Periodicity of Asthma, Emphysema, and Chronic Bronchitis in a Northwest Health Maintenance Organization*

Periodicity of Asthma, Emphysema, and Chronic Bronchitis in a Northwest Health Maintenance Organization* Molly L. Osborne, MD, PhD, FCCP; William M. Vollmer, PhD; and A Sonia Buist, MD, FCCP Study objective: Since seasonal patterns in morbidity may identify triggers provoking hospital-based care for airflow obstruction, this study examined seasonal variation in patterns of hospitalizations for asthma, chronic bronchitis, and emphysema. Design and setting: The data for this analysis were derived from the abstracted medical records of a large health maintenance organization, Kaiser Pennanente, Northwest region, over the period 1979 to 1987. Patients: In all, 2,6 primary hospital discharges for asthma and 1,121 primary hospital discharges for the combination chronic bronchitis/emphysema were observed. Results: The monthly patterns varied for asthma and chronic bronchitis/emphysema, and also varied by age and sex. For young children to 14 years, asthma hospitalizations peaked primarily in the fall. In contrast, for young children to 14 years, hospitalizations for chronic bronchitis/ emphysema peaked in the fall/winter months. Seasonal variation decreased as age increased for chronic bronchitis/emphysema, such that for the 6+ year group, there was no seasonal variation. Conclusion: A better understanding of the causes of the age-specific seasonal patterns in these obstructive respiratory diseases may help to reduce the morbidity that is associated with them. (CHEST 1996; 11:148-62) Key words: asthma; chronic bronchitis; emphysema; epidemiology; health maintenance organization; hospitalization; seasonal patterns R espiratory diseases such as asthma, chronic bronchitis, and emphysema are among the leading causes of morbidity and mortality in many countries and appear to be on the rise. 1 - This upward trend is in contrast to sharply downward trends for heart disease, stroke, and other chronic diseases. Trends in asthma morbidity and mortality have been studied, and emergency department visits, hospitalization, and deaths have been shown to be increasing in all age groups over the past two decades in many countries. 6 These increases may be due to changes in asthma prevalence, incidence, and/or modification of the management of asthma or exposure to triggers. 7 8 Seasonal patterns in asthma morbidity have long been recognized and may shed insight into the triggers provoking hospital-based care for asthma. 9 1 For example, such patterns have been linked to seasonal exposure to specific antigens, 11 12 periodicity of infections, 13 and periodicity in high levels of air pollutants.14,l *From the Departments of Medicine and Physiology, Oregon Health Sciences University, Portland, and Kaiser Permanente Center for Health Research, Portland, Ore. Supported by NIH FIRST Award R29-HL 4139 (Dr. Vollmer). Manuscript received October, 199; revision accepted July 1, 1996. 148 Less is known about seasonal patterns in morbidity for chronic bronchitis and emphysema. These diseases are excluded from analyses of morbidity due to asthma. Indeed, many of the studies of asthma morbidity have been limited to children and young adults to minimize diagnostic overlap of asthma with chronic bronchitis and emphysema. The aims of this study were (I) to examine seasonal variation in patterns of hospitalizations for asthma, chronic bronchitis, and emphysema among members of a large health maintenance organization, and (2) to contrast these patterns for different age-sex subgroups. Population MATERIALS AND METHODS The data for this analysis derive from the abstracted medical records of Kaiser Permanente (KP), Northwest r egion, a arge l health maintenance organization centered in Portland, Ore. The KP membership, which grew from 221,743 to 31,819 during the years covered by this study (1979 to 1987), is generally representative of the area population as a whole. 16.l 7 No evidence exists of systematic selection of healthy individuals either into or out of the system. Data Systems Data for the study have been d erived from the abstracted inpatient medical records of the entire KP membership. Details of this Clinical Investigations

4 4 3 3 2 1 1 - -1 ) -1-2 - -3» -3 :s c ::E 2 E 1 1 <l:: ) () c - -1-1 i:s -2!>" - 2 1 1 - - 1-1 -2 - i -14 y.o. n= 721 -= W1l W1l W J. l J 1-64 y.o. J n=832 W1l W1l_ W1l_ """' - 6+ y.o. = n-7-2 =! '. - =- W J. l = l _ l ' Z i a =... F M A M A N D Month FIGURE l. Seasonal patterns of hospital discharges for asthma by age (3 months moving average). J 4 4 3 3 2 1 1 - ) -1 & -1 ) -2 < -» -3 :s -3 c -4 ::E -4 E 3 <l:: 3 ) g 2 1 1 i:s!>" - -1-1 :ll -1 JWii.!rat - I1Z1il W1l ' llizi " " " ' 1-64 y.o. t n=298 r e i r! e! i!! rei!! W J. l! ' w W1l. l - r e i!! lim! fll!':ll I l"$i! I F M A M A N D Month n=78 F!GURE 2. Seasonal pattern of hospital discharges for chronic bronchitis/emphysema by age (3 months moving average). database are given elsewhere. 18 19 Briefly, the inpatient database includes information about each discharge from the two Portland area KP hospitals and from the contracted hospitals in Salem and Longview since 1966. Data include, but are not limited to, primary hospital discharge diagnosis and up to eight secondary discharge diagnoses, each coded according to the International Classification of Diseases (ICD) coding system in effect at the time of the discharge. This report uses information only from 1979 to 1987 (ICD-9). Because the diagnoses of chronic bronchitis and emphysema often overlap with asthma, we examined utilization data for asthma and for the combination of chronic bronchitis and emphysema. To determine the extent to which some of the seasonal vmiation in hospitalizations might be attributable to infections, we also examined secondary hospital discharge diagnoses of pneumonia and influenza (ICD-9 codes 48-487). Statistical Methods We used standard nonparametric methods (Pearson x 2 ) for the analysis of contingency table data, and log-linear models 2 to examine the joint influence of age, sex, and season on hospitalizations. We further used two methods to quantify "season." The first was simply the month in which the utilization occurred. Although these divisions do not correspond to any natural definitions of season, variation in outcome from month to month should be indicative of seasonal variation. The second method used three-month groupings (January to March, April to June, July to September, October to December) that roughly correspond to winter, spring, summer, and fall. To present graphic data on seasonal variation (Figs 1 and 2), we used the method adopted by Weiss, 9 in which each month's data is replaced by a 3-month moving average. This tends to "smooth" the resulting data and minimize the noise from the month-to-month variations. To more clearly illustrate peaks and troughs in utilization, the moving averages were then expressed as percent differences from the overall monthly average. For example, in the absence of seasonal variation, we would expect 1 of 12 (8.3%) of the asthma hospitalizations to occur each month. A 3-month moving average of 9.2% would thus translate to 1.4% above the expected average. RESULTS In all, we observed 2,6 prima:ry hospital discharges for asthma and 1,121 prima:ry hospital discharges for emphysema or chronic bronchitis over the 9-year period. For asthma, the 3-month moving average of hospital discharges varied significantly by age (p<.1; Fig 1). The - to 14-year-old group showed a small spring peak and a larger fall peak. Although hospitalizations in this age group appear to be highest in October, this is an artifact of the 3-month moving averages. The peak actually occurs in September ( 1.3% of all asthma hospitalizations), following a lull in July (.1%) and August (4.9%). The 1- to 64-year-old group showed only a spring peak, while the over-64- year-old group exhibited a single peak in the late winter/early spring months. In general, these age-related seasonal patterns were similar for male and female patients. For the 1- to 64-year-old group, however, thepattemsdiddiffersignificantlybygender(p=.). In general, the peak was accentuated in female patients, with female patients having higher peaks in May and June and lower troughs in the fall, particularly CHEST / 11 / 6 / DECEMBER, 1996 149

Table!-Diagnostic Overlap for Hospitalizations. KP, Northwest Region, 1979 to 1987* Age, yr, at Discharge n Asthma Only, No.(%) -14 786 721 (91.7) 1-64 1,13 774 (68.) 6+ 1,26 41 (32.8) Total 3,181 1,91 (6.) Chronic Bronchitis/ Asthma and Chronic Emphysema Only, No. (%) Bronchitis/Emphysema, No. (%) 64 (8.1) 1 (.1 ) 27 (24.3) 81 (7.2) 727 (7.) 123 (97) 1,66 (33.) 2 (6.4) *x 2 test for independence=767.9 on 4 df, p<o.oool. September and October. Log-linear models indicated statistically significant interactions of both age and sex with month. For the combination of chronic bronchitis and emphysema, the monthly patterns of hospital discharges differed from asthma and also varied significantly by age (p=.3; Fig 2). The two younger groups each showed a single peak, although these were somewhat out of phase with each other. The - to 14-year-old group peaked in the fall/winter months (the actual peak was in October), while the 1- to 64-year-old group peaked in the late winter and early spring months. We found no seasonal variation in the 6+-year age group. Generally, we found little evidence of diagnostic overlap between hospitalizations for asthma and hospitalizations for chronic bronchitis/emphysema. Of the 3,181 hospitalizations for which either asthma or chronic bronchitis/emphysema was listed as the primary hospital discharge diagnosis, only 2 (6.4%) included both diagnoses on the discharge summary (Table 1). Even in the 6+-year age group, this figure was less than 1%. To explore the extent to which these seasonal patterns might be explained by seasonal trends in infections, we also determined the extent to which pneumonia and influenza were listed as secondary diagnoses ( comorbidities) when either asthma or chronic bronchitis/emphysema was listed as a primary diagnosis (Table 2). Overall, 4.8% of primary asthma dis- charges and 6.3% of chronic bronchitis/emphysema discharges listed pneumonia or influenza as a comorbidity. In both asthma and chronic bronchitis/emphysema, pneumonia/influenza was most common from January through June. This was statistically significant only for chronic bronchitis/emphysema. Whether there was inadequate statistical power to identify the trend in both groups is unclear. Certainly the proportion of hospitalizations involving pneumonia or influenza as a secondary morbidity was relatively low and accounted for only a small minority of hospitalizations in these groups. DISCUSSION We have demonstrated age-related seasonal patterns in the occurrence of hospitalizations for asthma and for chronic bronchitis/emphysema. The differences in these seasonal patterns by age are unlikely to be related to diagnostic overlap between asthma and chronic bronchitis/emphysema, as the joint occurrence of these conditions as hospital discharge diagnoses was low. However this does not exclude misclassification that may have occurred in older patients. Indeed, following asthma in administrative databases is increasingly unreliable with increasing age because of the likelihood of misclassification of smoking-related COPD. The reasons for differences in seasonal patterns between age groups in both asthma and the combination Table 2-Proportion of Hospitalizations Involving Pneumonia or Influenza as a Secondary Morbidity, KP, Northwest Region 1979 to 1987 Proportion With Secondary Diagnosis Primary Diagnosis Month No. of Discharges of Influenza, % p Value* Asthma January-March 18.8 April-June 2.2..48 July-September 472 3.8 October-December 18 4.4 Total 2,6 4.8 Chronic bronchitis/emphysema January-March 312 8.3 April-June 279 7.9.18 July-September 274 2.6 October-December 6.9 Total 1,121 6.3 *Two-sided p value based on Pearson's x 2 statistic. 146 Clinical Investigations

of chronic bronchitis and emphysema are unclear. In the case of chronic bronchitis/emphysema, the seasonal variations in morbidity decrease with age, with the least seasonal variation seen in the 6+-year-old patients. Reviewing the ICD-9 codes for the children aged to 14 years reveals that the large majmity (n=64) had ICD-9 code 49 bronchitis, NOS (not otherwise specified). Furthermore, the seasonal variation suggests that most of the hospitalizations were in the late fall and early winter. Therefore, we think it likely that these children had either acute or chronic bronchitis. However, it is conceivable that some of the patients are misclassified, with either underlying cystic fibrosis or a 1-antitrypsin deficiency. In any event, the pathophysiologic condition is presumably inflammatory and quite different from that resulting in chronic bronchitis/ emphysema in the older population, with COPD much more common in the latter population, and likely to be related to cigarette smoking. While our data do not permit us to identify the causes of these seasonal patterns, similar patterns for hospitalization for asthma have been reported by Weiss, 9 drawing on the National Hospital Discharge Survey. Many explanations have been suggested. For example, the seasonal pattern in asthma morbidity has been attributed to seasonal fluctuations in the following: specific aeroallergen exposures; 11 12 21-23 "atmospheric" factors such as temperature or humidity; 24 infections; 21 and irritant gases such as ozone and sulfur dioxide. 26 27 Specifically in our cohort, the spring and fall peaks for asthma that we observed in the younger cohorts appear to correlate with seasonal patterns of aeroallergens and, in the - to 14-year-old group, with infections associated with the start of school. However, there may be a different explanation for the fall peak in chronic bronchitis/emphysema since the peak is slightly later than that for asthma whether comparing the monthly peak or the 3-month moving average. That the peak in health-care utilization for asthma in early fall may be related to exposure to infectious agents as children return to school has been suggested elsewhere. 14 Similarly, the fall peaks in chronic bronchitis hospitalizations in the to 14-year-old group (essentially all chronic bronchitis hospitalizations in this age range) suggest more of a link with infections than with aeroallergens. 28 29 However, it is important to recognize that different mechanisms of inflammation might be additive or synergistic, that both aeroallergens and infections may contribute to the increase in fall hospitalizations. 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