Background While low socioeconomic status (SES) has been associated with inferior cancer outcome among adults, its impact in pediatric oncology is unclear. Our objective was therefore to conduct a systematic review to determine the impact of SES upon outcome in children with cancer. Methods We searched Ovid Medline, EMBASE and CINAHL from inception to December 2012. Studies for which survival-related outcomes were reported by socioeconomic subgroups were eligible for inclusion. Two reviewers independently assessed articles and extracted data. Given anticipated heterogeneity, no quantitative meta-analyses were planned a priori. Results Of 7,737 publications, 527 in ten languages met criteria for full review; 36 studies met final inclusion criteria. In low- and middle-income countries (LMIC), lower SES was uniformly associated with inferior survival, regardless of the measure chosen. The majority of associations were statistically significant. Of 52 associations between socioeconomic variables and outcome among high-income country (HIC) children, 38 (73.1%) found low SES to be associated with worse survival, 15 of which were statistically significant. Of the remaining 14 (no association or high SES associated with worse survival), only one was statistically significant. Both HIC studies examining the effect of insurance found uninsured status to be statistically associated with inferior survival. Conclusions Socioeconomic gradients in which low SES is associated with inferior childhood cancer survival are ubiquitous in LMIC and common in HIC. Future studies should elucidate mechanisms underlying these gradients, allowing the design of interventions mediating socioeconomic effects. Targeting the effect of low SES will allow for further improvements in childhood cancer survival.
References
[1]
Braveman PA, Cubbin C, Egerter S, Chideya S, Marehi KS, et al. (2005) Socioeconomic status in health research: One size does not fit all. JAMA 294: 2879–2888. doi: 10.1001/jama.294.22.2879
[2]
Rabi DM, Edwards AL, Svenson LW, Graham MM, Knudston ML, et al. (2010) Association of median household income with burden of coronary artery disease among individuals with diabetes. Circ Cardiovasc Qual Outcomes 3: 48–53. doi: 10.1161/circoutcomes.108.840611
[3]
Frederiksen BL, Osler M, Harling H (2009) Danish Colorectal Cancer Group, Ladelund S, et al (2009) The impact of socioeconomic factors on 30-day mortality following elctive colorectal cancer surgery: a nationwide study. Eur J Cancer 45: 1248–1256. doi: 10.1016/j.ejca.2008.11.035
[4]
Luo ZC, Wilkins R, Kramer MS (2006) Effect of neighbourhood income and maternal education on birth outcomes: A population-based study. CMAJ 174: 1415–1421. doi: 10.1503/cmaj.051096
[5]
Woods LM, Rachet B, Coleman MP (2006) Origins of socio-economic inequalities in cancer survival: a review. Annals of Oncology 17: 5–19. doi: 10.1093/annonc/mdj007
[6]
Tang Y, Xu X, Song H, Yang S, Shi S, et al. (2008) Long-term outcome of childhood acute lymphoblastic leukemia treated in China. Pediatr Blood Cancer 51: 380–386. doi: 10.1002/pbc.21629
[7]
Mostert S, Sitaresmi MN, Gundy CM, Sutaryo, Veerman AJ (2006) Influence of socioeconomic status on childhood acute lymphoblastic leukemia treatment in Indonesia. Pediatrics 118: e1600–1606. doi: 10.1542/peds.2005-3015
[8]
McWhirter WF, Smith H, McWhirther KM (1983) Social class as a prognostic variable in acute lymphoblastic leukemia. Med J Aust 2: 319–321.
[9]
Schillinger JA, Grosclaude PC, Honjo S, Quinn MJ, Sloggett A, et al. (1999) Survival after acute lymphoblastic leukaemia: Effects of socioeconomic status and geographic region. Arch Dis Child 80: 311–317. doi: 10.1136/adc.80.4.311
[10]
Charalampopoulou A, Petridou E, Spyridopoulos T, Dessypris N, Oikonomou A, et al. (2004) An integrated evaluation of socioeconomic and clinical factors in the survival from childhood acute lymphoblastic leukaemia: a study in Greece. European Journal of Cancer Prevention 13: 397–401. doi: 10.1097/00008469-200410000-00007
[11]
Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Medicine 6.
[12]
Harvey RC, Mullighan CG, Chen IM, Wharton W, Mikhail FM, et al. (2010) Rearrangement of CRLF2 is associated with mutation of JAK kinases, alternation if IKZF1, Hispanic/Latino ethnicity, and a poor outcome in pediatric B-progenitor acute lymphoblastic leukemia. Blood 115: 5312–5321. doi: 10.1182/blood-2009-09-245944
[13]
Landis R, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33: 159–174. doi: 10.2307/2529310
[14]
Marmot MG (2003) Understanding social inequalities in health. Persp Biol Med 46: S9–S23. doi: 10.1353/pbm.2003.0056
[15]
Hayden JA, Cote P, Bombardier C (2006) Evaluation of the quality of prognosis studies in systematic reviews. Ann Intern Med 144: 427–437. doi: 10.7326/0003-4819-144-6-200603210-00010
[16]
Simon C, Zyzanski SJ, Eder M, Raiz P, Kodish ED, et al. (2003) Groups potentially at risk for making poorly informed decisions about entry into clinical trials for childhood cancer. J Clin Oncol 21: 2173–2178. doi: 10.1200/jco.2003.03.003
[17]
Drotar D, Miller V, Willard V, Anthony K, Kodish E (2004) Correlates of parental participation during informed consent for randomized clinical trials in the treatment of childhood leukemia. Ethics Behav 14: 1–15. doi: 10.1207/s15327019eb1401_1
[18]
Mostert S, Arora RS, Arreola M, Bagai P, Friedrich P, et al. (2011) Abandonment of treatment for childhood cancer: Position statement of a SIOP PODC Working Group. Lancet Oncol 12: 719–720. doi: 10.1016/s1470-2045(11)70128-0
[19]
The World Bank (2012) Data - A Short History. The World Bank.
[20]
Rockhill B, Newman B, Weinberg C (1998) Use and misuse of population attributable fractions. Am J Public Health 88: 15–19. doi: 10.2105/ajph.88.1.15
[21]
Bonilla M, Gupta S, Vasquez R, Fuentes SL, deReyes G, et al. (2010) Predictors of outcome and methodological issues in children with acute lymphoblastic leukaemia in El Salvador. European Journal of Cancer 46: 3280–3286. doi: 10.1016/j.ejca.2010.07.001
[22]
Carlos L-L, Roberto R-L, Victor T-G, Carlos H-G, Eduardo L-P (2002) Risk of dying of retinoblastoma in Mexican children. Medical & Pediatric Oncology 38: 211–213. doi: 10.1002/mpo.1314
[23]
Dinand V, Dawar R, Arya LS, Unni R, Mohanty B, et al. (2007) Hodgkin’s lymphoma in Indian children: Prevalence and significance of Epstein-Barr virus detection in Hodgkin’s and Reed-Sternberg cells. European Journal of Cancer 43: 161–168. doi: 10.1016/j.ejca.2006.08.036
[24]
Mostert S, Sitaresmi MN, Gundy CM, Janes V, Sutaryo, et al (2010) Comparing childhood leukaemia treatment before and after the introduction of a parental education programme in Indonesia. Archives of Disease in Childhood 95: 20–25. doi: 10.1136/adc.2008.154138
[25]
Tang Y, Xu X, Song H, Yang S, Shi S, et al. (2008) Long-term outcome of childhood acute lymphoblastic leukemia treated in China. Pediatric Blood & Cancer 51: 380–386. doi: 10.1002/pbc.21629
[26]
Viana MB, Fernandes RA, de Carvalho RI, Murao M (1998) Low socioeconomic status is a strong independent predictor of relapse in childhood acute lymphoblastic leukemia. International Journal of Cancer - Supplement 11: 56–61.
[27]
Wang YR, Jin RM, Xu JW, Zhang ZQ (2011) A report about treatment refusal and abandonment in children with acute lymphoblastic leukemia in China, 1997–2007. Leukemia Research 35: 1628–1631. doi: 10.1016/j.leukres.2011.07.004
[28]
Gupta S, Bonilla M, Fuentes SL, Caniza M, Howard SC, et al. (2009) Incidence and predictors of treatment-related mortality in paediatric acute leukaemia in El Salvador. British Journal of Cancer 100: 1026–1031.
[29]
Kulkarni KP, Marwaha RK (2010) Pattern and implications of therapy abandonment in childhood acute lymphoblastic leukemia. Asian Pacific Journal of Cancer Prevention: Apjcp 11: 1435–1436.
[30]
Pedrosa MF, Pedrosa F, Lins MM, Pontes Neto NT, Falbo GH (2007) Non-Hodgkin’s lymphoma in childhood: clinical and epidemiological characteristics and survival analysis at a single center in Northeast Brazil. Jornal de Pediatria 83: 547–554. doi: 10.2223/jped.1726
[31]
Birch JM, Pang D, Alston RD, Rowan S, Geraci M, et al. (2008) Survival from cancer in teenagers and young adults in England, 1979–2003. British Journal of Cancer 99: 830–835.
[32]
Croucher C, Whelan JS, Moller H, Davies EA (2009) Trends in the incidence and survival of cancer in teenagers and young adults: regional analysis for South East England 1960–2002. Clinical Oncology (Royal College of Radiologists) 21: 417–424. doi: 10.1016/j.clon.2009.02.006
[33]
Hsieh MH, Meng MV, Walsh TJ, Matthay KK, Baskin LS (2009) Increasing incidence of neuroblastoma and potentially higher associated mortality of children from nonmetropolitan areas: analysis of the surveillance, epidemiology, and end results database. Journal of Pediatric Hematology/Oncology 31: 942–946. doi: 10.1097/mph.0b013e3181bcc809
[34]
Kent EE, Sender LS, Largent JA, Anton-Culver H (2009) Leukemia survival in children, adolescents, and young adults: influence of socioeconomic status and other demographic factors. Cancer Causes & Control 20: 1409–1420. doi: 10.1007/s10552-009-9367-2
[35]
McWhirter WR, Smith H, McWhirter KM (1983) Social class as a prognostic variable in acute lymphoblastic leukaemia. Medical Journal of Australia 2: 319–321.
[36]
Metzger ML, Castellino SM, Hudson MM, Rai SN, Kaste SC, et al. (2008) Effect of race on the outcome of pediatric patients with Hodgkin’s lymphoma. Journal of Clinical Oncology 26: 1282–1288. doi: 10.1200/jco.2007.14.0699
[37]
Petridou E, Kosmidis H, Haidas S, Tong D, Revinthi K, et al. (1994) Survival from childhood leukemia depending on socioeconomic status in Athens. Oncology 51: 391–395. doi: 10.1159/000227372
[38]
Szklo M, Gordis L, Tonascia J, Kaplan E (1978) The changing survivorship of white and black children with leukemia. Cancer 42: 59–66. doi: 10.1002/1097-0142(197807)42:1<59::aid-cncr2820420109>3.0.co;2-j
[39]
Walters TR, Bushore M, Simone J (1972) Poor prognosis in Negro children with acute lymphocytic leukemia. Cancer 29: 210–214. doi: 10.1002/1097-0142(197201)29:1<210::aid-cncr2820290131>3.0.co;2-u
[40]
Lightfoot TJ, Johnston WT, Simpson J, Smith AG, Ansell P, et al. (2012) Survival from childhood acute lymphoblastic leukaemia: the impact of social inequality in the United Kingdom. European Journal of Cancer 48: 263–269.
[41]
Rondelli R, Dini G, De Rosa M, Quarello P, Bisogno G, et al.. (2011) Foreign children with cancer in Italy. Italian Journal of Pediatrics 37.
[42]
Syse A, Lyngstad TH, Kravdal O (1870) Is mortality after childhood cancer dependent on social or economic resources of parents? A population-based study. International Journal of Cancer 130: 1870–1878. doi: 10.1002/ijc.26186
[43]
Youlden DR, Baade PD, Valery PC, Ward LJ, Green AC, et al. (1649) Differentials in survival for childhood cancer in Australia by remoteness of residence and area disadvantage. Cancer Epidemiology, Biomarkers & Prevention 20: 1649–1656. doi: 10.1158/1055-9965.epi-11-0432
[44]
Bhatia S, Sather HN, Heerema NA, Trigg ME, Gaynon PS, et al. (2002) Racial and ethnic differences in survival of children with acute lymphoblastic leukemia. Blood 100: 1957–1964. doi: 10.1182/blood-2002-02-0395
[45]
Galobardes B, Lynch J, Smith GD (2007) Measuring socioeconomic position in health research. British Medical Bulletin 81: 21–37. doi: 10.1093/bmb/ldm001
[46]
Bonilla M, Rossell N, Salaverria C, Gupta S, Barr R, et al. (2009) Prevalence and predictors of abandonment of therapy among children with cancer in El Salvador. International Journal of Cancer 125: 2144–2146. doi: 10.1002/ijc.24534
[47]
Hord MH, Smith TL, Culbert SJ, Frankel LS, Pinkel DP (1996) Ethnicity and cure rates of Texas children with acute lymphoid leukemia. Cancer 77: 563–569. doi: 10.1002/(sici)1097-0142(19960201)77:3<563::aid-cncr20>3.0.co;2-1
[48]
Bhatia S, Landier W, Shangguan M, Hageman L, Schaible AN, et al. (2012) Nonadherence to oral mercaptopurine and risk of relapse in Hispanic and non-Hispanic white children with acute lymphoblastic leukemia: A report from the Children’s Oncology Group. J Clin Oncol 30: 2094–2101. doi: 10.1200/jco.2011.38.9924
[49]
Borowitz MJ, Devidas M, Hunger SP, Bowman WP, Carroll A, et al. (2008) Clinical significance of minimal residual disease in childhood acute lymphoblastic leukemia and its relationship to other prognostic factors: a Children’s Oncology Group study. Blood 111: 5477–5485. doi: 10.1182/blood-2008-01-132837
[50]
Chen I-M, Harvey RC, Mullighan CG, Gastier-Foster J, Wharton W, et al. (2012) Outcome modeling with CRLF2, IKZF1, JCK, and minimal residual disease in pediatric acute lymphoblastic leukemia: A Children’s Oncology Group Study. Blood 119: 3512–3522. doi: 10.1182/blood-2011-11-394221
[51]
Stiller C, Kroll ME, Boyle PJ, Feng Z (2008) Population mixing, socioeconomic status and incidence of childhood acute lymphoblastic leukaemia in England and Wales: analysis by census ward. Br J Cancer 98: 1006–1011.