- Email: [email protected]
National Rates of Diarrhea-Associated Ambulatory Visits in Children
National Rates of Diarrhea-Associated Ambulatory Visits in Children Stephen J. Pont, MD, MPH, Carlos G. Grijalva, MD, MPH, Marie R. Griffin, MD, MPH, Theresa A. Scott, MS, and William O. Cooper, MD, MPH Objective To estimate national rates of ambulatory healthcare visits due to diarrhea- and rotavirus-associated illness before the introduction of rotavirus vaccine. Study design Annual rates for diarrhea-associated visits in children age < 5 years were calculated for 1995-2004 using National Ambulatory Medical Care Survey, National Hospital Ambulatory Medical Care Survey, and US Census Bureau data. Rates by age, race, and time period were compared using Poisson regression. Results Annual rates of outpatient and emergency department (ED) visits for 1995-2004 were 955 (95% confidence interval [CI] = 803 to 1107) and 314 (95% CI = 278 to 350)/10 000 person-years, respectively. Annual outpatient (P = .470) and ED (P = .734) visit rates remained stable from 1995 to 2004. Outpatient visits were less frequent in African Americans than Caucasians (716/10 000 person-years vs 1012/10 000 person-years; P < .05; incidence rate ratio [IRR] = 0.71; 95% CI = 0.51 to 0.99), whereas ED visits were more frequent in African Americans than Caucasians (520/10 000 person-years vs 286/10 000 person-years; P < .05; IRR = 1.83; 95% CI = 1.58 to 2.11). Approximately 29% of outpatient diarrhea-associated outpatient visits (273/10 000 person-years; 95% CI = 145 to 401) and 25% of diarrhea-associated ED visits (78/10 000 person-years; 95% CI = 64 to 83) were due to rotavirus. Conclusions Diarrhea- and rotavirus-associated illness is associated with significant healthcare utilization. Future studies are needed to investigate factors causing differences in healthcare use by race and to explore the impact of the rotavirus vaccine. (J Pediatr 2009;155:56-61).
A
mong US children age < 5 years, diarrhea-associated illness leads to approximately 220 000 hospitalizations (9% of all hospitalizations in this age group) and an estimated 300 deaths annually.1,2 In addition, gastroenteritis and dehydration trail only asthma as the leading reason for hospital admission in US children age 1 to 5 years.1,2 Diarrhea-associated illness entails substantial costs to society. Rotavirus is the leading cause of diarrhea in US children; rotavirus diarrhea alone is associated with an estimated annual healthcare cost of $319 million and a total annual cost to society of $893 million.3 Even though diarrhea-associated healthcare utilization occurs predominantly in outpatient clinics and emergency departments (EDs),3 previous studies have focused on hospitalization, and current estimates of national rates of ambulatory visits are limited. Contemporary rates are needed, because a rotavirus vaccine has recently been recommended for all US infants.4 The determination of incidence rates and trends present before the introduction of rotavirus vaccine will allow for an appropriate evaluation of the vaccine’s impact on diarrhea-associated illness. Furthermore, although differences in morbidity, mortality, and healthcare utilization patterns due to diarrhea between Caucasian and African-American children have been reported, whether these differences also exist for ambulatory visits in a nationally representative population remains unknown.5-7 We undertook the present study with the goals of estimating US rates of ambulatory healthcare encounters due to diarrhea- and rotavirus-associated illness before the introduction of rotavirus vaccine; assessing changes in these rates over time; and determining prevaccine healthcare utilization differences by race and age.
Methods Data were obtained from the National Ambulatory Medical Care Survey (NAMCS) and the National Hospital Ambulatory Medical Care Survey (NHAMCS) for 1995-2004. These surveys are conducted by the National Center for Health Statistics (NCHS) to provide estimates of ambulatory healthcare services rendered to the US population by both non–federally employed office-based physicians enFrom the Department of Pediatrics, University of Texas gaged primarily in patient care (NAMCS) and in the hospital EDs and outpatient CI ED ICD-9-CM IRR NAMCS NCHS NHAMCS
Confidence interval Emergency department International Classification of Diseases, Ninth Revision, Clinical Modification Incidence rate ratio National Ambulatory Medical Care Survey National Center for Health Statistics National Hospital Ambulatory Medical Care Survey
Medical Branch-Austin Programs (S.P.) and Department of Kinesiology and Health Education, College of Education (S.P.), University of Texas, Austin, TX and the Departments of Preventive Medicine (C.G., M.G.), Biostatistics (T.S.), and Pediatrics (W.C.), Vanderbilt University, Nashville, TN
Supported by an Academic Pediatric Association Young Investigator Award and a National Institutes of Health National Research Service Award Grant (T32 HS01383303) The authors declare no conflicts of interest related to this work. 0022-3476/$ - see front matter. Copyright Ó 2009 Mosby Inc. All rights reserved. 10.1016/j.jpeds.2009.01.075
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Vol. 155, No. 1 July 2009 departments of noninstitutional general and short-stay hospitals, exclusive of federal, military, and Veterans Administration hospitals (NHAMCS).8-10 The NAMCS and NHAMCS collect information about healthcare providers, services rendered, and patient characteristics. Survey information is collected through a multistage sampling procedure that includes healthcare facilities or providers and patient records and is designed to produce unbiased estimates for the US population.9,10 Data collected directly from the healthcare sites and/or their records identify healthcare encounters, with the physician–patient encounter or visit as the basic sampling unit.9,10 Visits conducted solely for administrative purposes and visits in which no medical care was provided are excluded. For the NAMCS, a systematic random sample of office visits from a randomly assigned 1-week reporting period is obtained from selected physicians.9 The samples are then weighted to be nationally representative. The sampling and data collection methodologies of the NHAMCS are similar to those of the NAMCS; within emergency service areas or outpatient department clinics, patient visits are selected systematically over a randomly assigned 4-week reporting period for the NHAMCS.10 The unweighted item nonresponse rate for both surveys is generally # 5%.8 For each encounter, up to 3 diagnoses were recorded using the International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM).11 Using NAMCS and NHAMCS data, all ICD-9-CM–coded diarrhea-associated visits were identified that met the following requirements: either the visit had a diagnosis of diarrhea (see Appendix 1) as the primary diagnosis or the visit had a primary diagnosis of dehydration (ICD-9-CM 276.5) or nausea and vomiting (ICD-9-CM 787.0), with a diarrhea visit diagnosis code listed as the second or third diagnosis.5 Visits occurring between 1995 and 2004 for children age < 5 years were included. Each visit was characterized according to the child’s age (0 to 11 months, 1 to 2 years, or 3 to 4 years), ethnicity (Latino, non-Latino, or missing), race (Caucasian, African American, or other), sex, expected source of payment (private insurance, Medicaid/SCHIP, or other, including Medicare, worker’s compensation, self-pay, no charge/charity, and unknown), and month and calendar year of the visit. Statistical Analysis The outcome of interest was the annual rate of diarrhea-associated healthcare encounters in the outpatient and ED settings. Numerators for rates were calculated for each stratum on the basis of our definition of a diarrhea visit, and the denominator was the US Census Bureau population estimate for July 1 of each study year.12 The NCHS recommends a minimum unweighted cell size of 30 when using NAMCS and NHAMCS data, to provide robust national estimates.9,10 To meet this requirement, study years were collapsed into 2-year groupings: 1995-1996, 1997-1998, 1999-2000, 20012002, and 2003-2004. Standard errors of the number of diarrhea-associated visits for compared stratum were estimated, taking into account
the multistage sampling designs of the NAMCS and NHAMCS, The relative standard errors were < 30% for all estimates, in accordance with NCHS recommendations.13,14 Estimated rates were compared using rate ratios and standard errors, and along with the delta method were used to compute 95% confidence intervals for all rate ratios.13 In addition, a test for linear trend was performed to assess for rate changes with time over the five 2-year study periods. The rotavirus disease burden was estimated using the winter residual excess morbidity method described by Jin et al.15 This method subtracts the diarrhea-associated visit rates from the months with less rotavirus activity (June through November) from those from the months with greater rotavirus activity (December through May). The estimated rotavirus burden is the difference between the ‘‘summer’’ and ‘‘winter’’ diarrhea-associated visit rates. Because children age < 5 years are most susceptible to severe diarrhea-associated illness, the rotavirus disease burden was estimated in children age < 3 years and in those age < 5 years. Rate differences by race controlling for age were calculated across the entire study period, to provide robust estimates. In a separate model, diarrhea rates in Caucasians and African Americans were compared, controlling for study period. All analyses were performed using Stata 9.2 (StataCorp, College Station, Texas). All survey data released by the NCHS were deidentified, and the study protocol was reviewed and approved by Vanderbilt University’s Institutional Review Board.
Results Annual Rates and Trends Between 1995 and 2004, US children age < 5 years experienced approximately 18 495 002 outpatient visits and 6 078 147 ED visits due to diarrhea-associated illness. Children age < 3 years accounted for 82% of these visits. Caucasian and African-American children represented approximately 80% and 15% of the visits, respectively. In 53% of the visits, private insurance was the primary payment source. The demographics for the eligible population were similar for each study year, except that the number of children in the ‘‘other’’ race category, the number of children age 0 to 11 months, and the number of children of Hispanic ethnicity increased over the study period. Table I presents demographic data for the children experiencing a diarrhea-associated ambulatory healthcare visit during the study period. Infants age 0 to 11 months experienced the highest rates of healthcare encounters for diarrhea-associated illness, with 1613 (95% CI = 1293 to 1932) outpatient visits/10 000 person-years and 605 (95% CI = 518 to 693) ED visits/10 000 person-years. Children age 1 to 2 years accounted for 1165 (95% CI = 927 to 1403) outpatient visits and 339 (95% CI = 293 to 385) ED visits per 10 000 person-years, whereas children age 3 to 4 years accounted for 417 (95% CI = 307 to 526) outpatient visits and 143 (95% CI = 116–170) ED visits per 10 000 person-years. Figure 1 displays annualized visit rates for diarrhea-associated illness for 1995-2004 by 2-year period. Outpatient visits 57
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Table I. Outpatient and ED visits for diarrhea-associated illness among US children age < 5 years, 1995-2004 Total Age 0-11 months 1-2 years 3-4 years Race Caucasian African American Other Sex Female Male Ethnicity Non-Hispanic/Latino Hispanic/Latino Missing Source of payment* Total* Private insurance Medicaid/SCHIP Other†
Outpatient
ED
Total
18 495 002 (100.0%)
6 078 147 (100.0%)
24 573 149 (100.0%)
6 277 916 (33.9%) 8 980 311 (48.6%) 3 236 775 (17.5%)
2 355 782 (38.8%) 2 614 257 (43.0%) 1 108 108 (18.2%)
8 633 698 (35.1%) 11 594 568 (47.2%) 4 344 883 (17.7%)
15 262 454 (82.5%) 2 099 989 (11.4%) 1 132 559 (6.1%)
4 313 481 (71.0%) 1 525 246 (25.1%) 239 420 (3.9%)
19 575 935 (79.7%) 3 625 235 (14.8%) 1 371 979 (5.6%)
9 343 282 (50.5%) 9 151 720 (49.5%)
2 787 299 (45.9%) 3 290 848 (54.1%)
12 130 581 (49.4%) 12 442 568 (50.6%)
11 913 161 (64.4%) 4 863 719 (26.3%) 1 718 122 (9.3%)
3 952 476 (65.0%) 1 565 574 (25.8%) 560 097 (9.2%)
15 865 637 (64.6%) 6 429 293 (26.2%) 2 278 219 (9.3%)
14 877 282 (100%) 8 717 810 (58.6%) 3 925 244 (26.4%) 2 234 228 (15.0%)
4 738 469 (100%) 1 603 848 (33.8%) 2 152 553 (45.4%) 982 068 (20.7%)
19 615 751 (100%) 10 321 658 (52.6%) 6 077 797 (31.0%) 3 216 296 (16.4%)
Source: NAMCS and NHAMCS. *Summed across 1997-2004. †Includes Medicare, worker’s compensation, self-pay, no charge/charity, and unknown (missing).
resulting from diarrhea-associated illnesses among all children remained stable (P = .470), with rates of 932 (95% CI = 631 to 1233) visits/10 000 person-years for 1995-1996 and 1011 (95% CI = 540 to 1483) visits/10 000 person-years for 2003-2004. ED visits also remained stable (P = .734), with rates of 345 (95% CI = 263 to 427) visits/10 000 person-years for 1995-1996 and 327 (95% CI = 253 to 401) visits/10 000 person-years for 2003-2004. For the period 1995-2004, children age < 5 years experienced 955 (95% CI = 803 to 1107) outpatient visits and 314 (95% CI = 278 to 350) ED visits/ 10 000 person-years, and those age < 3 years had 1315 (95% CI = 1099 to 1532) outpatient visits and 428 (95% CI = 377 to 480) ED visits/10 000 person-years. Utilization Differences by Race The rate of total ambulatory visits (outpatient and ED visits combined) was comparable in Caucasians and African Americans (1298/10 000 person-years [95% CI = 1107 to 1490] vs 1236/10 000 person-years [95% CI = 985 to 1486]). After adjusting for age and study year, African-American children had a lower visit rate for diarrhea-associated illness than Caucasian children in the outpatient clinic setting (716/10 000 person-years [95% CI = 496 to 936) vs 1012/10 000 person-years [95% CI = 830 to 1194]; IRR = 0.71; 95% CI = 0.51 to 0.99), but a higher visit rate for diarrhea-associated illness in the ED setting (520/10 000 person-years [95% CI = 425 to 615] vs 286/10 000 person-years [95% CI = 250 to 322]; IRR = 1.83; 95% CI = 1.58 to 2.11). Because US Census data (used as the denominator in rate calculations) contain no information regarding health insurance status, we were unable to control for source of payment in our regression analyses. Instead, to explore the influence of insurance status on site of utilization, we evaluated the proportion of diar58
rhea-associated visits that occurred in each setting by race and source of payment (Table II), then evaluated the visit setting for African-American and Caucasian children with private insurance and Medicaid/SCHIP by calculating row percentages from the data presented in Table II. Of all 1 118 657 diarrhea-associated visits by African-American children with private insurance, 26% (95% CI = 18% to 34%), or 286 441 visits, were to EDs. During the study period, a total of 8 510 201 diarrhea-associated visits were made by Caucasian children with private insurance; 15% of these visits (95% CI = 12% to 18%) , or 1 254 165 visits, were to EDs. Of all diarrhea-associated visits by African-American children with Medicaid/SCHIP (1 214 724), 55% (95% CI = 43% to 68%), or 673 926 visits, were to EDs, compared with 31% (95% CI = 25% to 36%), or 1 395 089 visits, for Caucasian children with Medicaid/SCHIP. Visits Due to Rotavirus Figure 2 shows the seasonal variation for diarrhea-associated healthcare utilization, with increased visit rates during the winter, apparently driven by the rotavirus disease burden. Using the winter excess residual method, we estimated the proportion of diarrhea-associated visits due to rotavirus for children age < 3 years and < 5 years. We estimate that rotavirus contributed to 29% (273/10 000 person-years [95% CI = 145 to 401]) of the outpatient diarrhea-associated visits, or 5 285 636 visits, and to 25% (78/10 000 person-years [95% CI = 64 to 83]) of the ED diarrhea-associated visits, or 1 519 661 visits, in children age < 5 years. In children age < 3, for 19952004, we estimate that rotavirus contributed to 29% of the outpatient diarrhea-associated visits, or 4 365 821 visits, and to 28% of the diarrhea-associated ED visits, or 1 386 245 visits. Pont et al
ORIGINAL ARTICLES
Visit Rate (N per 10,000 children per year)
July 2009
and a high proportion of diarrhea-associated healthcare visits and contributed to approximately 750 000 ambulatory visits annually in children age <5 years. The recently released rotavirus vaccine may produce a substantial reduction in these healthcare visits, and future studies should be performed to quantify this vaccine’s impact. Our analysis of 10 years of nationally representative data indicates that Caucasians had a significantly greater (40%) rate of healthcare utilization for diarrhea-associated illness in outpatient clinics than African Americans, but that African Americans utilized the ED for diarrhea-associated illness at nearly double the rate of Caucasians. The total rate of ambulatory healthcare utilization due to diarrhea-associated illness was comparable in African-American and Caucasian children. We also found differences in site of healthcare visit for diarrhea-associated illness by source of payment. Although the available data limited our ability to generate and analyze rates by insurance status, our findings suggest an association between insurance status and site of care, with a larger proportion of visits to the ED by children with Medicaid/SCHIP compared with those with private insurance. Our data suggest that both race and insurance status may influence the site of care for diarrhea-associated illness in children. Differing rates of healthcare coverage, access to outpatient clinics, cultural attitudes, disease susceptibility and acuity, and perceived or experienced racial disparities might contribute to these differences in healthcare utilization. Fischer et al7 recently reported that in the United States, African-American children age < 5 years have a significantly greater risk of dying from rotavirus compared with Caucasian children in this age group, with a risk ratio of 2.0. Glass et al6 reported an increased risk of death from diarrheal illness in African-American children from the southern US. Further study is warranted. Differential healthcare utilization by race, with proportionally decreased outpatient clinic use and increased ED use by African Americans, could be associated with this observed increased risk of death. African-American children could be sicker when they come to medical attention, and additional unmeasured sociocultural factors also could affect when and where individual children seek medical care. Access to healthcare can vary according to location (ie, the availability of physicians in rural vs urban areas); we were unable to control for location and income in this study, however. These determinants also could contribute to the differences observed. Further studies are
1500 1250 1000 p = 0.470* 750
OUTPT
500
250
ED
p = 0.734*
0 1995-1996
1997-1998
1999-2000
2001-2002
Year
2003-2004
* Test for linear trend
Figure 1. Outpatient and ED visit rates for diarrhea-associated illness for US children age < 5 years, 1995-2004. The solid gray line represents outpatient visits; the gray dashed line represents ED visits. Error bars represent 95% CIs.
Discussion This study derived national rates of diarrhea-associated healthcare encounters among children age < 5 years for 1995-2004. Although most diarrhea-associated morbidity is managed in the ambulatory setting, previous studies have focused on diarrhea-associated hospitalizations. Before the present study, information on national rates of healthcare utilization for diarrhea-associated illness in outpatient clinics and EDs was limited. Although 3 previous studies have reported outpatient visit rates, 2 of these studies are from the early to mid-1990s (1992-1994 and 1993-1996) and thus are dated.16,17 Furthermore, both of these studies reported rates from privately insured populations; thus, nationally representative rates from more recent time periods were unknown. Our group recently reported ambulatory and inpatient diarrhea-associated healthcare rates, but these rates were for children enrolled in TennCare, Tennessee’s expanded Medicaid program, and thus may not be nationally representative.5 The present study estimated that rotavirus contributed to approximately 25% of all outpatient and ED diarrhea-associated visits in children age < 3 and < 5 years. In both settings, rotavirus resulted in a substantial number
Table II. Source of payment by race and site for diarrhea-associated illness in children age < 5 years, 1995-2004 All visits
Source of payment % (n) Medicaid/SCHIP Private insurance Other* Total
Outpatient visits
ED visits
Caucasian
African American
Caucasian
African American
Caucasian
African American
29.4% (4 546 128) 55.0% (8 510 201) 15.7% (2 425 722) 100% (15 482 051)
41.6% (1 214 724) 38.4% (1 118 657) 20.0% (583 247) 100% (2 916 628)
26.0% (3 151 039) 60.0% (7 256 036) 14.0% (1 693 565) 100% (12 100 640)
30.8% (540 798) 47.4% (832 216) 21.8% (381 986) 100% (1 755 000)
41.3% (1 395 089) 37.1% (1 254 165) 21.7% (732 157) 100% (3 381 411)
58.0% (673 926) 24.7% (286 441) 17.3% (201 261) 100% (1 161 628)
*Includes Medicare, worker’s compensation, self-pay, no charge/charity, and unknown (missing).
National Rates of Diarrhea-Associated Ambulatory Visits in Children
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Crude Indidence Rate (N per 10,000 children per year)
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3000 2750 2500 2250 2000 1750 1500 1250 1000 750 500
OUTPT
250 0
ED
Jul
Aug
Sep
Oct
Nov
Dec
Jan
Feb
Mar
Apr
May
Jun
Month
Figure 2. Outpatient and ED visit rates by month for diarrheaassociated illness for US children age < 5 years, 1995-2004. The solid gray line represents outpatient visits; the gray dashed line represents ED visits. Error bars represent 95% CIs.
needed to elucidate the specific factors responsible for these different patterns of healthcare utilization and to explore whether improved access to outpatient clinics might decrease this disparity. Our estimated rate of diarrhea-associated outpatient visits of 955/10 000 person-years in children age < 5 years is comparable with the rate of 943 visits/10 000 person-years in children age < 5 years reported by Zimmerman et al17 and the rate of 1190 visits/10 000 person-years in children age 1 to 59 months extrapolated from the study of Parashar et al.16 Recent data on ED utilization due to diarrhea-associated illness are limited, however. The most recent report comes from Parashar et al’s 1998 review of data for 1992-1994.16 Our rates of 428 ED visits/10 000 person-years for children age < 3 years and 314 ED visits/10 000 person-years for those age < 5 years is higher than Parashar et al’s rates of 157 ED visits/10 000 person-years for children age 4 to 23 months and of 98 ED visits/10 000 person-years for those age < 59 months. In our TennCare study, we reported rates of 792 ED visits/10 000 person-years for children age < 3 years and 595 ED visits/10 000 person-years for those age < 5 years.5 The nationally representative rates of ED utilization that we report, 428 visits/ 10 000 person-years for children age < 3 years and 314 visits/10 000 person-years for those age < 5 years, falls between Parashar et al’s private payer population rate and the Tennessee Medicaid rate. Our study has several limitations. First, although the NAMCS and NHAMCS are designed and weighted to represent the US population, the overall number of recorded visits for children is limited. We combined annual data to provide reliable estimates meeting NCHS requirements; however, these requirements precluded some analyses, such as a more robust multivariate regression model allowing assessment of the effect of race on healthcare utilization. We also were unable to control for socioeconomic and health insur60
Vol. 155, No. 1 ance status. In addition, the surveys were based on visits rather than on individual children.9,10 Thus, it is possible that increased visit rates in one group over another could be due to more visits per child, rather than to more total children from one group seeking healthcare. Nonetheless, the inclusion of all visits provides a reliable assessment of overall diarrhea-associated ambulatory healthcare utilization, even if some visits were due to a particular child visiting a healthcare site or provider more than once. Finally, the identification of diarrhea-associated visits within the NAMCS and NHAMCS was based on ICD-9-CM codes, the accuracy of which could not be determined in this study. Jin et al’s15 winter residual method for rotavirus proportion estimation was established with hospitalized patients and later validated by a prospective study involving stool testing in hospitalized children. Less severe diarrhea not requiring admission may have a different spectrum of etiology and may involve a different proportion of visits due to rotavirus. Although the precise etiology of diarrhea was unknown in our study, the winter peaks that occurred in the outpatient and ED setting are consistent with previous epidemiologic studies of rotavirus and suggest that the winter residual method is valid, and that rotavirus is a significant cause of diarrhea-associated visits in both settings. n Submitted for publication Oct 10, 2008; last revision received Jan 7, 2009; accepted Jan 30, 2009.
References 1. Chabra A, Chavez GF, Taylor D. Hospital use by pediatric patients: implications for change. Am J Prev Med 1997;13(6 Suppl):30-7. 2. McConnochie KM, Conners GP, Lu E, Wilson C. How commonly are children hospitalized for dehydration eligible for care in alternative settings? Arch Pediatr Adolesc Med 1999;153:1233-41. 3. Widdowson MA, Meltzer MI, Zhang X, Bresee JS, Parashar UD, Glass RI. Cost-effectiveness and potential impact of rotavirus vaccination in the United States. Pediatrics 2007;119:684-97. 4. American Academy of Pediatrics Committee on Infectious Diseases. Recommended immunization schedules for children and adolescents– United States, 2007. Pediatrics 2007;119:207–8. 5. Pont SJ, Carpenter LR, Griffin MR, Jones TF, Schaffner W, Dudley JA, et al. Trends in healthcare usage attributable to diarrhea, 1995-2004. J Pediatr 2008;153:777-82. 6. Glass RI, Lew JF, Gangarosa RE, LeBaron CW, Ho MS. Estimates of morbidity and mortality rates for diarrheal diseases in American children. J Pediatr 1991;118(4 Pt 2):S27-33. 7. Fischer TK, Viboud C, Parashar U, Malek M, Steiner C, Glass R, et al. Hospitalizations and deaths from diarrhea and rotavirus among children < 5 years of age in the United States, 1993-2003. J Infect Dis 2007;195: 1117-25. 8. Centers for Disease Control and Prevention, National Center for Health Statistics. Ambulatory health care data. Available from: www.cdc.gov/ nchs/about/major/ahcd/ahcd1.htm. Accessed October 10, 2006. 9. Centers for Disease Control and Prevention, National Center for Health Statistics. Ambulatory health care data. Available from: www. cdc.gov/nchs/about/major/ahcd/namcsdes.htm. Accessed October 10, 2006. 10. Centers for Disease Control and Prevention. National Center for Health Statistics. Ambulatory health care data. Available from: www.cdc.gov/ nchs/about/major/ahcd/nhamcsds.htm. Accessed October 10, 2006.
Pont et al
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July 2009 11. International Classification of Diseases, Ninth Revision, Clinical Modification. Washington, DC: Public Health Service, US Dept of Health and Human Services; 1998. 12. United States Census Bureau. Population estimates datasets. Available from: www.census.gov/popest/datasets.html. Accessed October 10, 2006. 13. Casella G, Berger RL. Statistical Inference. 2nd ed. Duxbury, CA: Duxbury Press; 2002. 14. Cochran W. Sampling Techniques. 3rd ed. New York: Wiley; 1977. 15. Jin S, Kilgore PE, Holman RC, Clarke MJ, Gangarosa EJ, Glass RI. Trends in hospitalizations for diarrhea in United States children from 1979
through 1992: estimates of the morbidity associated with rotavirus. Pediatr Infect Dis J 1996;15:397-404. 16. Parashar UD, Holman RC, Bresee JS, Clarke MJ, Rhodes PH, Davis RL, et al. Epidemiology of diarrheal disease among children enrolled in four West Coast health maintenance organizations. Vaccine Safety Datalink Team. Pediatr Infect Dis J 1998;17:605-11. 17. Zimmerman CM, Bresee JS, Parashar UD, Riggs TL, Holman RC, Glass RI. Cost of diarrhea-associated hospitalizations and outpatient visits in an insured population of young children in the United States. Pediatr Infect Dis J 2001;20:14-9.
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A
mong US children age < 5 years, diarrhea-associated illness leads to approximately 220 000 hospitalizations (9% of all hospitalizations in this age group) and an estimated 300 deaths annually.1,2 In addition, gastroenteritis and dehydration trail only asthma as the leading reason for hospital admission in US children age 1 to 5 years.1,2 Diarrhea-associated illness entails substantial costs to society. Rotavirus is the leading cause of diarrhea in US children; rotavirus diarrhea alone is associated with an estimated annual healthcare cost of $319 million and a total annual cost to society of $893 million.3 Even though diarrhea-associated healthcare utilization occurs predominantly in outpatient clinics and emergency departments (EDs),3 previous studies have focused on hospitalization, and current estimates of national rates of ambulatory visits are limited. Contemporary rates are needed, because a rotavirus vaccine has recently been recommended for all US infants.4 The determination of incidence rates and trends present before the introduction of rotavirus vaccine will allow for an appropriate evaluation of the vaccine’s impact on diarrhea-associated illness. Furthermore, although differences in morbidity, mortality, and healthcare utilization patterns due to diarrhea between Caucasian and African-American children have been reported, whether these differences also exist for ambulatory visits in a nationally representative population remains unknown.5-7 We undertook the present study with the goals of estimating US rates of ambulatory healthcare encounters due to diarrhea- and rotavirus-associated illness before the introduction of rotavirus vaccine; assessing changes in these rates over time; and determining prevaccine healthcare utilization differences by race and age.
Methods Data were obtained from the National Ambulatory Medical Care Survey (NAMCS) and the National Hospital Ambulatory Medical Care Survey (NHAMCS) for 1995-2004. These surveys are conducted by the National Center for Health Statistics (NCHS) to provide estimates of ambulatory healthcare services rendered to the US population by both non–federally employed office-based physicians enFrom the Department of Pediatrics, University of Texas gaged primarily in patient care (NAMCS) and in the hospital EDs and outpatient CI ED ICD-9-CM IRR NAMCS NCHS NHAMCS
Confidence interval Emergency department International Classification of Diseases, Ninth Revision, Clinical Modification Incidence rate ratio National Ambulatory Medical Care Survey National Center for Health Statistics National Hospital Ambulatory Medical Care Survey
Medical Branch-Austin Programs (S.P.) and Department of Kinesiology and Health Education, College of Education (S.P.), University of Texas, Austin, TX and the Departments of Preventive Medicine (C.G., M.G.), Biostatistics (T.S.), and Pediatrics (W.C.), Vanderbilt University, Nashville, TN
Supported by an Academic Pediatric Association Young Investigator Award and a National Institutes of Health National Research Service Award Grant (T32 HS01383303) The authors declare no conflicts of interest related to this work. 0022-3476/$ - see front matter. Copyright Ó 2009 Mosby Inc. All rights reserved. 10.1016/j.jpeds.2009.01.075
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Vol. 155, No. 1 July 2009 departments of noninstitutional general and short-stay hospitals, exclusive of federal, military, and Veterans Administration hospitals (NHAMCS).8-10 The NAMCS and NHAMCS collect information about healthcare providers, services rendered, and patient characteristics. Survey information is collected through a multistage sampling procedure that includes healthcare facilities or providers and patient records and is designed to produce unbiased estimates for the US population.9,10 Data collected directly from the healthcare sites and/or their records identify healthcare encounters, with the physician–patient encounter or visit as the basic sampling unit.9,10 Visits conducted solely for administrative purposes and visits in which no medical care was provided are excluded. For the NAMCS, a systematic random sample of office visits from a randomly assigned 1-week reporting period is obtained from selected physicians.9 The samples are then weighted to be nationally representative. The sampling and data collection methodologies of the NHAMCS are similar to those of the NAMCS; within emergency service areas or outpatient department clinics, patient visits are selected systematically over a randomly assigned 4-week reporting period for the NHAMCS.10 The unweighted item nonresponse rate for both surveys is generally # 5%.8 For each encounter, up to 3 diagnoses were recorded using the International Classification of Diseases, Ninth Revision, Clinical Modification (ICD-9-CM).11 Using NAMCS and NHAMCS data, all ICD-9-CM–coded diarrhea-associated visits were identified that met the following requirements: either the visit had a diagnosis of diarrhea (see Appendix 1) as the primary diagnosis or the visit had a primary diagnosis of dehydration (ICD-9-CM 276.5) or nausea and vomiting (ICD-9-CM 787.0), with a diarrhea visit diagnosis code listed as the second or third diagnosis.5 Visits occurring between 1995 and 2004 for children age < 5 years were included. Each visit was characterized according to the child’s age (0 to 11 months, 1 to 2 years, or 3 to 4 years), ethnicity (Latino, non-Latino, or missing), race (Caucasian, African American, or other), sex, expected source of payment (private insurance, Medicaid/SCHIP, or other, including Medicare, worker’s compensation, self-pay, no charge/charity, and unknown), and month and calendar year of the visit. Statistical Analysis The outcome of interest was the annual rate of diarrhea-associated healthcare encounters in the outpatient and ED settings. Numerators for rates were calculated for each stratum on the basis of our definition of a diarrhea visit, and the denominator was the US Census Bureau population estimate for July 1 of each study year.12 The NCHS recommends a minimum unweighted cell size of 30 when using NAMCS and NHAMCS data, to provide robust national estimates.9,10 To meet this requirement, study years were collapsed into 2-year groupings: 1995-1996, 1997-1998, 1999-2000, 20012002, and 2003-2004. Standard errors of the number of diarrhea-associated visits for compared stratum were estimated, taking into account
the multistage sampling designs of the NAMCS and NHAMCS, The relative standard errors were < 30% for all estimates, in accordance with NCHS recommendations.13,14 Estimated rates were compared using rate ratios and standard errors, and along with the delta method were used to compute 95% confidence intervals for all rate ratios.13 In addition, a test for linear trend was performed to assess for rate changes with time over the five 2-year study periods. The rotavirus disease burden was estimated using the winter residual excess morbidity method described by Jin et al.15 This method subtracts the diarrhea-associated visit rates from the months with less rotavirus activity (June through November) from those from the months with greater rotavirus activity (December through May). The estimated rotavirus burden is the difference between the ‘‘summer’’ and ‘‘winter’’ diarrhea-associated visit rates. Because children age < 5 years are most susceptible to severe diarrhea-associated illness, the rotavirus disease burden was estimated in children age < 3 years and in those age < 5 years. Rate differences by race controlling for age were calculated across the entire study period, to provide robust estimates. In a separate model, diarrhea rates in Caucasians and African Americans were compared, controlling for study period. All analyses were performed using Stata 9.2 (StataCorp, College Station, Texas). All survey data released by the NCHS were deidentified, and the study protocol was reviewed and approved by Vanderbilt University’s Institutional Review Board.
Results Annual Rates and Trends Between 1995 and 2004, US children age < 5 years experienced approximately 18 495 002 outpatient visits and 6 078 147 ED visits due to diarrhea-associated illness. Children age < 3 years accounted for 82% of these visits. Caucasian and African-American children represented approximately 80% and 15% of the visits, respectively. In 53% of the visits, private insurance was the primary payment source. The demographics for the eligible population were similar for each study year, except that the number of children in the ‘‘other’’ race category, the number of children age 0 to 11 months, and the number of children of Hispanic ethnicity increased over the study period. Table I presents demographic data for the children experiencing a diarrhea-associated ambulatory healthcare visit during the study period. Infants age 0 to 11 months experienced the highest rates of healthcare encounters for diarrhea-associated illness, with 1613 (95% CI = 1293 to 1932) outpatient visits/10 000 person-years and 605 (95% CI = 518 to 693) ED visits/10 000 person-years. Children age 1 to 2 years accounted for 1165 (95% CI = 927 to 1403) outpatient visits and 339 (95% CI = 293 to 385) ED visits per 10 000 person-years, whereas children age 3 to 4 years accounted for 417 (95% CI = 307 to 526) outpatient visits and 143 (95% CI = 116–170) ED visits per 10 000 person-years. Figure 1 displays annualized visit rates for diarrhea-associated illness for 1995-2004 by 2-year period. Outpatient visits 57
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Table I. Outpatient and ED visits for diarrhea-associated illness among US children age < 5 years, 1995-2004 Total Age 0-11 months 1-2 years 3-4 years Race Caucasian African American Other Sex Female Male Ethnicity Non-Hispanic/Latino Hispanic/Latino Missing Source of payment* Total* Private insurance Medicaid/SCHIP Other†
Outpatient
ED
Total
18 495 002 (100.0%)
6 078 147 (100.0%)
24 573 149 (100.0%)
6 277 916 (33.9%) 8 980 311 (48.6%) 3 236 775 (17.5%)
2 355 782 (38.8%) 2 614 257 (43.0%) 1 108 108 (18.2%)
8 633 698 (35.1%) 11 594 568 (47.2%) 4 344 883 (17.7%)
15 262 454 (82.5%) 2 099 989 (11.4%) 1 132 559 (6.1%)
4 313 481 (71.0%) 1 525 246 (25.1%) 239 420 (3.9%)
19 575 935 (79.7%) 3 625 235 (14.8%) 1 371 979 (5.6%)
9 343 282 (50.5%) 9 151 720 (49.5%)
2 787 299 (45.9%) 3 290 848 (54.1%)
12 130 581 (49.4%) 12 442 568 (50.6%)
11 913 161 (64.4%) 4 863 719 (26.3%) 1 718 122 (9.3%)
3 952 476 (65.0%) 1 565 574 (25.8%) 560 097 (9.2%)
15 865 637 (64.6%) 6 429 293 (26.2%) 2 278 219 (9.3%)
14 877 282 (100%) 8 717 810 (58.6%) 3 925 244 (26.4%) 2 234 228 (15.0%)
4 738 469 (100%) 1 603 848 (33.8%) 2 152 553 (45.4%) 982 068 (20.7%)
19 615 751 (100%) 10 321 658 (52.6%) 6 077 797 (31.0%) 3 216 296 (16.4%)
Source: NAMCS and NHAMCS. *Summed across 1997-2004. †Includes Medicare, worker’s compensation, self-pay, no charge/charity, and unknown (missing).
resulting from diarrhea-associated illnesses among all children remained stable (P = .470), with rates of 932 (95% CI = 631 to 1233) visits/10 000 person-years for 1995-1996 and 1011 (95% CI = 540 to 1483) visits/10 000 person-years for 2003-2004. ED visits also remained stable (P = .734), with rates of 345 (95% CI = 263 to 427) visits/10 000 person-years for 1995-1996 and 327 (95% CI = 253 to 401) visits/10 000 person-years for 2003-2004. For the period 1995-2004, children age < 5 years experienced 955 (95% CI = 803 to 1107) outpatient visits and 314 (95% CI = 278 to 350) ED visits/ 10 000 person-years, and those age < 3 years had 1315 (95% CI = 1099 to 1532) outpatient visits and 428 (95% CI = 377 to 480) ED visits/10 000 person-years. Utilization Differences by Race The rate of total ambulatory visits (outpatient and ED visits combined) was comparable in Caucasians and African Americans (1298/10 000 person-years [95% CI = 1107 to 1490] vs 1236/10 000 person-years [95% CI = 985 to 1486]). After adjusting for age and study year, African-American children had a lower visit rate for diarrhea-associated illness than Caucasian children in the outpatient clinic setting (716/10 000 person-years [95% CI = 496 to 936) vs 1012/10 000 person-years [95% CI = 830 to 1194]; IRR = 0.71; 95% CI = 0.51 to 0.99), but a higher visit rate for diarrhea-associated illness in the ED setting (520/10 000 person-years [95% CI = 425 to 615] vs 286/10 000 person-years [95% CI = 250 to 322]; IRR = 1.83; 95% CI = 1.58 to 2.11). Because US Census data (used as the denominator in rate calculations) contain no information regarding health insurance status, we were unable to control for source of payment in our regression analyses. Instead, to explore the influence of insurance status on site of utilization, we evaluated the proportion of diar58
rhea-associated visits that occurred in each setting by race and source of payment (Table II), then evaluated the visit setting for African-American and Caucasian children with private insurance and Medicaid/SCHIP by calculating row percentages from the data presented in Table II. Of all 1 118 657 diarrhea-associated visits by African-American children with private insurance, 26% (95% CI = 18% to 34%), or 286 441 visits, were to EDs. During the study period, a total of 8 510 201 diarrhea-associated visits were made by Caucasian children with private insurance; 15% of these visits (95% CI = 12% to 18%) , or 1 254 165 visits, were to EDs. Of all diarrhea-associated visits by African-American children with Medicaid/SCHIP (1 214 724), 55% (95% CI = 43% to 68%), or 673 926 visits, were to EDs, compared with 31% (95% CI = 25% to 36%), or 1 395 089 visits, for Caucasian children with Medicaid/SCHIP. Visits Due to Rotavirus Figure 2 shows the seasonal variation for diarrhea-associated healthcare utilization, with increased visit rates during the winter, apparently driven by the rotavirus disease burden. Using the winter excess residual method, we estimated the proportion of diarrhea-associated visits due to rotavirus for children age < 3 years and < 5 years. We estimate that rotavirus contributed to 29% (273/10 000 person-years [95% CI = 145 to 401]) of the outpatient diarrhea-associated visits, or 5 285 636 visits, and to 25% (78/10 000 person-years [95% CI = 64 to 83]) of the ED diarrhea-associated visits, or 1 519 661 visits, in children age < 5 years. In children age < 3, for 19952004, we estimate that rotavirus contributed to 29% of the outpatient diarrhea-associated visits, or 4 365 821 visits, and to 28% of the diarrhea-associated ED visits, or 1 386 245 visits. Pont et al
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Visit Rate (N per 10,000 children per year)
July 2009
and a high proportion of diarrhea-associated healthcare visits and contributed to approximately 750 000 ambulatory visits annually in children age <5 years. The recently released rotavirus vaccine may produce a substantial reduction in these healthcare visits, and future studies should be performed to quantify this vaccine’s impact. Our analysis of 10 years of nationally representative data indicates that Caucasians had a significantly greater (40%) rate of healthcare utilization for diarrhea-associated illness in outpatient clinics than African Americans, but that African Americans utilized the ED for diarrhea-associated illness at nearly double the rate of Caucasians. The total rate of ambulatory healthcare utilization due to diarrhea-associated illness was comparable in African-American and Caucasian children. We also found differences in site of healthcare visit for diarrhea-associated illness by source of payment. Although the available data limited our ability to generate and analyze rates by insurance status, our findings suggest an association between insurance status and site of care, with a larger proportion of visits to the ED by children with Medicaid/SCHIP compared with those with private insurance. Our data suggest that both race and insurance status may influence the site of care for diarrhea-associated illness in children. Differing rates of healthcare coverage, access to outpatient clinics, cultural attitudes, disease susceptibility and acuity, and perceived or experienced racial disparities might contribute to these differences in healthcare utilization. Fischer et al7 recently reported that in the United States, African-American children age < 5 years have a significantly greater risk of dying from rotavirus compared with Caucasian children in this age group, with a risk ratio of 2.0. Glass et al6 reported an increased risk of death from diarrheal illness in African-American children from the southern US. Further study is warranted. Differential healthcare utilization by race, with proportionally decreased outpatient clinic use and increased ED use by African Americans, could be associated with this observed increased risk of death. African-American children could be sicker when they come to medical attention, and additional unmeasured sociocultural factors also could affect when and where individual children seek medical care. Access to healthcare can vary according to location (ie, the availability of physicians in rural vs urban areas); we were unable to control for location and income in this study, however. These determinants also could contribute to the differences observed. Further studies are
1500 1250 1000 p = 0.470* 750
OUTPT
500
250
ED
p = 0.734*
0 1995-1996
1997-1998
1999-2000
2001-2002
Year
2003-2004
* Test for linear trend
Figure 1. Outpatient and ED visit rates for diarrhea-associated illness for US children age < 5 years, 1995-2004. The solid gray line represents outpatient visits; the gray dashed line represents ED visits. Error bars represent 95% CIs.
Discussion This study derived national rates of diarrhea-associated healthcare encounters among children age < 5 years for 1995-2004. Although most diarrhea-associated morbidity is managed in the ambulatory setting, previous studies have focused on diarrhea-associated hospitalizations. Before the present study, information on national rates of healthcare utilization for diarrhea-associated illness in outpatient clinics and EDs was limited. Although 3 previous studies have reported outpatient visit rates, 2 of these studies are from the early to mid-1990s (1992-1994 and 1993-1996) and thus are dated.16,17 Furthermore, both of these studies reported rates from privately insured populations; thus, nationally representative rates from more recent time periods were unknown. Our group recently reported ambulatory and inpatient diarrhea-associated healthcare rates, but these rates were for children enrolled in TennCare, Tennessee’s expanded Medicaid program, and thus may not be nationally representative.5 The present study estimated that rotavirus contributed to approximately 25% of all outpatient and ED diarrhea-associated visits in children age < 3 and < 5 years. In both settings, rotavirus resulted in a substantial number
Table II. Source of payment by race and site for diarrhea-associated illness in children age < 5 years, 1995-2004 All visits
Source of payment % (n) Medicaid/SCHIP Private insurance Other* Total
Outpatient visits
ED visits
Caucasian
African American
Caucasian
African American
Caucasian
African American
29.4% (4 546 128) 55.0% (8 510 201) 15.7% (2 425 722) 100% (15 482 051)
41.6% (1 214 724) 38.4% (1 118 657) 20.0% (583 247) 100% (2 916 628)
26.0% (3 151 039) 60.0% (7 256 036) 14.0% (1 693 565) 100% (12 100 640)
30.8% (540 798) 47.4% (832 216) 21.8% (381 986) 100% (1 755 000)
41.3% (1 395 089) 37.1% (1 254 165) 21.7% (732 157) 100% (3 381 411)
58.0% (673 926) 24.7% (286 441) 17.3% (201 261) 100% (1 161 628)
*Includes Medicare, worker’s compensation, self-pay, no charge/charity, and unknown (missing).
National Rates of Diarrhea-Associated Ambulatory Visits in Children
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Crude Indidence Rate (N per 10,000 children per year)
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3000 2750 2500 2250 2000 1750 1500 1250 1000 750 500
OUTPT
250 0
ED
Jul
Aug
Sep
Oct
Nov
Dec
Jan
Feb
Mar
Apr
May
Jun
Month
Figure 2. Outpatient and ED visit rates by month for diarrheaassociated illness for US children age < 5 years, 1995-2004. The solid gray line represents outpatient visits; the gray dashed line represents ED visits. Error bars represent 95% CIs.
needed to elucidate the specific factors responsible for these different patterns of healthcare utilization and to explore whether improved access to outpatient clinics might decrease this disparity. Our estimated rate of diarrhea-associated outpatient visits of 955/10 000 person-years in children age < 5 years is comparable with the rate of 943 visits/10 000 person-years in children age < 5 years reported by Zimmerman et al17 and the rate of 1190 visits/10 000 person-years in children age 1 to 59 months extrapolated from the study of Parashar et al.16 Recent data on ED utilization due to diarrhea-associated illness are limited, however. The most recent report comes from Parashar et al’s 1998 review of data for 1992-1994.16 Our rates of 428 ED visits/10 000 person-years for children age < 3 years and 314 ED visits/10 000 person-years for those age < 5 years is higher than Parashar et al’s rates of 157 ED visits/10 000 person-years for children age 4 to 23 months and of 98 ED visits/10 000 person-years for those age < 59 months. In our TennCare study, we reported rates of 792 ED visits/10 000 person-years for children age < 3 years and 595 ED visits/10 000 person-years for those age < 5 years.5 The nationally representative rates of ED utilization that we report, 428 visits/ 10 000 person-years for children age < 3 years and 314 visits/10 000 person-years for those age < 5 years, falls between Parashar et al’s private payer population rate and the Tennessee Medicaid rate. Our study has several limitations. First, although the NAMCS and NHAMCS are designed and weighted to represent the US population, the overall number of recorded visits for children is limited. We combined annual data to provide reliable estimates meeting NCHS requirements; however, these requirements precluded some analyses, such as a more robust multivariate regression model allowing assessment of the effect of race on healthcare utilization. We also were unable to control for socioeconomic and health insur60
Vol. 155, No. 1 ance status. In addition, the surveys were based on visits rather than on individual children.9,10 Thus, it is possible that increased visit rates in one group over another could be due to more visits per child, rather than to more total children from one group seeking healthcare. Nonetheless, the inclusion of all visits provides a reliable assessment of overall diarrhea-associated ambulatory healthcare utilization, even if some visits were due to a particular child visiting a healthcare site or provider more than once. Finally, the identification of diarrhea-associated visits within the NAMCS and NHAMCS was based on ICD-9-CM codes, the accuracy of which could not be determined in this study. Jin et al’s15 winter residual method for rotavirus proportion estimation was established with hospitalized patients and later validated by a prospective study involving stool testing in hospitalized children. Less severe diarrhea not requiring admission may have a different spectrum of etiology and may involve a different proportion of visits due to rotavirus. Although the precise etiology of diarrhea was unknown in our study, the winter peaks that occurred in the outpatient and ED setting are consistent with previous epidemiologic studies of rotavirus and suggest that the winter residual method is valid, and that rotavirus is a significant cause of diarrhea-associated visits in both settings. n Submitted for publication Oct 10, 2008; last revision received Jan 7, 2009; accepted Jan 30, 2009.
References 1. Chabra A, Chavez GF, Taylor D. Hospital use by pediatric patients: implications for change. Am J Prev Med 1997;13(6 Suppl):30-7. 2. McConnochie KM, Conners GP, Lu E, Wilson C. How commonly are children hospitalized for dehydration eligible for care in alternative settings? Arch Pediatr Adolesc Med 1999;153:1233-41. 3. Widdowson MA, Meltzer MI, Zhang X, Bresee JS, Parashar UD, Glass RI. Cost-effectiveness and potential impact of rotavirus vaccination in the United States. Pediatrics 2007;119:684-97. 4. American Academy of Pediatrics Committee on Infectious Diseases. Recommended immunization schedules for children and adolescents– United States, 2007. Pediatrics 2007;119:207–8. 5. Pont SJ, Carpenter LR, Griffin MR, Jones TF, Schaffner W, Dudley JA, et al. Trends in healthcare usage attributable to diarrhea, 1995-2004. J Pediatr 2008;153:777-82. 6. Glass RI, Lew JF, Gangarosa RE, LeBaron CW, Ho MS. Estimates of morbidity and mortality rates for diarrheal diseases in American children. J Pediatr 1991;118(4 Pt 2):S27-33. 7. Fischer TK, Viboud C, Parashar U, Malek M, Steiner C, Glass R, et al. Hospitalizations and deaths from diarrhea and rotavirus among children < 5 years of age in the United States, 1993-2003. J Infect Dis 2007;195: 1117-25. 8. Centers for Disease Control and Prevention, National Center for Health Statistics. Ambulatory health care data. Available from: www.cdc.gov/ nchs/about/major/ahcd/ahcd1.htm. Accessed October 10, 2006. 9. Centers for Disease Control and Prevention, National Center for Health Statistics. Ambulatory health care data. Available from: www. cdc.gov/nchs/about/major/ahcd/namcsdes.htm. Accessed October 10, 2006. 10. Centers for Disease Control and Prevention. National Center for Health Statistics. Ambulatory health care data. Available from: www.cdc.gov/ nchs/about/major/ahcd/nhamcsds.htm. Accessed October 10, 2006.
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July 2009 11. International Classification of Diseases, Ninth Revision, Clinical Modification. Washington, DC: Public Health Service, US Dept of Health and Human Services; 1998. 12. United States Census Bureau. Population estimates datasets. Available from: www.census.gov/popest/datasets.html. Accessed October 10, 2006. 13. Casella G, Berger RL. Statistical Inference. 2nd ed. Duxbury, CA: Duxbury Press; 2002. 14. Cochran W. Sampling Techniques. 3rd ed. New York: Wiley; 1977. 15. Jin S, Kilgore PE, Holman RC, Clarke MJ, Gangarosa EJ, Glass RI. Trends in hospitalizations for diarrhea in United States children from 1979
through 1992: estimates of the morbidity associated with rotavirus. Pediatr Infect Dis J 1996;15:397-404. 16. Parashar UD, Holman RC, Bresee JS, Clarke MJ, Rhodes PH, Davis RL, et al. Epidemiology of diarrheal disease among children enrolled in four West Coast health maintenance organizations. Vaccine Safety Datalink Team. Pediatr Infect Dis J 1998;17:605-11. 17. Zimmerman CM, Bresee JS, Parashar UD, Riggs TL, Holman RC, Glass RI. Cost of diarrhea-associated hospitalizations and outpatient visits in an insured population of young children in the United States. Pediatr Infect Dis J 2001;20:14-9.
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