun d b et w ee n re gi on a nd s ta ge a t di ag no sis, in di ca tin g t ha t t he st ag e a t di ag no sis wa s n ot a ss oci at ed w ith t he re gi on. A s ig nifi ca nt diff er en ce wa s n ot f oun d bet w ee n r eg io n a nd t um or s iz e a t di ag no sis, in di -ca tin g t ha t t he t um or g ra de s iz e a t di ag no sis wa s al so n ot a ss oci at ed w ith t he r eg io n. K rzyza k et  al . 2010 (48) Voi vo ds hip C an ce r Re gi str y W om en di ag no se d w ith br ea st c an ce r d ur in g 2001 –2002 696 Po la nd N at io na l Offic ia l R eg ist er o f T er rit or ia l Di vi -sio n o f t he C oun tr y – ur ba n a nd r ura l Th e p ro po rt io n o f l oc aliz ed s ta ge wa s 35.5% in ur ba n a nd 29.5% in r ura l w om en. E ve n m or e t ha n ha lf o f t he w om en w er e di ag no se d in r eg io na l s ta ge at di se as e in b ot h ur ba n a nd r ura l a re as (52.4% vs 52.0%). Liff et  al . 1991 (34) G eo rg ia C en te r f or C an cer S ta tis tic s A ll in ci de nt c an ce rs am on g r es id en ts o f m et ro po lit an A tla nt a a nd te n n eig hb or in g r ura l co un tie s b et w ee n 1978 an d 1985. 35,6 10 U .S.A. Rura l ur ba n - un de fin ed Re sid en ts o f t he r ura l a re a w er e t w ic e a s li ke ly to h av e un st ag ed c an ce rs 18.3%) a s w er e ur ba n re sid en ts (9.6%]. A m on g p at ie nts w ith k no w n s ta ge at di ag no sis, r ura l p at ie nts t en de d t o h av e m or e ad va nc ed di se as e t ha n ur ba n p at ie nts. T he r el at iv e ex ce ss o f n on lo ca liz ed m alig na nci es in r ura l G eo r-gi a wa s 21% f or w hi te s a nd 37% f or b la cks. ( Co nt in ue d o n p . 1365 )

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Au th or D ata ba se/S our ce Sa mp le P opu la tio n a nd D ata Y ea r Siz e (N) C ou nt ry Rur al- U rb an D efini tio n Prim ar y F in din g M ar ko ss ian & H in es 2012 (21) Th e A tla nt a a nd Rura l G eo rg ia C an ce r Re gi str ie s A ll in ci de nt b re as t t um or s di ag no se d f or no n- H isp an ic w hi te a nd no n- H isp an ic A fr ic an A m er ic an w om en f or t he ye ar s 1992 –2007 23,500 U .S.A. Rura l U rb an C om m in ut in g A re a C od es. U rb an c oun tie s h av e c od es ≤3, a nd rura l c oun tie s h av e c od es ≥6 Rura l r es id en ts w er e l es s li ke ly t o b e di ag no se d w ith in s itu t um or s (14.6% v er su s 18.0%) a nd s ta ge I t um or s (32.7% vs 34.9%), a nd m or e li ke ly t o b e un st ag ed (7.0% vs 5.5%) (p<.0001). U rb an a nd rura l r es id en ts di d n ot diff er s ig nifi ca nt ly r eg ar din g tum or g ra de . U rb an r es id en ts w er e m or e li ke ly t o ha ve e st ro ge n r ec ep to r p os iti ve t um or s (49.9% vs 43.1%, p<.0001) a nd p ro ge ste ro ne r ec ep to r p os iti ve tu m or s (44.0% v s 37.7%, p<.0001). M cL affe rt y et  al . 2011 (40) Illin oi s S ta te C an -ce r R eg ist ry Br ea st c an ce r c as es am on g Il lin oi s r es id en ts in t w o t im e p er io ds, 1988 –92 a nd 1998 –2002. C as es a m on g Il lin oi s r es i-de nts t ha t w er e di ag no se d in n eig hb or in g s ta te s s uc h as M iss our i a nd W is co n-sin a re in cl ud ed 37,392 (1988 –92) 15,454 (1998 –2002) U .S.A. Rura l U rb an C om m ut in g A re as c la ss ifi -ca tio n s ch em e. U rb an r eg io ns: (i) C hi -ca go ci ty , (ii) C hi ca go s ub ur bs, (iii) O th er m et ro po lit an a re as. R ura l a re as: (i) L ar ge to w ns, t ow ns w ith p op ul at io n s iz es f ro m 10,000 –50,000, (ii) S m al l t ow ns w ith p op u-la tio n s iz es 10,000 In b ot h t im e p er io ds, t he r isk o f l at e- st ag e di ag no -sis i s h ig he st a m on g p at ie nts li vin g in t he m os t ur -ba niz ed a re as, a n in di ca tio n o f ur ba n di sa dva nt ag e. Th us, l at e- st ag e di ag no sis d ecr ea se s w ith in cr ea sin g rura lit y, w ith a s lig ht u pt ur n in t he m os t r ura l s et -tin gs. H ow ev er , F or b la ck b re as t c an ce r p at ie nts, t he rura l- ur ba n g ra di en t i s r ev er se d, w ith h ig he r r isks am on g p at ie nts li vin g o uts id e t he ci ty o f C hi ca go . M cL aff er ty & W an g 2009 (39) Illin oi s S ta te C an -ce r R eg ist ry C an ce r c as es f ro m 1998 to 2002 44,070 U .S.A. Rura l U rb an C om m ut in g A re as c la ss ifi ca -tio n. (i) U rb an c or e a re as, (ii) S ub ur ba n ar ea s, (iii) L ar ge t ow n a re as (ur ba niz ed po pu la tio n 10,000 –49,999) a nd (i v) S m al l to w n a nd i so la te d r ura l a re as Th e r isk o f l at e- st ag e di ag no sis i s l es s f or t ho se li v-in g in o th er m et ro po lit an a nd l ar ge t ow n s et tin gs. M en ck et  al . 2001 (35) C alif or ni a C an ce r Re gi str y Br ea st c an ce r c as es di ag no se d b et w ee n 1994 an d 1997 54,541 U .S.A. C oun ty/c oun ty g ro up s: (i) N on ur ba n (c oun -tie s t ha t in cl ud e a t l ea st 10,000 a cr es a nd a po pu la tio n d en sit y <30 in ha bi ta nts/a cr e), (ii) U rb an Lo w er pe rc en ta ge s o f e ar ly di ag no sis br ea st c ar cin o-m as w er e r ep or te d f or t he n on ur ba n c oun ty/c oun ty gro up s. M itc he ll et  al . 2006 (22) W es te rn A us tra lia C an ce r R eg ist ry W om en di ag no se d w ith in va siv e b re as t c an ce r in 1999 in W es te rn A us tra lia 1,025 A us tra lia U rb an a nd r ura l - un de fin ed N o s ig nifi ca nt diff er en ce s in s ta ge a t di ag no sis bet w ee n ur ba n a nd r ura l w om en w ith b re as t c an ce r. ( Co nt in ue d o n p . 1366 )

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Au th or D ata ba se/S our ce Sa mp le P opu la tio n a nd D ata Y ea r Siz e (N) C ou nt ry Rur al- U rb an D efini tio n Prim ar y F in din g M on te lla et  al . 2006 (36) C am pa ni a I ns tit ut e H os pit al T um or Re gi str y W om en di ag no se d w ith br ea st c an ce r b et w ee n Ja nu ar y 1991 a nd D ec em -be r 1993 976 Ita ly Ita lia n C en tra l I ns tit ut e o f S ta tis tics c la s-sifi ca tio n in to ur ba n (in cl udin g s em i- ur ba n) an d r ura l (in cl udin g s em i- r ura l Rura l m un ici pa l w om en a re a t g re at er r isk t o h av e a de la ye d b re as t c an ce r di ag no sis. O lso n et  al . 2012 (37) Br iti sh C olu m bi a C anc er A ge nc y C an ce r R eg ist ry A ll p at ie nts di ag no se d w ith b re as t c an ce r d ur in g 2002 2,869 C an ad a M in ist ry o f H ea lth a dm in ist ra tiv e l oc al au th or iti es. L ar ge/ur ba n if a t l ea st 95% o f its r es id en ts li ve d in a c om m un ity >100,000. Rura l g re at er t ha n 50% o f i ts p op ul at io n re sid ed in c om m un iti es o f <10,000 Pa tie nts f ro m r ura l c om m un iti es p re se nt ed w ith m or e a dva nc ed di se as e (p=.01). Sa ri eg o 2009 (38) The A me ri -ca n C ol le ge o f Su rge ons N at io na l C an ce r D at a B as e A m er ic an C ol le ge o f Sur ge on s N at io na l C an ce r Da ta B as e 811,652 U .S.A. U .S. C en su s B ur ea u r eg io ns: N or th ea st , M id w es t, S ou th, a nd W es t A s ta tis tic al ly s ig nifi ca nt r el at io ns hi p (p<.001) i de n-tifi ed b et w ee n s ta ge o f b re as t c an ce r a t t he t im e o f pr es en ta tio n a nd r eg io n o f t he c oun tr y. Th e g re at es t pe rc en ta ge o f e ar ly- st ag e di se as e (s ta ge I) wa s re co rd ed in t he N or th ea st r eg io n (61%), w he re as th e l ow es t p er ce nt ag e wa s r ec or de d in t he S ou th (57%). C on ve rs el y, a s e xp ec te d, a h ig he r p er ce nt ag e of p at ie nts p re se nt ed w ith a dva nc ed di se as e (s ta ge s III a nd IV ) in t he S ou th w he n c om pa re d w ith t he re st o f t he c oun tr y (11.2% vs 10.3%). Sh ee ha n et  al . 2005 (49) M as sa ch us et ts C an ce r R eg ist ry Fe m al e in va siv e b re as t ca nc er di ag no se d b et w ee n 1988 a nd 1997 46,666 U .S.A. M in or ci vi l di vi sio n (t ow n c od e), ZIP C od e, a nd c en su s t ra ct Re su lts s ho w ed t ha t in ci de nc e i s r el at ed t o ur ba n/ rura l s ta tu s w ith ur ba n t ra cts h av in g a n in ci de nc e ra te o n a ve ra ge 2.7% h ig he r t ha n r ura l t ra ct . W an g et  al . 2008 (11) Illin oi s S ta te C an -ce r R eg ist ry La te s ta ge c an ce r in ci -de nc e in Il lin oi s f ro m 1998 t o 2000 9,077 U .S.A. Rura l U rb an C om m ut in g A re as c la ss ifi ca -tio n. (i) C hi ca go ci ty , (ii) O th er ur ba n, (iii) Su bur ba n, (i v) L ar ge t ow n, (v) S m al l t ow n an d i so la te d r ura l P oo r g eo gra ph ic al a cc es s t o p rim ar y h ea lth c ar e sig nifi ca nt ly in cr ea se s t he r isk o f l at e di ag no sis f or pe rs on s li vin g o uts id e t he ci ty o f C hi ca go .

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Au th or Prim ar y I ss ue(s) A ddr es se d in T erm s of S tag e a t Di ag no sis C on cl us ion A m ey et  al . 1997 (23) Va ri at io n b y G eo gra ph y/L oc at io n Va ri at io n b y R ac e/E th ni ci ty Rura l r es id en ts a re m or e li ke ly t o b e di ag no se d f or b re as t c an ce r l at er in t he di se as e p ro gr es sio n th an t he ir ur ba n c oun te rp ar ts. T he m os t di sa dva nt ag ed a re t he m os t g eo gra ph ic al ly r em ot e, sug ge st in g t ha t p ro xim ity t o s er vi ce s p la ys s om e r ol e in d et er m in in g t he s ta ge a t di ag no sis. Th e di sa dva nt ag e o f r es id en ce a pp lie s o nl y t o b la ck w om en. E ve n t he m os t r ura l w hi te w om en suff er n o s ig nifi ca nt di sa dva nt ag e f ro m r es id en ce . A rm st ro ng & B or m an 1996 (14) G eo gra ph y/L oc at io n Th er e a re s m al l diff er en ce s b et w ee n ra te s o f b re as t c an ce r in r ura l a nd ur ba n r es id en ce s in N ew Ze al an d, a s c om pa re d t o o th er c oun tr ie s. Baa de et  al . 2011 (22) G eo gra ph y/L oc at io n Va ri at io n b y S oci oe co no m ic s ta tu s (S ES) A w om an ’s r isk o f b ein g di ag no se d a s h av in g a dva nc ed b re as t c an ce r d ep en ds o n w he re s he li ve s, sep ara te f ro m t he in di vi du al c ha ra ct er ist ics o f t he w om an h er se lf. Bo th t he r ura lit y a nd s oci o- ec on om ic c ha ra ct er ist ics o f t he g eo gra ph ic al a re a in w hi ch w om en liv ed w er e im po rt an t. T he s oci o- ec on om ic f ac to rs c on tr ib ut in g t o a dva nc ed b re as t c an ce r, exi st in g in b ot h ur ba n a nd r ura l e nv iro nm en ts. Ba rr y & B re en 2005 (25) G eo gra ph y/L oc at io n O ve ra ll, h ea lth c ar e m ar kets in t he U ni te d S ta te s h av e p er fo rm ed im pe rf ec tly in s er vin g p oo r, l es s ed uc at ed , a nd un in sur ed w om en. Be nn et t et  al . 2007 (15) G eo gra ph y/L oc at io n Th e s tu dy di d n ot s ho w a n ur ba n/r ura l di sp ar ity in s ta ge a t di ag no sis o r s ur vi va l f or w om en w ith br ea st c an ce r in N ew Z ea la nd . Bl air et  al . 2006 (16) G eo gra ph y/L oc at io n Pe op le in r ura l a nd ur ba n a re as h av e t he ir c an ce rs di ag no se d a t c om pa ra bl e s ta ge s. C el aya et  al . 2010 (17) G eo gra ph y/L oc at io n M os t w om en li vin g in N ew H am ps hir e h av e g oo d g eo gra ph ic al a cc es s t o m am m og ra ph y, a nd n o in di ca tio n wa s f oun d t ha t t ra ve l t im e o r t ra ve l di st an ce t o m am m og ra ph y s ig nifi ca nt ly a ffe ct ed st ag e a t b re as t c an ce r di ag no sis. H ea lth in sura nc e, a ge a nd m ar ita l s ta tu s w er e t he m aj or f ac to rs as so ci at ed w ith l at er s ta ge b re as t c an ce r. C ho et  al . 2011 (26) G eo gra ph y/L oc at io n Va ri at io n b y R ac e/E th ni ci ty N eig hb or ho od di sa dva nt ag e i s s tr on gl y a ss oci at ed w ith l at e s ta ge di ag no sis o f b re as t c an ce r. Sp ecifi ca lly , b re as t c an ce r p at ie nts r es idin g in n eig hb or ho od s t ha t b ec am e r el at iv el y m or e di sa dva nt ag ed o ve r t he 1990 –2000 d ec ad e e xp er ie nc ed a n a ddi tio na l r isk o f l at e s ta ge di ag no sis. In cr ea sin g c on ce nt ra tio n o f im m ig ra nt p op ul at io ns w ith in n eig hb or ho od s o ve r t he c our se o f th at d ec ad e a ddi tio na lly c on tr ib ut ed t o t he r isk o f l at e s ta ge di ag no sis o f b re as t c an ce r a m on g w om en in t ho se c om m un iti es. ( Co nt in ue d o n p . 1368 )

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Au th or Prim ar y I ss ue(s) A ddr es se d in T erm s of S tag e a t Di ag no sis C on cl us ion C ut hb er ts on et  al . 2009 (27) G eo gra ph y/L oc at io n R ac e/ E thni ci ty SES a nd S ta ge a t D ia gn os is D es pi te un ifo rm b re as t c an ce r c ar e p ro gra m m es w ith in r eg io ns a nd w ith in c oun tr ie s, g eo gra ph ic al diff er en ce s in b re as t c an ce r s ur vi va l a nd s ta ge a t di ag no sis p er sis t. Th e ri sk of di ag no sis w ith la te- st ag e br ea st ca nc er is gr ea te r fo r th os e w om en f ro m et hn ic m in or ity gr ou ps t ha n f or W hi te B rit ish w om en. I n p ar tic ul ar , t he B la ck/B la ck B rit ish a nd C hin es e/O th er et hn ic g ro up s h ad a g re at er t ha n 25% in cr ea se d r isk o f di ag no sis w ith l at e- st ag e b re as t c an ce r. W om en in t he t hr ee m os t d ep riv ed q uin til e g ro up s a ll h av e a s ig nifi ca nt ly in cr ea se d r isk o f di ag no sis w ith t he m os t a dva nc ed s ta ge o f b re as t c an ce r (S ta ge IV ), c om pa re d w ith t he le as t d ep riv ed w om en, w hi ch s ug ge sts t ha t d ep riv ed w om en a re l es s li ke ly t o p ar tici pa te in t he s cr ee nin g p ro gra m m e a nd t ha t t he y a re m or e li ke ly t o ig no re s ym pt om s f or l on ge r. C on se qu en tly , t he d el ay in di ag no sis a nd t re at m en t a ffo rd s t he m os t d ep riv ed w om en t he po ore st p ro gn os is. D al to n et  al . 2006 (28) G eo gra ph y/L oc at io n a nd S ES Re su lt s ho w s a n in cr ea se d r isk f or b ein g di ag no se d w ith a h ig h- ri sk b re as t c an ce r w ith s ho rt er ed uc at io n, w ith l ow er di sp os ab le in co m e, w ith a r es id en ce in r ura l a re as, a nd w ith h av in g n o ac ce ss t o o rg an iz ed m am m og ra ph y s cr ee nin g. D ey et  al . 2010 (42) G eo gra ph y/L oc at io n U rb an w om en h av e a h ig he r in ci de nc e ER+ in ci de nc e t ha n r ura l w om en a nd x en oe st ro ge n m ig ht be a s ig nifi ca nt c au se o f t hi s in d ev el op ed c oun tr ie s a nd ur ba n a re as o f d ev el op in g c oun tr ie s. El lio tt et  al . 2004 (29) G eo gra ph y/L oc at io n Rura l p at ie nts a s c om pa re d w ith t he ir ur ba n c oun te rp ar ts w er e di sa dva nt ag ed in p ro po rt io n st ag ed , s ta ge a t di ag no sis, in iti al m an ag em en t p ro ce dur es, p os t- tr ea tm en t s ur ve ill an ce t es tin g an d p ar tici pa tio n in c an ce r c lin ic al t ri al s. Es s et  al . 2010 (30) G eo gra ph y/L oc at io n Im po rt an t r eg io na l va ri at io ns in t he w ho le c ha in o f c ar e f or b re as t c an ce r p at ie nts (e ar ly di ag no sis, m alig na nc y c on fir m at io n, t he ra peu tic a pp ro ac h a nd t he ra pi es) w er e f oun d a cr os s r eg io ns in Sw itz erl and . Fr ie de ll et  al . 2003 (43) G eo gra ph y/L oc at io n Eff or ts t o im pr ov e s cr ee nin g ra te s s ho ul d b e in cr ea se d in a ll p ar ts o f K en tu ck y, b ut m os t n ee de d im pr ov em en t w ill h av e t o b e in r ura l a nd p ar tic ul ar ly A pp al ac hi an a re as. G re go ri o et  al . 2002 (44) G eo gra ph y/L oc at io n G eo gra ph ic diff er en ce s o f in va siv e a nd in s itu b re as t c an ce r in ci de nc e w er e o bs er ve d. H al l et  al . 2005 (45) G eo gra ph y/L oc at io n Ex ce ss in ci de nc e in ur ba n c oun tie s, b ut a pp ea re d t o b e e xp la in ed t hr oug h t he ur ba n pr ep on de ra nc e o f r eg ist ry h os pi ta ls. H au sa ue r et  al . 2009 (46) G eo gra ph y/L oc at io n a nd S ES H ig he r p ro po rt io ns o f w om en di ag no se d w ith b re as t c an ce r r es id ed in ur ba n t ha n r ura l a nd l ow or m id dl e- th an h ig h- po ve rt y c oun tie s, ir re sp ec tiv e o f in va siv e s ta tu s. ( Co nt in ue d o n p . 1369 )

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Au th or Prim ar y I ss ue(s) A ddr es se d in T erm s of S tag e a t Di ag no sis C on cl us ion H en ry et  al . 2011 (18) G eo gra ph y/L oc at io n R ac e/E th ni ci ty a nd S ES Tra ve l t im e t o di ag no sin g f aci lit y o r n ea re st m am m og ra ph y f aci lit y wa s n ot a d et er m in an t o f la te s ta ge o f b re as t c an ce r a t di ag no sis, a nd b et te r g eo gra ph ic p ro xim ity di d n ot a ss ur e m or e fa vo ra bl e s ta ge di st ri bu tio ns. N on- ge og ra ph ic f ac to rs s uc h a s p ov er ty , ra ce/et hn ici ty , a nd h ea lth in sura nc e in dep en de nt ly pr es en t m or e s ub st an tia l r isks f or a l at e- st ag e di ag no sis o f b re as t c an ce r. H ig gin bo th am et  al . 2001 (31) G eo gra ph y/L oc at io n a nd R ac e Fin din gs s ug ge st t ha t r ura l r es id en ts in M iss iss ip pi a nd r ura l A fr ic an A m er ic an w om en in pa rt ic ul ar , h av e l es s a cc es s t o, o r u tiliza tio n o f, e ar ly c an ce r d et ec tio n p ro gra m s a nd/o r q ua lit y m edi ca l c ar e. H off m an et  al . 2000 (47) G eo gra ph y/L oc at io n R ac e/E th ni ci ty SES a nd F am ily H ist or y A re a o f r es id en ce wa s a m on g t he s tr on ge st d et er m in an ts o f t he s ta ge a t di ag no sis, a nd t he o dd s of h av in g l oc aliz ed ra th er t ha n a dva nc ed b re as t c an ce r wa s m or e t ha n t w of ol d a m on g w om en re sid en t in ur ba n a re as. In ci de nc e ra te s o f b re as t c an ce r in c ol our ed a nd ur ba n w om en w er e h ig he r t ha n in b la ck a nd rura l w om en. Ea rly s ta ge a t di ag no sis wa s a ss oci at ed w ith a h ig he r e du ca tio na l l ev el , b ein g r es id en t in a n ur ba n ar ea, b ein g o n m edi ca l a id a nd h av in g a f am ily h ist or y o f b re as t c an ce r. H ow e et  al . 1992 (32) G eo gra ph y/L oc at io n Th is s tu dy d em on st ra te s ur ba n- rura l diff er en ce s in t um or s ta gin g. T he p ro po rt io n o f un st ag ed br ea st c an ce r in o ur r ura l p op ul at io n wa s m uc h h ig he r (31%) c om pa re d w ith W hi te r ura l w om en in G eo rg ia (7.1%). U ns ta ge d c as es a lso m ad e u p a l ar ge r p ro po rt io n o f o ur ur ba n c as es (fi ve p er ce nt) c om pa re d w ith t he ur ba n W hi te c as es in G eo rg ia (2.5%). H ua ng et  al . 2009 (19) G eo gra ph y/L oc at io n A lth oug h s oci oe co no m ic s ta tu s, ra ce , a nd a ge m ay h el p e xp la in a dva nc ed di ag no se s, l on ge r t ra ve l di st an ce a lso a dv er se ly a ffe cts e ar ly d et ec tio n f or r ura l p op ul at io ns. In no s et  al . 2010 (33) G eo gra ph y/L oc at io n Pl ac e o f r es id en ce a pp ea re d t o b e t he s tr on ge st p re di ct or o f a dva nc ed s ta ge di ag no sis in a ll a ge gr ou ps. Y oun ge r a nd e ld er ly w om en, t ho se li vin g in r em ot e a re as a nd o f l ow er s oci o- ec on om ic st at us s ho ul d b e a ddr es se d w ith s pe cifi c m ea sur es t o p ro m ot e e ar lie r d et ec tio n o f b re as t c an ce r, pa rt ic ul ar ly in v ie w o f c ur re nt e co no m ic diffi cu lti es a nd a s ha rp ly r isin g un em pl oy m en t ra te . K le in et  al . 2011 (20) G eo gra ph y/L oc at io n Re su lt s ho w ed t ha t m et ro po lit an/n on m et ro po lit an diff er en ce s in t um or g ra de s iz e a nd c an ce r st ag e a t di ag no sis w er e n ot s ta tis tic al ly s ig nifi ca nt . K rzyza k et  al . 2010 (48) G eo gra ph y/L oc at io n Th e p ro po rt io n o f e ar ly b re as t c an ce r in P od la sk ie V oi vo ds hi p i s l ow , a nd a lso r el at ed t o p la ce of r es id en ce , a dv er se ly t o t he r ura l p op ul at io n. A lso , t he ur ba n- rura l diff er en tia tio n in b re as t ca nc er in ci de nc e a nd s ta ge di st ri bu tio n s ho ul d b e c on sid er ed a s t he a pp ea ra nc es o f h ea lth in eq ua lit ie s in t he P oli sh p op ul at io n ( Co nt in ue d o n p . 1370 )

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Au th or Prim ar y I ss ue(s) A ddr es se d in T erm s of S tag e a t Di ag no sis C on cl us ion Liff et  al . 1991 (34) G eo gra ph y/L oc at io n R ac e/ Et hni ci ty D iff er en ce s in a cc es s t o o r u tiliza tio n o f e ar ly d et ec tio n m et ho ds m ay c on tr ib ut e t o t he r ura l- ur ba n diff er en tia l in t he e xt en t o f di se as e a t di ag no sis. Bl ac k G eo rg ia r ura l r es id en ts w er e m or e li ke ly t o h av e n on lo ca liz ed m alig na nci es t ha n w hi te s. M ar ko ss ia n & H in es 2012 (21) G eo gra ph y/L oc at io n N o s ig nifi ca nt a ss oci at io n b et w ee n g eo gra ph ic r es id en cy s ta tu s a nd l at e s ta ge b re as t c an ce r di ag no sis. M cL aff er ty et  al . 2011 (40) G eo gra ph y/L oc at io n R ac e/ Et hni ci ty N o e vi de nc e o f r ura l di sa dva nt ag e in e ith er t im e p er io d. I n f ac t t he p er ce nt ag e o f b re as t c an ce r ca se s di ag no se d l at e i s h ig he r in t he h ig hl y ur ba niz ed ci ty o f C hi ca go t ha n i t i s in o th er r eg io ns of t he s ta te- an in di ca tio n o f ur ba n di sa dva nt ag e. Fo r t he b la ck p op ul at io n, r ura l- ur ba n di sp ar iti es w er e m ar ke dl y diff er en t: t he re i s c le ar e vi de nc e of r ura l di sa dva nt ag e a s o pp os ed t o t he ur ba n di sa dva nt ag e o bs er ve d f or t he p op ul at io n a s a w hol e. M cL aff er ty & W an g 2009 (39) G eo gra ph y/L oc at io n In t he m os t r ura l a re as, t he l ow er ra te s o f l at e- st ag e di ag no sis p rim ar ily r efl ec t t he g re at er pr es en ce o f e ld er ly p at ie nts w ho h av e a l ow er r isk o f l at e- st ag e di ag no sis M ec k et  al . 2001 (35) G eo gra ph y/L oc at io n R ac e/ Et hni ci ty SE S Lo w er p er ce nt ag es o f e ar ly di ag no sis b re as t c ar cin om as w er e r ep or te d f or t he n on ur ba n co un ty/c oun ty g ro up s. E ld er ly w om en, H isp an ic a nd b la ck w om en, a nd w om en w ho r es id e in n on ur ba n a re as s ho ul d b e t ar get ed a s h ig h p ri or ity s ub po pu la tio ns f or m am m og ra ph ic scr ee nin g. N on- H isp an ic w hi te w om en w er e di ag no se d w ith 14.4% in s itu b re as t c ar cin om a a nd 51.4% lo ca liz ed b re as t c ar cin om a w ith s m al l t um or s iz e. H isp an ic w om en w er e di ag no se d w ith l ow er le ve ls o f in s itu b re as t c ar cin om a: 12.0%. H isp an ic a nd b la ck w om en w er e di ag no se d w ith l es s lo ca liz ed b re as t c ar cin om a w ith s m al l t um or s iz e: 41.4% a nd 39.1%, r es pe ct iv el y. A sia n/P acifi c Is la nd er w om en w er e di ag no se d w ith 16.6% in s itu b re as t c ar cin om a, a nd 45.1% l oc aliz ed br ea st c ar cin om a w ith s m al l t um or s iz e. Th es e fin din gs w er e s ta tis tic al ly s ig nifi ca nt ( P, 0.0001). Br ea st c ar cin om a wa s di ag no se d a t a n e ar ly s ta ge m os t f re qu en tly in w om en o f y oun ge r a ge , in no n- H isp an ic w hi te w om en o r w om en o f A sia n a nd P acifi c I sla nd a nc es tr y, in w om en w ho liv ed in ur ba n c oun tie s c ha ra ct er iz ed b y h ig he r h ou se ho ld in co m es, a nd in w om en w ho w er e di ag no se d in m or e r ec en t y ea rs. ( Co nt in ue d o n p . 1371 )

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Au th or Prim ar y I ss ue(s) A ddr es se d in T erm s of S tag e a t Di ag no sis C on cl us ion M itc he ll et  al . 2006 (22) G eo gra ph y/L oc at io n D es pi te s im ila rit ie s in m od e o f p re se nt at io n a nd t um or c ha ra ct er ist ics, w om en w ith b re as t ca nc er f ro m r ura l W es te rn A us tra lia e xp er ie nc e a p oo re r s ur vi va l o ut co m e t ha n t he ir ur ba n co un te rp ar ts. M on te lla et  al . 2006 (36) G eo gra ph y/L oc at io n Re sid en ts o f r ura l m un ici pa lit ie s, a s w el l a s p oo rly e du ca te d s ub je cts, a re m or e li ke ly t ha n t he ir re sp ec tiv e c oun te rp ar ts t o h av e a d el ay ed di ag no sis o f b re as t c an ce r. O lso n et  al . 2012 (37) G eo gra ph y/L oc at io n Th e s tu dy i de nt ifi ed di sp ar iti es in u se o f b re as t c an ce r s cr ee nin g, s ta ge di st ri bu tio n a nd b re as t- co ns er vin g t he ra py b y t he p op ul at io n s iz e o f t he p at ie nts ’ l oc al h ea lth a ut ho rit y a t t he t im e o f di ag no sis. Sa ri eg o 2009 (38) G eo gra ph y/L oc at io n/R ac e/E th ni ci ty A r el at io ns hi p e xi sts b et w ee n t he p at te rn o f b re as t c an ce r p re se nt at io n a nd g eo gra ph ic al l oc at io n w ith in t he U ni te d S ta te s. Th e N or th ea st- w ith t he h ig he st p er ce nt ag e o f ur ba n a re as a nd w hi te p op ul at io n- rep or te d t he h ig he st p er ce nt ag e o f e ar ly- st ag e b re as t c an ce r a t p re se nt at io n. C on ve rs el y, t he S ou th- w ith m or e r ura l a nd n on w hi te p op ul at io n- ha d t he h ig he st p er ce nt ag e o f la te r-{\h}s ta ge di se as e. Sh ee ha n et  al . 2005 (49) G eo gra ph y/L oc at io n O nl y o ne a re a o f e xc es s l at e s ta ge b re as t c an ce r di ag no se s wa s i de nt ifi ed in t he s pa ce- tim e an al ys es f or t he fir st t hr ee y ea rs o f t he s tu dy a nd r em ain ed s ta tis tic al ly s ig nifi ca nt a fte r c ova ri at e ad ju st m ent . W an g et  al . 2008 (11) G eo gra ph y/L oc at io n SES/A cc es s Li vin g in a re as w ith p oo r g eo gra ph ic al a cc es s t o p rim ar y c ar e p hy sici an s in cr ea se s t he li ke lih oo d of l at e di ag no sis f or b re as t c an ce r. So ci oc ul tura l b ar ri er s a nd s pa tia l a cc es s t o p rim ar y c ar e (a cc es s) h av e s ta tis tic al ly s ig nifi ca nt as so ci at io ns w ith l at e b re as t c an ce r di ag no sis. A s e xp ec te d, s oci oe co no m ic di sa dva nt ag e a nd so ci oc ul tura l b ar ri er s h av e p os iti ve r el at io ns hi ps, in di ca tin g t ha t p er so ns li vin g in a re as w he re in co m e a nd e du ca tio n l ev el s a re l ow a nd lin gui st ic a nd s oci oc ul tura l b ar ri er s a re h ig h h av e a gr ea te r r isk o f l at e- st ag e di se as e. S pa tia l a cc es s t o p rim ar y c ar e p hy sici an s i s in ve rs el y r el at ed t o la te- s ta ge ri sk.

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1372 Location and stage of breast cancer diagnosis

area (among others) were used in 12 studies16,19,25,26,29,31,32,35,38,44,45,49 while one study34 did

not provide information on the measurement type used.

Using a population- based cancer registry data from Georgia, Liff et al.34 [N = 35,610]

(rural, urban, not defined) revealed rural patients were twice as likely to have unstaged cancer (18.3%) as urban residents (9.6%). Among patients with known stages, rural residents tended to have more advanced stage of the disease. Similarly in a Danish study, Dalton et al.28 [N = 28,765] found that women living in rural areas of Denmark

had a 10% higher odds (OR) of high- risk breast cancer than their urban counterparts (95% CI: 1.02, 1.18), while those living in the capital suburban areas had a 15% lower OR (95% CI: 078, 0.93) than those living in provincial cities.

Long distance travel time to health care services has been shown to influence both access and utilization.11,39,40 There is also an assumption that the greater the distance to

travel, the higher the incidence of psychological morbidity and the poorer the compli-ance with treatment.11,41 A study by Wang and colleagues11 [N = 9,077] on late- stage

breast cancer diagnosis and health care access in Illinois, argued that spatial access to primary care doctors and time travel is critically important in achieving high rates of early breast cancer detection in Illinois and surrounding states. Consequently, living in areas with poor geographical access to primary care physicians increases the likeli- hood of late diagnosis for breast cancer.11

On the other hand, other studies have reported that rural disadvantage does not contribute to distant metastasis breast cancer diagnosis.39,40,42– 49 Gregorio et al.44 [N =

12,415] examined geographical differences in breast cancer according to precise geo-graphic coordinates in Connecticut, 1991–1995. Results showed that breast cancer rates were lower than expected for the rural, outermost counties of northeast (risk of disease among residents relative to elsewhere in the state [RR] was .67; p=.001) and northwest (RR = .88; p = .03) Connecticut. However, a higher incidence rate was found for a predominantly suburban/ urban county of southwest Connecticut (RR = 1.06; p=.004).

Additionally Hall et al.45 [N = 27,989] used the Urban Influence Code (UIC)

mea-surement to analyze urbanization and breast cancer incidence in North Carolina, 1995– 1999. The authors found that, in situ breast cancer incidence rates were high-est in the most urbanized counties among Whites (incidence rate ratio (IRR = 1.60) comparing most urban with most rural) and among non- Whites (IRR = 1.27 for the same comparison). Invasive breast cancer rates were also shown to be higher in the most urban counties for Whites (IRR = 1.18 comparing most urban with most rural) but not non- Whites (IRR = .99 for the same comparison). In another study, using the Gharbiah population- based cancer registry to determine urban- rural differences in breast cancer incidence in Egypt, Dey et al.42 [N = 3,673] suggest that compared with

rural incidences, urban incidences showed that for all hormone receptor status (HRS) was higher in urban areas than rural areas for all age- groups with the urban incidence of estrogen receptor positive (ER+) cancer being the highest in all age- groups.

In contrast to these findings Amey et al.,23 Armstrong and Borman,14 Bennett et al.,15

Blair et al.,16 Celaya et al.,17 Henry et al.,18 Huang et al.,19 Klein et al.,20 Markossian and

Hines,21 and Mitchell et  al.22 found no statistically significant difference in stage of

breast cancer and rural- urban geographic location and distance travel to mammogra-phy screening facility. Markossian and Hines’s.21 [N = 23,500] analysis of Atlanta and

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1373 Williams, Jeanetta, and James Rural Georgia Cancer Registry to assess disparities in late stage diagnosis and rural residence found that rural- urban designation was not significantly associated with late stage breast cancer diagnosis, and late stage did not vary significantly across counties (p=1.0). Additionally, while rural patients had over 22% increased odds of unknown tumor type compared with urban patients, the association was not statistically significant.

Using the rural urban continuum code (RUCC) classification system definition and Florida cancer data system and area resource file, Amey et al.23 [N = 79,946] analyzed

the role of race and residence on stage at breast cancer diagnosis. Results indicated that residents of rural counties that are adjacent to a metropolitan county have the highest percentage (64.5%) of women whose breast cancer was detected at an early stage compared with their urban counterparts. This stood in contrast to the findings of Farley and Flannery51 who reported that adequately served rural counties were better off

than their urban counterparts. The authors also reported that even nonadjacent rural counties had a slightly higher percentage of women diagnosed early (63.1%) than did urban counties (62.9%). However, the last difference was not statistically significant, suggesting proximity to services seems not to inhibit the residents of these most rural counties from receiving a timely diagnosis. Celaya et al.17 [N = 5,966] used the Rural

Urban Commuting Area codes to classify the rural- urban areas in New Hampshire, and found no significant association between rural residence and stage of breast cancer diagnosis. Similarly, Klein et al.20 [N = 4,222] analyzed differences in male breast cancer

stage, tumor size, and stage at diagnosis using metropolitan and non- metropolitan classification and found no statistical differences in proportions of stage or tumor size at diagnosis.

Variation by race or ethnicity. Large disparities in cancer burden and health out-comes exist between Whites and ethnic/ racial minorities. For many decades, African American women experienced a lower incidence rates of breast cancer, but a higher mortality rates than White women.1,2,6 Nonetheless, recent new evidence concerning

disparities in breast cancer has demonstrated that the incidence rates of breast cancer in African American women have increased slightly (by 0.4% per year) while the rates in White women have remained stable.1,2 Rural populations are generally

disadvan-taged in terms of access to medical care services.23,35,38,40,47 Particularly for Black and

Hispanic White women, living in rurally remote areas is likely to affect their cancer health prognosis and survival.4,27 Amey et  al.23 [N = 79,946] revealed that place of

residence had a differential impact on stage at diagnosis across racial groups. While the odds of receiving a late diagnosis for Black women in nonadjacent rural counties are approximately 46% higher than for Black urban residents, it is inconsequential for White women. The study further reported that even low- risk Black women in remote rural counties have approximately a 17% chance of receiving a late diagnosis, and the 12% probability for the most disadvantaged Whites is equivalent to the probability of the most advantaged Black group.

In the United Kingdom (U.K.) Cuthbertson et al.27 [N = 31,551] examined racial

inequalities in breast cancer diagnosis between ethnic minorities and British White women in the Trent region. Results showed that ethnic minority groups have a significantly increased risk of diagnosis with late stage breast cancer relative to the White British group. For the Black/ Black British and Chinese/ Other ethnic groups, risk

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1374 Location and stage of breast cancer diagnosis

of diagnosis with late stage breast cancer is more than 25% higher [RR = 1.28 (95% CI: 1.11, 1.49) and RR = 1.26 (95% CI: 1.04, 1.53)]. Analysis further revealed women residing in nine primary care trusts (PCT) have a significant risk of being diagnosed at late stage, compared with women residing in the Nottingham City PCT. The differ-ences in risk range from an increase of 22% in Doncaster [RR = 1.22 (95% CI: 1:00, 1.48)] to 42% for women in Bassetlaw [RR = 1.42 (95% CI: 1.15, 1.77)] and Leicester City [RR = 1.41 (95% CI: 1.18, 1.17)] PCTs. Liff et al.34 [N = 35,610] also reported that

the relative excess of non- localized malignancies in rural Georgia was almost twice for Blacks (37%) as for Whites (21%). This finding suggests that for Black and other minority populations, the rural- urban disparities are markedly different.40

Consistent with these variations by stage at diagnosis and race, Menck and Mills35

[N = 54,541], descriptive analysis of the California Cancer Registry (1994–1997) showed that non- Hispanic White women were diagnosed with 14.4% in situ breast carcinoma and 51.4% localized breast carcinoma with small tumor size. Hispanic women were diagnosed with lower levels of in situ breast carcinoma (12.0%). Hispanic and Black women were diagnosed with less localized breast carcinoma with small tumor size: 41.4% and 39.1%, respectively. Asian/ Pacific Islander women were diagnosed with 16.6% in situ breast carcinoma, and 45.1% localized breast carcinoma with small tumor size. These differences were statistically significant (p=.0001).

Geographic location variability in rural vs. urban and White vs. Black populations differs within the U.S. The Northeast regions are considered urban and have the largest proportion of Whites. On the other, the Southeast is predominantly rural has the largest number of African Americans.38,52 To assess whether geography matters, Sariego38 [N =

811,652] used the American College of Surgeons’ national cancer database to examine the distribution patterns of breast cancer patterns in the U.S. His findings indicated that a large geographic variation exists in proportion of patients diagnosed in stage with regard to race. Results indicated a statistically significant dependent relationship between race and region with regard to breast cancer tumor size (p<.001). Results indicated a statistically significant dependent relationship between race and region with regard to breast cancer tumor size (p<.001). There were more White women in all four regions of the U.S. than Black women. However, when stage at diagnosis was compared across the U.S. as a whole, a higher percentage of the White women (90.1%) were diagnosed with early stage breast cancer (stages I and II) than of the Black women (85.3%). These differences were statistically significant (p<.001). Similarly, in terms of rural or non-urban population distribution, more women lived in the Midwest (23.6%) than in the South (20.4%). Even though the Midwest has a larger number of women residing in rural areas than the South, more late stage breast cancer was reported among women in the South than among women in the Midwest. This association was also statisti-cally significant (p<.002). Finally, in terms of urbanicity, the Northeast has a larger proportion of urban areas as well as White population than the South. Nonetheless, an inverse relationship exists between early stage at diagnosis and the proportion of rural population.38 Thus, women residing in rural areas (South and West) experienced

more late stage breast cancer diagnosis than those in urban areas.

Variation by socioeconomic status. There is a strong relationship between low socioeconomic status and an increased risk of being on the losing end of health

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dispari-1375 Williams, Jeanetta, and James ties.53 A study by Adler and Newman53 on socioeconomic disparities in health reported

that whether assessed by income, level of education, or occupation, socioeconomic status clearly predicts the health status of an individual. These three measurements of socioeconomic status influence minority populations only indirectly, but it remains important to consider these three main SES determinants of health.

In Australia, Baade et al.24 [N = 18,658] analyzed Queensland Cancer Registry data

to investigate links between geographic remoteness, area disadvantage, individual- level factors and advanced breast cancer. Results showed that women who lived in the most socioeconomically disadvantaged regions were significantly more likely (OR 1.21, 95% CI 1.07, 1.37) than residents of the most economically advantaged areas to be diagnosed with more advanced breast cancer. Further, when place of residence and socioeconomic status were adjusted, the effect of geographic region/ resident and area advantage were statistically significant, and the rates of late detection remained significantly higher for women in the most geographically remote and disadvantaged areas compared with women who lived in the cities. Celaya et al.17 [N = 5,966] and Henry et al.18 [N =

161,619], however, found no association between rural and urban residence and stage at diagnosis. Ceyala et al.17 for instance noted that New Hampshire women were more

likely to be diagnosed with breast cancer at later stages if they lacked private health insurance (p=<.001), were not married (p=<.001) and were older (p=<.001). There was also a borderline association with diagnosis during non- winter and winter months (p=.074). Barry and Breen25 [N = 12,395] revealed that late diagnosis was prevalent in

socially distressed and medically underserved areas.

Henry et al.18 [N = 161,619] analyzed 10 population- based state cancer registries

and suggested that for women living in census tracts with poverty rates greater than 20%, the odds of late stage breast cancer were 1.34 times (95% CI = 1.29, 1.39) greater than the odds for women living in census tracts with poverty rates less than 5%. Other studies have suggested socioeconomic status and residing in urban areas provide an advantage for early diagnosis.28,35,47 Dalton et al.28 [N = 28,765] results showed that the

risk for late diagnosis decreased with increasing education, income, and urbanicity in women diagnosed with breast cancer in Denmark. Similarly, Cho et al.26 [N = 42,714],

Hoffman et al.47 [N = 485] and Wang et al.11 [N = 9,077] also reported an association

between socioeconomic status and late stage breast cancer diagnosis. In a study of the association between changes in immigrant population and the likelihood of distant metastasis stage at diagnosis of breast cancer in Cook County Illinois, Cho et al.26 [N =

42,714] discovered that neighborhood disadvantage is strongly associated with late stage diagnosis of breast cancer. Specifically, breast cancer patients residing in neighborhoods that became relatively more disadvantaged over the 1990-2000 decade experienced an additional risk of late stage diagnosis.26 Hoffman and colleagues47 also [N = 485]

suggested that early stage at diagnosis was associated with a higher educational level, being resident in an urban area, on medical aid and having a family history of breast cancer. Similarly, Wang et al.11 [N = 9,077] revealed that socioeconomic disadvantage

and sociocultural barriers have positive relationships indicating that people living in areas where income and education levels are low and linguistic and sociocultural barriers are high have a greater risk of late stage disease compared with those in high socioeconomic neighborhoods.

References

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