 RESEARCH AND PRACTICE  Variability and Vulnerability at the Ecological Level: Implications for Understanding the Social Determinants of Health | Adam Karpati, MD, MPH, Sandro Galea, MD, MPH, Tamara Awerbuch, PhD, and Richard Levins, PhD Recent research into the role of the social en- Objectives. We examined variability in disease rates to gain understanding of the vironment as a determinant of individual complex interactions between contextual socioeconomic factors and health. health has reinvigorated inquiry into the rela- Methods. We compared mortality rates between New York and California counties in tion between context and health.1–3 Questions the lowest and highest quartiles of socioeconomic status (SES), assessed rate variability regarding mechanism follow naturally from between counties for various outcomes, and examined correlations between outcomes’ this work. A key aspect of many contextual sensitivity to SES and their variability. variables is that they cannot be measured at Results. Outcomes with mortality rates that differed most by county SES were among the individual level; they are essentially group, those whose variability across counties was high (e.g., AIDS, homicide, cirrhosis). Lower- or ecological, characteristics. Contextual fac- SES counties manifested greater variability among outcome measures. tors likely interact with the large number of Conclusions. Differences in health outcome variability reflect differences in SES im- individual characteristics that determine pact on health. Health variability at the ecological level might reflect the impact of stressors on vulnerable populations. (Am J Public Health. 2002;92:1768–1772) health and illness, such as genetics, behavioral choices, and access to medical care. Analyses of community factors attempt to after myocardial infarction.12 For public states in the United States and their county elucidate how context affects the health of in- health surveillance or for epidemiological mortality rates are based on relatively large dividuals.4 Although multilevel analysis al- analysis, variability in population health or its denominators. We excluded from the analysis lows statistical determination of the relative determinants may be a more informative any county in either state with a population effect of individual and community factors,5 characteristic than the absolute level of par- of less than 15000 persons. the manner in which these measures exert ticular components. Similarly, for policy or their effects on public health is likely to be program evaluation, variability might be a Data more complex than is suggested by general- useful measure of the relative effects of dif- We used New York State Department of ized multilevel linear models.6,7 A more accu- ferent interventions. Health and California Department of Health rate understanding of the interplay between We studied the relation between contextual Services data to obtain age-adjusted mortality individuals and their environments requires effects and population health outcomes by ex- rates in each county for the various out- construction of models that take into account amining mortality rates associated with sev- comes.13,14 Table 1 presents the mortality our knowledge of interactions on various lev- eral conditions in counties in New York and rates for the outcomes studied. We selected els, contextual and otherwise, and the fact California. We hypothesized that, first, certain outcomes on the basis of data availability, that system components are interconnected diseases or health outcomes (e.g., traumatic range of clinical conditions, and consistency and likely display feedback loops.8–10 events or communicable diseases) are more with previously published studies. Rates for One approach to understanding complex sensitive to population socioeconomic factors New York were from 1997; rates for Califor- systems is to examine variability among their than are others, reflecting the degree to which nia were either from 1997 alone or were an components. Variability refers to the extent to those outcomes are avoidable or preventable. average of rates from 1995 to 1997. which a characteristic of a complex system Second, the rates of the outcomes that are We obtained the following measures of (e.g., heart rate or stock prices) changes over most sensitive to socioeconomic factors also county socioeconomic status (SES) from the time or space. Variability in a complex system vary the most among counties, reflecting the US Census Bureau: unemployment rate might reflect the effect of external influences wide distribution of responses to the stressors (1997), percentage living in poverty (1995), (“stressors”) through their interaction with the to which populations are exposed. percentage of children aged less than 18 system’s homeostatic mechanisms.11 years living in poverty (1995), median house- Most evaluations of variability in complex METHODS hold income (1995), and high school gradua- physiological systems have been done in the tion rate (1990).15 Percentage living in pov- context of individual clinical characteristics. The unit of analysis for this study was the erty is defined as the percentage of For example, a decrease in heart rate vari- county. We selected New York and California households under the federal poverty thresh- ability has been shown to predict mortality because they are among the most populous old, adjusted for family size and composi- 1768 | Research and Practice | Peer Reviewed | Karpati et al. American Journal of Public Health | November 2002, Vol 92, No. 11  RESEARCH AND PRACTICE  TABLE 1—Mortality Rates from Various Causes in New York and California, 1997.a New York California Outcome Mean Range Range / Mean Mean Range Range / Mean All-cause mortality (all ages) 829 274 0.3 453.8 228.5 0.5 All-cause mortality (≥ 75 y) 21 655 9070 0.4 19 284.2 8714 0.5 All-cause mortality (10–24 y)b 120 310 2.6 75.0 155.1 2.1 Infant mortality 6.7 12.5 1.9 7.0 12.3 1.8 AIDS 4.9 53.7 10.9 3.4 24.6 7.3 Pneumoniac 34.4 65.1 1.9 15.8 22.3 1.4 COPD 42.7 58.3 1.4 23.5 29.6 1.3 Cardiovascular disease 286 234 0.8 89.5 75.0 0.8 Stroke 47.9 64.0 1.6 26.4 22.6 0.9 All neoplastic disease 204 107 0.5 118.8 56.1 0.5 Lung cancer n/a n/a n/a 34.9 32.3 0.9 Female breast cancer n/a n/a n/a 19.1 19.1 1.0 Cirrhosis 8.0 15.6 2.0 10.1 24.7 2.4 Accidentsd 29.2 33.8 1.2 18.5 29.5 1.6 Homicide 2.6 16.7 6.3 6.7 17.7 2.6 Suicide n/a n/a n/a 12.1 18.3 1.5 Note. COPD = chronic obstructive pulmonary disease; n/a = not available. aNew York data from 1997. California data from 1997 or aggregated from 1995–1997. New York rates are age-adjusted to New York State census population 1990. California rates are standardized to US standard population 1940. (As such, these rates are not directly comparable.) All rates are per 100 000 population. bCalifornia—ages 15–24 years. cCalifornia—includes influenza. dCalifornia—motor vehicle accidents only. tion.16 These socioeconomic factors were cho- correlation coefficients between rate ratios Table 1 shows the mean, range, and range di- sen on the basis of data availability and con- and variability measures and examined vari- vided by mean across counties in both states. sistency with previously published studies.11,17 ability in outcomes across counties, stratified In New York, the largest variability in out- by SES. comes was in AIDS mortality (range/mean= Analysis We also calculated smoothed county- 10.9), followed by homicide (6.3), all-cause We analyzed counties in California and specific rates, in which the observed rate in a mortality among persons aged 10–24 years New York separately. We stratified counties county was “stabilized” by replacing it with (2.6), and mortality from cirrhosis (2.0). The into quartiles by each of the SES measures, the weighted average of the county rate and smallest variability was observed in all-cause calculated the average rate of each health all adjacent county rates; weights were pro- mortality across all ages (0.3) and among per- outcome for the bottom and top quartiles, portionate to population size.18 We repeated sons aged more than 75 years (0.4), as well as and obtained the rate ratio for a given health all of the analyses described here on the in mortality from neoplastic disease (0.5) and outcome by comparing counties in the lowest smoothed rate estimates. Finally, we com- mortality from cardiovascular disease (0.8). and highest socioeconomic quartiles. pared outcome rankings and correlations de- In California, variability was highest for We also calculated the variability of each rived using the range-divided-by-mean mea- AIDS (range/mean=7.3), followed by homi- health outcome across all counties in each sure with rankings obtained using 2 other cide (2.6), mortality from cirrhosis (2.4), and state. Following Levins and Lopez, we used variability measures: interquartile range di- mortality among persons aged 15–24 years the range of values divided by the mean vided by mean, and the coefficient of varia- (2.1). The lowest variability was in rates for value as the measure of variability; this mea- tion (SD/mean×100%). all-cause mortality across all ages and for per- sure provides a useful estimate for qualitative sons aged more than 75 years as well as mor- analyses.11 The larger the range divided by RESULTS tality from neoplastic disease (0.5 for each) the mean value, the higher the variability of and mortality from cardiovascular (0.8) or a particular health outcome across counties. We included 61 (98%) of 62 counties in cerebrovascular (0.9) disease. The ordering of No statistical inferences were based on this New York and 53 (91%) of 58 counties in diseases by their intercounty variability was measure of variability. We calculated Pearson California in the analysis. For each outcome, similar between the 2 states. November 2002, Vol 92, No. 11 | American Journal of Public Health Karpati et al. | Peer Reviewed | Research and Practice | 1769  RESEARCH AND PRACTICE  TABLE 2—Relative Mortality Rates Comparing Counties in the Lowest to Highest Quartiles of Economic Indicators, New York and California, 1997. New York California Under-18 % high Row Under-18 % high Row Outcome Employment Poverty poverty Income school grad mean Employment Poverty poverty Income school grad mean All-cause mortality (all ages) 1.05 1.07 1.05 1.05 1.03 1.05 1.16 1.19 1.22 1.21 1.13 1.18 All-cause mortality (≥ 75 y) 0.97 0.97 0.96 1.01 0.95 0.97 0.95 0.94 0.94 0.91 0.92 0.93 All-cause mortality (10–24 y) 1.00 1.41 1.22 1.21 1.47 1.26 1.32 1.16 1.27 1.32 1.46 1.31 Infant mortality 1.04 1.14 1.04 0.96 1.17 1.07 1.24 1.35 1.41 1.29 1.17 1.29 AIDS 3.47 3.13 4.00 1.64 2.59 2.96 0.40 0.68 0.88 0.57 0.68 0.64 Pneumonia 0.92 1.11 1.09 1.10 1.01 1.04 0.93 1.07 1.09 0.88 0.99 0.99 COPD 1.01 1.22 1.10 1.16 1.12 1.12 1.35 1.32 1.34 1.47 1.19 1.33 Cardiovascular disease 1.12 1.06 1.07 1.05 1.04 1.07 1.18 1.28 1.33 1.18 1.23 1.24 Stroke 0.85 1.16 1.13 1.02 0.96 1.02 1.11 1.11 1.17 1.09 1.15 1.12 All neoplastic disease 1.01 0.97 0.97 1.00 0.94 0.98 1.07 1.02 1.05 1.12 1.01 1.05 Lung cancer n/a n/a n/a n/a n/a n/a 1.15 1.11 1.12 1.23 0.99 1.12 Female breast cancer n/a n/a n/a n/a n/a n/a 1.00 0.86 0.85 0.94 0.88 0.90 Cirrhosis 1.42 1.40 1.37 1.20 1.00 1.28 1.13 1.44 1.38 1.43 0.98 1.27 Accidents 0.91 1.25 1.13 1.17 1.23 1.14 2.56 1.71 1.75 2.38 1.76 2.03 Homicide 1.40 1.94 2.23 1.13 1.20 1.58 1.40 2.02 2.61 1.39 1.86 1.85 Suicide n/a n/a n/a n/a n/a n/a 0.93 1.00 0.98 1.06 0.73 0.94 Column mean 1.23 1.36 1.39 1.13 1.20 1.18 1.20 1.27 1.22 1.13 Note. COPD = chronic obstructive pulmonary disease; n/a = not available. Rate ratios comparing mean disease-specific (0.90 for female breast cancer and 1.12 for living in poverty). In New York, the Pearson mortality rates between counties in the lower lung cancer). The highest mean ratios were correlation coefficient was 0.97; in California, and upper quartiles of various socioeconomic for mortality rates from motor vehicle acci- it was 0.70 (0.01 when AIDS was included in markers are shown in Table 2. Rate ratios dents (2.03) and for homicide rates (1.85). the calculation). greater than 1.0 imply that counties with The mean ratio for cirrhosis was 1.27. All- Figure 1 shows the relation between the lower SES have higher disease-specific mor- cause mortality for persons aged more than homicide rates in New York counties and tality than do those with higher SES. 75 years, suicide, pneumonia and influenza their socioeconomic status. Homicide rates for The range of all rate ratios in New York mortality, and female breast cancer mortality each county were plotted against tertiles of was 0.85–4.00. The mean ratios across eco- each had rate ratios of less than 1.10 for all poverty (percentage of persons aged <18 nomic marker categories ranged from 0.98 economic markers. In addition, ratios for years living in poverty). Counties of lower for neoplastic disease to 2.96 for AIDS. Mean AIDS mortality ranged from 0.40 to 0.88. economic status displayed greater variability homicide and cirrhosis mortality ratios were Mortality from all causes in persons aged in their rates of homicide than do counties 1.58 and 1.28, respectively. For all economic 10–24 years had a mean rate ratio of 1.31, with high economic status. The general trend markers, all-cause mortality, all-cause mortal- whereas for persons aged more than 75 years of the relation was linear, with a positive ity for persons aged more than 75 years, and the mean ratio was 0.93. The mean ratios for slope; however, among counties with the low- mortality from neoplasms had ratios less than all outcomes across economic measures est economic status, there were both low and 1.10. Mortality from all causes in persons ranged from 1.13 (high school graduation high rates. aged 10–24 years had a mean rate ratio of rate) to 1.27 (percentage of persons aged Smoothed rates showed less variability than 1.26. The mean ratios for all outcomes across <18 years in poverty). did observed rates (range/mean for all out- economic measures ranged from 1.13 (me- In both states, the variability (range/mean) comes varied from 0.2 to 6.4, compared with dian household income) to 1.39 (percentage of health outcomes across counties was 0.3 to 11.0 in the original analysis); nonethe- of persons aged <18 years in poverty). strongly correlated with the mean ratio of less, the trends and correlations present in the In California, ratios ranged from 0.40 to rates between counties in the lowest and original analysis were preserved. In both New 2.61. The mean ratio across economic indica- highest quartiles of economic status (mea- York and California, AIDS rates and homicide tors for neoplastic disease rates was 1.05 sured by percentage of children <18 years rates continued to display the most variability 1770 | Research and Practice | Peer Reviewed | Karpati et al. American Journal of Public Health | November 2002, Vol 92, No. 11  RESEARCH AND PRACTICE  comes that are sensitive to SES.1920 For exam- ple, in California, lung cancer mortality (largely a consequence of smoking) had a higher mean ratio than did female breast can- 15 cer mortality. In New York, cirrhosis mortality (largely a consequence of alcohol misuse) had a higher rate ratio than did neoplasms. A comparison of age-specific mortality further supports this hypothesis. In New York and 10 California, county rates between economic strata exhibit low ratios for mortality among older persons and high ratios for youth mor- tality. Youth mortality has more potentially 5 modifiable behavioral and social causes at its root than does mortality among older per- sons. The economic sensitivity of AIDS was re- 0 versed in New York and California. In New Low poverty High poverty York State, counties in the lowest economic quartiles had an average of 2.96 times the Tertiles of under-18 poverty AIDS rates of counties in the highest quar- FIGURE 1—Intercounty variability in homicide rates stratified by tertiles of child (under 18 y) tiles, and AIDS is particularly prevalent in poverty, New York State, 1997. poor communities of New York City. By con- trast, in California, the populations with the lowest SES are both urban and rural, and AIDS incidence is more widely distributed in populations of varying SES. (New York AIDS range/mean=6.4, homicide variability of those rates across counties. We Our principal measures of interest were range/mean=3.4; California AIDS range/ hypothesized that the outcomes most sensi- variabilities in outcomes rather than absolute mean=2.0, homicide range/mean=1.4), and tive to SES would also exhibit the most vari- rates. Variability in mortality rates across mortality among persons aged more than 75 ability. Outcomes in both New York and Cali- counties was highest for the outcomes with years and neoplastic disease mortality contin- fornia that displayed high sensitivities to SES larger SES rate ratios. AIDS mortality and ued to display the least (range/mean= were AIDS, homicide, cirrhosis, and acci- homicide were the outcomes with the largest 0.2–0.3). Similarly, as expected, the magni- dents. Outcomes in both states were most variability in the 2 states. Rates for all-cause tudes of variability for each outcome were at- sensitive to the percentage of children living mortality across ages and for mortality in tenuated when the coeffecient of variation or in poverty as a single indicator of SES. older persons, as well as rates for neoplastic the interquartile range divided by mean were All-cause mortality and certain neoplastic disease mortality, exhibited small variability used (ranges 12%.–104% and 0.1–0.9, re- disease mortality rates did not differ greatly and were generally not sensitive to socioeco- spectively, in New York, and 7%–200% and between poorer and wealthier counties. The nomic conditions. 0.2–0.7 in California); the ordering of out- underlying mechanisms for these health out- Although we hypothesized that variability comes by variability, however, remained comes might account for the findings. Dis- reflects system-specific conditions (i.e., the largely unchanged in comparison with the or- eases with an incidence or course that is in- balance among vulnerability, stressors, and dering obtained with the range-divided-by- fluenced by behavioral or environmental protectors), variability may also be the prod- mean statistic (e.g., AIDS and homicide rates factors would be expected to exhibit sensitiv- uct of random events, especially when the remained most variable and all-cause mortal- ity to SES, whereas diseases with genetic or outcome of interest is rare or the population ity and mortality from neoplasms remained other nonmodifiable causes would not. Our within which it occurs is small. Moreover, least variable), as did the strong association analysis is consistent with earlier findings and there may be confounding of the SES– between variability and SES sensitivity. builds on previous small-area analyses in sensitivity/variability relationship if rare Kansas, Saskatchewan, and Cuba.11 events are also more sensitive to SES. To ad- DISCUSSION A general process underlying these obser- dress these possibilities, we repeated all vations has been articulated by Link and Phe- analyses using smoothed county-specific rates, This analysis investigated the effects of lan, who postulated that access to protections which reduce intercounty population variabil- counties’ SES on their mortality rates and the and avoidance of harms underlie health out- ity, as well as robust measures of variability, November 2002, Vol 92, No. 11 | American Journal of Public Health Karpati et al. | Peer Reviewed | Research and Practice | 1771 Homicides per 100 000  RESEARCH AND PRACTICE  which have low sensitivity to outliers. The ob- Health, Harvard School of Public Health, Boston, Mass. increased mortality after acute myocardial infarction. served rate variability was attenuated under Adam Karpati is also with the Epidemiology Program Of- Am J Cardiol. 1987;59:256–262. fice, Centers for Disease Control and Prevention, Atlanta, these circumstances, but trends in health out- 13. New York State Department of Health. AvailableGa. Sandro Galea is also with the Center for Urban Epide- come variability and associations with county- at: http://www.health.state.ny.us/nysdoh/research/re-miologic Studies, New York Academy of Medicine, New search.htm. Accessed April 2, 2002. level SES were preserved. York. Tamara Awerbuch and Richard Levins are with the Department of Population and International Health, Har- 14. California Department of Health Services. Avail- In their examination of ecological factors vard School of Public Health. able at: http://www.dhs.ca.gov/hisp. Accessed April 2, contributing to adverse health effects, Levins Requests for reprints should be sent to Adam Karpati, 2002. and Lopez suggested that the relation be- MD, MPH, Bureau of Community HealthWorks, New York 15. U.S. Bureau of the Census. Available at http:// City Department of Health, 40 Worth St, Room 1607, tween economic deprivation and variability in www.census.gov/hhes/www/saipe/estimatetoc.html.New York, NY 10013 (e-mail: aek3@cdc.gov). health status might be mediated by the vul- Accessed April 2, 2002.This article was accepted January 10, 2002. nerability of populations.11 They cited an ob- 16. Dalaker J. Poverty in the United States: 1998. Washington, DC: US Census Bureau, Current Popula- servation by a geneticist, I. I. Schmalhausen, Contributors tion Reports; 1999. Series P60-207. that “a system at the boundary of its toler- A. Karpati and S. Galea collected the data, performed 17. Cubbin C, Pickle LW, Fingerhut L. Social context ance along any dimension of its existence is the analysis, and wrote the article. T. Awerbuch con- tributed to the study design, oversaw the analysis, and and geographic patterns of homicide among US black more vulnerable to small differences in cir- contributed to the editing of the article. R. Levins con- and white males. Am J Public Health. 2000;90: cumstance along any dimension.”20(p.276) Pop- tributed to the study formulation and design, oversaw 579–587. ulations enduring social or economic depriva- the analysis, and contributed to the editing of the article. 18. Devine O, Parrish RG. Monitoring the health of a population. In: Stroup DF, Teutsch SM, eds. Statistics in tion will be more vulnerable to potential Public Health: Quantitative Approaches to Public Health stressors than will populations of higher sta- Acknowledgments Problems. New York, NY: Oxford University Press; Some of the ideas in this article were developed with tus. 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