Abdominal pain (AP) consultations are common in children. Most children brought to consultation for AP receive a diagnosis of functional disorder. Consultations for AP of nonorganic origin account for 2% to 4% of all pediatric office visits (1). A recent prospective community study revealed a prevalence of AP of 46% among elementary school students (2). Studies in children have shown an association of functional gastrointestinal disorders (FGIDs) with impaired quality of life and lifetime psychiatric disorders (3,4).
Seasonal exacerbations and remissions have been described in adults with FGIDs and several other conditions, including acute myocardial infarction (5–8), leukemia (9), eating disorders (10), anxiety, and mood disorders (11–14). A study of adult patients demonstrated a higher prevalence of seasonal changes in pain and defecation in patients with irritable bowel syndrome (IBS) than in control individuals (15).
Seasonal patterns have also been described in children. A study analyzing calls to a children's Red Cross helpline demonstrated higher levels of depression, anxiety, and pain among children in winter months and a greater number of reports of psychiatric disorders in January and February (16). A prospective cohort study demonstrated a seasonal pattern in AP in Pittsburgh school children of mixed socioeconomic backgrounds, with a higher prevalence of occurrences in February (2). The reasons for these variations are not completely understood. Functional disorders likely result from a combination of biological, environmental, and psychosocial factors, including school-related stress. Some studies demonstrate an influence of latitude on seasonality of various conditions and speculate on the possible influence of number of daylight hours or the effect of climate (17).
Although the pediatric community has long suspected that consultations for AP in children are more common during the winter months, a seasonal variation has never been demonstrated. To explore the consultation pattern of children with AP, we conducted a multicenter study investigating the annual variation of consultations for AP in 6 tertiary care centers. We hypothesized the presence of a seasonal variation in AP consultations, with a winter predominance. To distinguish between the possible influences of school-related factors and latitude, we selected 3 northern and 3 southern sites with similar school schedules.
PATIENTS AND METHODS
The number of outpatient consultations with the diagnosis of AP—International Classification of Diseases (ICD) 9:789.0—and the total number of outpatient consultations was obtained from the following tertiary care institutions at these latitudes: Children's Hospital of Pittsburgh, PA (40 N), Children's Memorial Hospital in Chicago, IL (42 N), Alfred I. DuPont Hospital for Children in Wilmington, DE (38 N), and Nemours Children's Clinics in Jacksonville, FL (30 N), Pensacola, FL (30N), and Orlando, FL (28 N) for the years 2001 through 2004. Pittsburgh, Chicago, and Wilmington will be referred to as northern sites and Jacksonville, Pensacola, and Orlando as southern sites.
All of the patients we considered were seen in primary care pediatric clinics and every pediatric specialty clinic. The visits we analyzed were billed under the 789.0 ICD-9 code, which is used for unspecified AP without a specific abdominal location. The ICD-9 code has specific codes for other conditions that may cause AP, including inflammatory bowel disorders, gastritis, appendicitis, pancreatitis, abdominal surgery, obstetric and gynecological AP, acute AP, and renal disorders. None of these diagnoses were considered to be AP in our study. We excluded all inpatient and emergency department visits.
To analyze the variation in consultation frequency, we selected 4 time periods of interest that we designated summer and winter. On the basis of previous data (2), we defined period 1 as January–February (winter) and period 2 as June–July (summer). As is consistent with customary seasonal definitions, we defined 2 additional 3-month periods: period 3, January–February–March (winter); and period 4, June–July–August (summer).
Rates were defined as the total number of AP consultations divided by the total number of outpatient consultations in each time period and are expressed as cases per 1000 consultations. To confirm that the pattern of consultations in each city behaved similarly in each year of the study, we separately analyzed the data from each city in each of year of the study. Logistic regression analysis was used to determine if there was a difference in the rate of outpatient AP cases by season or by year. An interaction effect was also considered to determine whether seasonal variation differed over the 4 years of observation and was excluded from the final model if it was not statistically significant. The primary interest was to study seasonal variation. Hence, odds ratios (OR) and 95% confidence intervals are reported for differences significant at the 5% level among the seasons only. For differences by year, 2001 was used as the reference year; only overall P values are reported for the effect of year. This study was approved by the institutional review boards at all of the participating institutions.
A total of 3,929,522 outpatient consultations and 73,591 AP consultations were conducted in the 6 tertiary care centers from 2001 through 2004. AP consultations constituted 0.019% (95% confidence interval 0.015%–0.03%) of all consultations. Figure 1 shows the cumulative seasonal patterns of consultation by center. Initially, a generalized model including all cities was used for all of the data. This model indicated that the seasonal effect differed among cities. Hence, separate analyses were conducted for each of the 6 cities. In each of these 6 models, the interaction term between season and year was not statistically significant.
January–February (Winter) vs June–July (Summer)
The rates of AP consultations were consistently higher in the winter months than in the summer months; the differences were statistically significant in all cities. In the northern sites, the winter and summer rates per 1000 consultations were 22.2 versus 18.2 (P < 0.001) in Chicago, 14.8 versus 14.1 (P = 0.023) in Wilmington, and 17.4 versus 15.5 (P < 0.001) in Pittsburgh. In the southern sites, the winter and summer rates per 1000 consultations were 18.1 versus 15.8 (P < 0.001) in Orlando, 20.9 versus 16.7 (P = 0.001) in Pensacola, and 22.1 versus 20.3 (P = 0.004) in Jacksonville. The number of AP consultations, number of total outpatient consultations, and odds ratios are presented in Table 1.
January–March (Winter) vs June–August (Summer)
The rates of AP consultations were consistently higher in the winter months than in the summer months; the differences were statistically significant in all of the cities except Pensacola and Jacksonville. Although the differences between winter and summer rates remained significantly different in Orlando, the third southern site, the difference was smaller in magnitude than when the 2-month periods were considered. In the northern sites, the winter and summer rates per 1000 consultations were 22.4 versus 17.4 (P = 0.002) in Chicago, 15.5 versus 14.0 (P < 0.001) in Wilmington, and 18.1 versus 15.7 (P < 0.001) in Pittsburgh. In the southern sites, the rates per 1000 consultations were 17.1 versus 16.1 (P = 0.011) in Orlando, 20.5 versus 19.3 (P = 0.24) in Pensacola, and 21.8 versus 21.3 (P = 0.25) in Jacksonville. The number of cases, number of total outpatient consultations, and odds ratios are presented in Table 2.
Our study demonstrates the existence of a seasonal variation in outpatient consultations for AP in children. The rates of AP consultations were consistently higher in January and February in each center during each year of our study (total of 24 periods), regardless of the geographic location.
The presence of a seasonal pattern in children is not unique to AP. Such patterns have been demonstrated previously in healthy children and those with other pediatric conditions. A survey conducted in the United States revealed a significantly higher prevalence of irritability, withdrawal, sadness, lower energy, and changes in sleeping and eating habits in healthy children during winter than in fall and spring (18).
The biopsychosocial model is the accepted framework to explain the pathogenesis of FGIDs. It presumes the child's condition to be the result of the interrelation of biological, psychological, and sociocultural factors. Seasonal affective disorder, a psychiatric condition characterized by a predominance of depressive symptoms during the winter months (19), has been associated with biological and psychosocial factors. This condition also seems to be influenced by environmental and geographic factors, including number of daylight hours, temperature, and latitude. An American study involving sites with latitudes similar to those in our study supports the relationship between latitude and seasonal affective disorder (20) by demonstrating a higher prevalence of winter symptoms at northern latitudes. The effect of climate was demonstrated by a study that found a paradoxical pattern in which depression was more prevalent during summer months in Australia. On the basis of study participants' reports that excessive heat and humidity were the 2 factors that most influenced their mood, the authors hypothesized that climate may explain the unique pattern in this particular geographical location (21). Climate was also implicated in the absence of an expected seasonal pattern in the incidence of myocardial infarction in 3 studies of patients living in temperate climates (8).
We propose that environmental factors such as light exposure and temperature as well as a possible effect of latitude may play an additional and yet unexplored role in the pathogenesis of FGIDs. Our study supports this assumption by revealing a potential role for latitude and temperature in the seasonal variation of AP. The analysis of 3-month periods (January–March vs June–August) reveals a change of pattern compared with 2-month periods (January–February vs June–July). When 3-month periods are considered, the difference between the rates in summer and winter decreases in the southern sites but increases in the northern sites. A possible effect of temperature may explain the altered pattern of significance. Average March temperatures in the 3 northern sites (average 39.9°F) are lower than in the southern sites (average 63.0°F), thus potentially limiting the opportunity for children to participate in outdoor activities at northern latitudes.
Several studies have shown a high prevalence of anxiety and depressive symptoms in children with functional AP (18,20,22–24). Stressful events place children at risk for the development of a variety of psychopathological conditions (25), and multiple studies have proposed stress as a risk factor in the onset of functional pain. A prospective study has suggested a positive correlation between AP, anxiety, and stress in adolescents (26). It is possible that school-related stress may play a role in the seasonal variation of AP consultations in our study population. Stress in combination with a busy school schedule, fewer opportunities to participate in outdoor activities, and shorter days may predispose children to anxiety, depression, and AP. Coping skills training based on distraction techniques, visual imagery, and muscle relaxation has proved beneficial in treating pain in children (27,28). Similarly, outside play and outdoor physical activity may serve as natural coping strategies in children with pain. We cannot exclude the effect of other unexplored factors, such as the effect of sunlight on homeostasis of calcium, which should be investigated in future studies.
A prospective study by our group showed a similar distribution of AP in healthy children at the community level (2), suggesting that this pattern is not limited to tertiary care patients. The fact that a similar seasonal pattern in AP was found in a group of healthy school children (25) leads us to speculate that children with AP exhibit a spectrum of behavior that ranges from apparently normal daily functioning to loss of functional capacity. Genetic susceptibility, early life experiences, psychiatric comorbidity, sociocultural issues, and coping mechanisms may be involved in these differential behavior patterns. Our analysis of the monthly pattern of symptoms did not demonstrate a correlation with the entire school year, suggesting that additional factors play a role in what is likely to be a multifactorial condition.
Differences in circadian rhythms and sleep–wake cycles may constitute additional factors that have not yet been investigated. The secretion of melatonin, a neurohormone initially associated exclusively with pineal gland production, varies with daylight and darkness. Melatonin concentration is several hundred–fold higher in the gastrointestinal tract than in the pineal gland. Serotonin, a neurotransmitter thought to play an important role in the pathogenesis of FGID, is also characterized by a dynamic circadian rhythm (29). Melatonin, a derivative of serotonin, is also involved in the regulation of gastrointestinal motility, sensation, stress, and mucosal inflammation—factors that have been associated with the pathogenesis of FGIDs (17,30). The concentration of gastrointestinal melatonin peaks at night and after meals. The effect of melatonin in the gastrointestinal tract and a possible relation with FGIDs has been recently shown in 3 randomized studies in adults, which demonstrated its effectiveness in comparison with placebo for the treatment of IBS (31–33).
Irritable bowel syndrome may follow an enteric infection (34,35). A possible peak in the prevalence of gastroenterological infections in winter months could be linked to an increase of consultations for AP. Postinfectious IBS has been described after bacterial and viral infections (36). Analysis of the Centers for Disease Control and Prevention monthly report of the bacterial pathogens usually associated with postinfectious IBS reveals a markedly different seasonal pattern from that in our study (37). The epidemiology of enteric viral infection is similar to that of the presentation of AP described in this report. Viral infections have been linked to the development of brief postinfectious FGIDs (36). Transient and mild gastrointestinal viral infections may be contributing factors to the seasonal variation that was described in our study.
To our knowledge, our study is the first pediatric investigation into the seasonal distribution of AP. The analysis of a large number of consultations, the consistency of the data across time and geographic locations, and the investigation of previously unexplored factors that could intervene in the pathogenesis of AP constitute some of the strengths of our investigation. Because of the methodology used in this study, we cannot determine how many children had a functional disorder rather than an organic disease as a cause of chronic AP. The vast majority of children referred to pediatric gastroenterologists with chronic AP have functional AP (38), and it is likely that this was also the case in our centers. To control for the accuracy of our data, a similar method was used to evaluate for a seasonal variation in patients consulting for Crohn disease, an organic condition frequently associated with pain (39). No seasonal pattern was found in this group of patients, a finding that correlates with previous American studies (40). The inability to distinguish between initial and subsequent consultations and to determine the age, sex, and socioeconomic composition of our sample constitutes another shortcoming that we acknowledge. In the future, prospective investigations should be designed to address these issues.
In summary, there seems to be a seasonal variation in the consultation patterns for AP at the tertiary care level. Given the high prevalence of AP in children, further studies exploring the role of daylight hours, climate, latitude, and stress in mediating its pathogenesis are warranted.
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