Association of Daily Variance in Air Temperature With Postoperative Adhesive Small Bowel Obstruction

Introduction: The influence of air temperature on adhesive small bowel obstruction (ASBO) is unknown. This study aimed to investigate the relationship between air temperature and postoperative ASBO. Methods: Overall, 312 patients with postoperative ASBO were included. They were categorized into two groups: the surgery group (n = 83) comprising patients who needed surgery, and the non-surgery group (n = 229) comprising patients who responded to conservative treatment. The associations between patients’ characteristics and weather variables on days of symptom onset with the need for surgical management were investigated. Weather variables included the daily mean barometric pressure, daily mean air temperature, day-to-day differences, daily variances, and diurnal variation in the air temperature. Day-to-day differences in weather variables were calculated as the daily mean variables on the day of symptom onset minus those on the previous day. The daily variances in weather variables were defined as the absolute value of day-to-day differences. Results: Compared to the non-surgery group, the surgery group had older patients (75 vs. 70 years, p = 0.009), a higher proportion of female patients (44.6% vs. 32.3%, p = 0.046), increased incidence of closed-loop sign (50.6% vs. 0.9%, p < 0.001), a lower proportion of feces sign (18.1% vs. 31.3%, p = 0.024), and a prolonged hospital stay (11 vs. 22 days, p < 0.001). The number distribution of patients in the surgery group in day-to-day differences in air temperature was different from that of the non-surgery group; the former has several peaks whereas the latter has almost one peak. Daily variance in mean air temperature on the day of symptom onset was higher in the surgery group than in the non-surgery group (2.3 vs. 1.3℃, p < 0.001). Multiple logistic regression analysis revealed that increased daily variance in air temperature on the onset day was associated with the need for surgical management (odds ratio 1.254, p = 0.002) and closed-loop obstruction (odds ratio 1.235, p = 0.017). Regarding seasonal variations, the risk of the need for surgery and closed-loop obstruction in each ASBO patient was the highest in spring, followed by that in summer, autumn, and winter. Consistently, the daily variance in mean air temperature in spring was higher than that in summer, autumn, and winter (p < 0.0001, p < 0.0001, and p = 0.0047, respectively). The risk of the need for surgery and closed-loop obstruction in each ASBO patient was the highest in spring, followed by that in summer, autumn, and winter. Consistently, daily variance in mean air temperature was higher in spring than that in summer, autumn, and winter (p < 0.0001, p < 0.0001, and p = 0.0047, respectively). Conclusion: Increased daily variance in mean air temperature on the day of onset is associated with the need for surgical management and closed-loop obstruction. Spring is characterized by the highest daily variance in mean air temperature among the four seasons, and is associated with high proportions of the need for surgery and closed-loop obstruction. These results can be clinically useful in terms of hospital resource reallocation and staffing, and can help clarify the pathogenesis of ASBO.


Introduction
Adhesive small bowel obstruction (ASBO) is one of the most common complications that occur after intraabdominal surgery. Several factors are associated with successful non-surgical management of patients with ASBO. For example, the feces sign (FS) [1][2][3], number of transitional zones [4], beak signs [5], anterior adhesion [6,7], sex differences [8], and administration of water-soluble contrast agents [6,7,9] affect the response of patients with ASBO to non-surgical management.
Recently, we reported that fluctuations in barometric pressure occurred in the pre-onset period in patients with postoperative ASBO, which indicates the impact of changes in weather variables on the onset of ASBO [10]. However, the influence of air temperature on ASBO has not yet been investigated. 1 1 1 1 1 The gastrointestinal tract is innervated by the enteric nervous system with cold chemosensors that are activated by low temperatures [11][12][13]. The enteric nervous system also influences secretory functions and modulates gastrointestinal tract motility [14,15]. Therefore, we hypothesized that air temperature could affect the etiology and the prognosis of patients with ASBO. This study aimed to investigate the relationship between air temperature and postoperative ASBO.

Patients and study design
A total of 341 patients with ASBO were admitted to Shinshu University Hospital, Japan, between March 1, 2007 and April 30, 2021. ASBO was diagnosed based on the presence of two criteria: 1) clinical symptoms, including nausea, vomiting, and abdominal pain; and 2) radiological imaging that showed a dilated small intestine with a diameter >2.5 cm. We excluded 29 patients who did not undergo abdominal surgery before the onset of ASBO. Our final study group comprised 312 patients with postoperative ASBO. We retrospectively reviewed their medical records and categorized them into two groups: the surgery group (n = 83), which comprised those who needed surgery, and the non-surgery group (n = 229), which comprised those who responded to conservative treatment (shown in Figure 1). Furthermore, we assessed the daily mean barometric pressure and the daily mean air temperature and determined their day-to-day differences and daily variances. Day-to-day differences in weather variables were calculated as the daily mean variables on the day of symptom onset minus those on the previous day. The daily variances in weather variables were defined as the absolute values of day-to-day differences. The daily variances in air temperature in the perionset period were also defined as the absolute differences between the daily mean air temperature on the index day and their respective values on the previous day. Diurnal variation in air temperature was defined as the variation between the highest and the lowest air temperature that occurred during the day of onset. The Shinshu University Hospital is located in Matsumoto City (altitude, 610 m), almost at the center of the main island of Japan. Daily weather variables in Matsumoto City were measured using the Automated Meteorological Data Acquisition System at the Matsumoto Meteorological Station, and the website of the Japan Meteorological Agency (URL: www.jma.go.jp/jma/index.html). Barometric pressure and air temperature were recorded as the average of continuous measurements from 0:00 to 24:00. The associations between the patients' characteristics, need for surgical management, closed-loop obstruction and weather variables were investigated. ASBO, adhesive small bowel obstruction.
Regarding the management of ASBO, intravenous fluids were administered to all patients. Initially, we assessed the presence of strangulation of the small intestine, which requires emergency surgery. When strangulation was excluded, the patients with non-strangulated ASBO were considered as candidates for non-surgical management. Regarding the general treatment strategies for non-strangulated ASBO, patients with active symptoms, such as abdominal pain and nausea, were treated using gastrointestinal decompression methods, including nasogastric tube placement and long tube placement. If intestinal obstruction continued for more than seven days, or if it recurred after the commencement of oral feeding, non-surgical management was considered to have failed and the patients underwent surgery. A closed-loop sign was defined as an obstruction of two points of the small intestine at the same site, and this was confirmed using computed tomography (CT) imaging.
Lastly, we analyzed the seasonal variations in the incidence of ASBO, risk of the need for surgery, proportion of the closed-loop obstruction, and daily variance in mean air temperature during the study period. Four seasons were defined as follows: spring, March 1 to May 31; summer, June 1 to August 31; autumn, September 1 to November 30; and winter, December 1 to February 28.

Statistical analysis
Demographic data were presented using descriptive statistics. Continuous variables were presented as medians with interquartile ranges (IQR) and were compared using the Mann-Whitney test. Multiple logistic regression analysis was performed to identify factors that were independently associated with the need for surgical management, emergency surgery, and closed-loop obstruction. The results of multiple logistic regression analysis are presented as odds ratios (ORs) with 95% confidence intervals (CIs). Unpaired ttest with Bonferroni correction for multiple comparison was used to compare daily variance in mean air temperature between the four seasons. In this test, a p-value of <0.0125 (0.05÷4) was considered statistically significant. All the other tests were two-tailed, and, except for unpaired t-test with Bonferroni correction, a p-value of <0.05 was considered statistically significant. Statistical analyses were performed using the Statistical Package for Social Sciences version 23.0 (IBM Corp., Armonk, NY, USA).

Results
The patients' characteristics are presented in  Compared to the non-surgery group, the surgery group had older patients (75 years vs. 70 years, p = 0.009), a higher proportion of female patients (44.6% vs. 32.3%, p = 0.046) and increased incidence of closed-loop sign (50.6% vs. 0.9%, p < 0.001), a lower proportion of patients with the feces sign (18.1% vs. 31.3%, p = 0.024), and had prolonged length of hospital stay (11 days vs. 22 days, p < 0.001). Regarding weather variables, the daily variance in mean air temperature on the day of symptom onset in the surgery group was larger than that in the non-surgery group (2.3 ℃ vs. 1.3 ℃, p < 0.001), whereas there was no difference in the diurnal variation in air temperature between these groups (11.0 ℃ vs. 10.3 ℃, p = 0.140) ( Table 2).

Demographic Characteristics Surgery (n = 83)
Non-surgery (n = 229) P-value 2022   Regarding weather variables, Figures 2A-2E show the distributions of the number of patients in the surgery and non-surgery groups for each of the five weather variables. The shapes of the histograms for the number of patients in the surgery group relative to day-to-day differences in air temperature are quite different from that in the non-surgery group, as the former has several peaks whereas the latter has nearly one peak. In this context, the daily variance in mean air temperature on the day of symptom onset in the surgery group was larger than that in the non-surgery group (2.3℃ vs. 1.3℃, p < 0.001) ( Table 2).   Table 3 show the daily variance in mean air temperature in the peri-onset period. The variance in the surgery group increased suddenly on the day of onset, resulting in a statistically significant difference between the variances on the day of onset and those on post-onset day one, compared to those in the nonsurgery group (2.3℃ vs. 1.3℃, p < 0.001 and 2.0℃ vs. 1.2℃, p < 0.001, respectively).

Surgery (n = 83) Non-surgery (n = 229) P-value
Pre-onset day 10 (°C)     Figure 4 shows the associations between seasons and the incidence of ASBO, the risk of the need for surgery, and the proportion of the closed-loop obstruction. The incidence of ASBO was higher in autumn than in any other season ( Figure 4A). On the other hand, the risk of the need for surgery and closed-loop obstruction in each ASBO patient was the highest in spring, followed by that in summer, autumn, and winter ( Figures 4B,  4C). Consistently, daily variance in mean air temperature in spring was higher than that in summer, autumn, and winter (p < 0.0001, p < 0.0001, and p = 0.0047, respectively) ( Figure 4D).

FIGURE 4: Seasonal variations in adhesive small bowel obstruction and daily variance in mean air temperature
Each graph shows seasonal variations in the incidence of ASBO (A), proportion of patients needing surgery (B), proportion of patients with closed-loop obstruction (C), and daily variance in mean air temperature (D). Data are presented as mean and standard deviation (D). P-values were determined by a two-tailed unpaired t-test with Bonferroni correction for multiple comparisons, and a p-value of <0.0125 was considered statistically significant. ASBO, adhesive small bowel obstruction.

Discussion
In the present study, we report that increased daily variance in mean air temperature on the day of symptom onset is associated with the need for surgery and the presence of a closed-loop obstruction in patients with ASBO. Our findings can predict the need for surgery based on the daily variance in mean air temperature, which is clinically useful for the reallocation of hospital resources and staffing, as well as help clarify the pathogenesis of ASBO.
The gastrointestinal tract is directly associated with temperature. The gastrointestinal tract is innervated by the enteric nervous system, comprising a widespread neural network enveloped by the intestinal wall, and controls motility, peristalsis, and intestinal secretions [16]. The transient receptor potential ion channel families are expressed by primary afferent neurons operating as cold chemosensors and activated by cold temperature in the gastrointestinal tract [11][12][13]. These neurons are involved in secretory mechanisms and modulation of the gastrointestinal tract motility [14,15], suggesting that fluctuations in air temperature affect the small intestine and may contribute to the pathogenesis of ASBO. A closed-loop obstruction occurs when two points of the small intestine are obstructed at the same site, and requires immediate surgical intervention [17,18]. It is observed in patients with ASBO due to an adhesive band and is not seen in patients with ASBO due to a matted adhesion [19]. These reports indicate the different etiologies of ASBO with and without a closed-loop sign. Our results suggest that the change in intestinal motility and secretion caused by fluctuation in air temperature can accelerate the onset of a closed-loop obstruction, which is associated with adhesive bands. This does not mean that daily variance of air temperature leads to deterioration in the condition of patients with ASBO but rather means that such variance is associated with the incidence of ASBO that requires surgical intervention, such as closed-loop obstruction. In the multiple logistic regression analysis, the closed-loop sign was not used as a predictor variable of surgical management. This is because the sign has already been reported to be associated with the requirement for immediate surgical intervention [17,18] and was regarded as an intermediate variable.
Regarding seasonal variations (Figure 4), although not statistically proven, spring is associated with a high risk of the need for surgery and closed-loop obstruction. Consistently, the daily variance in mean air temperature in spring was the highest among all seasons. These results support our data that increased daily variance in mean air temperature on the day of symptom onset of ASBO is associated with the need for surgery and the presence of a closed-loop obstruction.
This study has several limitations. First, the daily variance in mean air temperature in our result seemed too small to affect the small intestine. Diurnal variations in air temperature on the onset day in both groups were more than 10 ℃, thus, the value of the daily variance in mean air temperature on the onset day was considerably lower than the change in air temperature that patients with ASBO were exposed on onset day. Therefore, the daily variance in air temperature may be a surrogate marker of a meteorological factor that increased the incidence of ASBO requiring surgical management. Second, the weather variables we used did not perfectly represent the exact values at the specific times and locations of patients with ASBO. This is because not all the patients in this study lived in Matsumoto City, and the weather variables that we used in this study were the mean values in 24 hours. Finally, this was a single-center retrospective study and our findings may be subject to selection bias. Therefore, prospective multi-center studies that include a larger patient population are necessary to confirm these findings.

Conclusions
We report that increased daily variance in mean air temperature on the day of symptom onset is associated with the need for surgery in patients with ASBO. In addition, it is related to the occurrence of closed-loop obstruction. Further, spring, characterized by the highest daily variance in mean air temperature among four seasons, is associated with high proportions of the need for surgery and closed-loop obstruction.
ASBO is a common cause of postoperative morbidity and can be a life-threatening disease. These results can be clinically useful in terms of reallocation of hospital resources and staffing, as well as clarification of the pathogenesis of ASBO.

Additional Information Disclosures
Human subjects: Consent was obtained or waived by all participants in this study. Ethical Committee of Shinshu University Hospital issued approval 4557. Informed consent was obtained from each patient using the opt-out method. . Animal subjects: All authors have confirmed that this study did not involve animal subjects or tissue. Conflicts of interest: In compliance with the ICMJE uniform disclosure form, all authors declare the following: Payment/services info: All authors have declared that no financial support was received from any organization for the submitted work. Financial relationships: All authors have declared that they have no financial relationships at present or within the previous three years with any organizations that might have an interest in the submitted work. Other relationships: All authors have declared that there are no other relationships or activities that could appear to have influenced the submitted work.