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The synergy between diurnal temperature range and calcium concentration help to predict hospital mortality in patients with acute myocardial infarction

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Baseline demographic and clinical characteristics of the study participants stratified by serum calcium concentration on admission

A total of 3780 patients with AMI met the criteria for inclusion in our study. Among these 3780 patients, 188 (4.97%) died during hospitalization. The mean age of all our study patients was 58.9 years (SD, 10.6 years), and 2798 patients (74.0%) were male. A total of 1608 patients (42.5%) had hypertension, 759 (20.1%) had a history of diabetes mellitus, and 311 (8.2%) had a history of stroke. Most patients had STEMI (2614/3780, 69.2%), and more than half were current smokers (2030/3780, 53.7%).

Serum calcium concentration (measured in each patient at the time of hospital admission) approximated to a normal distribution (Supplemental Fig. S1) with a mean level of 2.26 mmol/L (SD, 0.15 mmol/L) and a median level of 2.26 mmol/L (IQR, 2.19–2.33 mmol/L). The distribution of DTR exhibited slight positive skewness (Supplemental Figure S2) with a mean temperature difference of 10.26 °C (SD, 3.56 °C) and a median temperature difference of 9.90 °C (IQR, 7.69–12.60 °C).

Based on the admission serum calcium concentrations, the patients were stratified into quartiles: Ca-Q1 (serum calcium concentration < 2.19 mmol/L), n = 892; Ca-Q2 (serum calcium concentration 2.19–2.26 mmol/L), n = 997; Ca-Q3 (serum calcium concentration 2.27–2.33 mmol/L), n = 883; and Ca-Q4 (serum calcium concentration > 2.33 mmol/L), n = 1008. The clinical characteristics of the patients in each of the serum calcium quartiles are shown in Table 1. Age, BUN, HDL-C, serum creatinine, uric acid, serum phosphate, serum magnesium, serum chloride and left atrial diameter (LAD) were significantly higher in patients with low serum calcium levels than in patients with elevated levels of serum calcium (all P < 0.05; Table 1).

Table 1 Clinical characteristics of the 3780 patients with acute myocardial infarction stratified according to serum calcium concentration quartiles.

Association between serum calcium concentration and in-hospital mortality

Patients in the lowest serum calcium quartile exhibited the highest incidence of in-hospital mortality (Table 1). As shown in Fig. 1, in-hospital mortality progressively increased with a decrease in the quartile of serum calcium concentration.

Figure 1
figure 1

In-hospital mortality of patients with AMI according to the quartile of the distribution of serum calcium concentration on admission. In-hospital mortality increased with a decrease in the quartile of serum calcium concentration.

Univariate logistic regression analysis found that age, gender, current smoking, current alcohol use, diabetes mellitus, HDL-C, uric acid, serum phosphate, serum potassium, left ventricular ejection fraction (LVEF), LAD and serum calcium concentration were factors significantly associated with in-hospital mortality (Supplemental Table S1). However, multivariate logistic regression analysis revealed that only age, gender, diabetes mellitus, HDL-C, uric acid, serum phosphate, LVEF and serum calcium concentration were independently associated with in-hospital mortality (Supplemental Table S2).

As shown in Table 2, the odds of in-hospital mortality were significantly lower among study patients with serum calcium concentration in the highest quartile (> 2.33 mmol/L) than among those with serum calcium concentration in the lowest quartile (< 2.19 mmol/L) in model 1 (unadjusted; OR, 0.53; 95% CI, 0.45–0.63; P for trend < 0.001), model 2 (adjusted for age and gender; OR, 0.57; 95% CI, 0.48–0.68; P for trend < 0.001) and model 3 (adjusted for all significant factors in the univariate analysis; OR, 0.56; 95% CI, 0.47–0.67; P for trend < 0.001).

Table 2 The association between serum calcium concentration and in-hospital mortality of patients with acute myocardial infarction analyzed using three different logistic regression models.

Moderating effect of DTR on the association between serum calcium concentration and in-hospital mortality

The patients were stratified into quartiles based on admission DTR: DTR-Q1 (DTR < 7.7 °C), n = 945; DTR-Q2 (DTR 7.7–9.9 °C), n = 910; DTR-Q3 (DTR 10.0–12.6 °C), n = 972; and DTR-Q4 (DTR > 12.6 °C), n = 953. Logistic regression analysis showed that DTR was not independently associated with in-hospital mortality (Supplemental Table S3). However, subgroup analyses revealed that the association between serum calcium concentration and in-hospital mortality was moderated by different quartiles of admission DTR (Table 3). Although the association between serum calcium concentration and in-hospital mortality was significant in most of the subgroups analyzed (Table 3), only DTR was observed to interact significantly with serum calcium concentration (P-interaction = 0.020).

Table 3 The association between serum calcium concentration and in-hospital mortality of patients with acute myocardial infarction: subgroup analyses.

All analyses were adjusted for the same variables as model 3 in Table 2, except for the stratification variable. Ca-Q1: serum calcium concentration < 2.19 mmol/L; Ca-Q2: serum calcium concentration 2.19–2.26 mmol/L; Ca-Q3: serum calcium concentration 2.27–2.33 mmol/L; Ca-Q4: serum calcium concentration > 2.33 mmol/L; DTR-Q1: diurnal temperature range < 7.7 °C; DTR-Q2: diurnal temperature range 7.7–9.9 °C; DTR-Q3: diurnal temperature range 10.0–12.6 °C; DTR-Q4: diurnal temperature range > 12.6 °C. NA: not available due to limited sample size. Abbreviations: ACEI, angiotensin converting enzyme inhibitor; AMI, acute myocardial infarction; ARB, angiotensin receptor blocker; DTR, diurnal temperature range; CI, confidence interval; NSTEMI, non-ST-segment elevation myocardial infarction; OR, odds ratio; STEMI, ST-segment elevation myocardial infarction.

Supplemental Table 4 showed that patients with low serum calcium levels in the highest quartile of admission DTR (> 12.6 °C) had a notably increased risk of in-hospital mortality compared with patients in the lowest quartile of DTR (< 7.7 °C) after adjustment for potential confounders (Q4:Q1 OR, 0.04; 95% CI, 0.01–0.23; P < 0.001). This strong negative association of DTR with in-hospital mortality was consistent between different regression models and the various quartiles of serum calcium concentration. This model of the moderating effect of DTR, built based on a multivariate logistic regression model, is shown in Fig. 2. The Odds ratios and 95% CIs of in-hospital mortality of serum calcium concentration (Q4 vs. Q1) for patients in the lowest, second and third quartiles of DTR were 0.29 (95% CI, 0.10–0.86; P = 0.025), 0.20(95% CI, 0.06–0.69; P = 0.011), and 0.15 (95% CI, 0.04–0.55; P = 0.004) respectively. Smooth curve fitting showed that for the third and fourth quartiles of DTR, the relationship between serum calcium concentration and in-hospital mortality was L-shaped, and the in-hospital mortality progressively decreased with increasing serum calcium concentration up to ~ 2.45 mmol/L (Fig. 3).

Table 4 Net reclassification improvement among patients in the highest quartile of diurnal temperature range (> 12.6 °C) after adjustment for serum calcium concentration.
Figure 2
figure 2

Model to show how different quartiles of admission diurnal temperature range (DTR) moderated the association between serum calcium concentration and in-hospital mortality of patients with acute myocardial infarction. β1 = age, gender, current smoking, current alcohol use, diabetes mellitus, high-density lipoprotein cholesterol, uric acid, serum phosphate, serum potassium, left ventricular ejection fraction and left atrial diameter. β2 = the independent effect of diurnal temperature range (DTR) on in-hospital mortality after adjusting for the above covariates. β3 = the interaction effect of serum calcium concentration and DTR on in-hospital mortality after adjusting for the above covariates. r = correlation between serum calcium concentration and DTR. *P < 0.05.

Figure 3
figure 3

Spline plots displaying the risk of in-hospital mortality over a range of serum calcium concentrations stratified by quartiles of diurnal temperature range (DTR). Smooth curve fitting revealed an L-shaped relationship of in-hospital mortality with serum calcium concentration for the third and fourth quartiles of DTR.

The value of serum calcium concentration for the prediction of in-hospital mortality

The value of serum calcium concentration for the prediction of in-hospital mortality in different quartiles of DTR is shown in Fig. 4. Compared with other quartiles of DTR, the independent ROCAUC for serum calcium concentration in the highest quartile of DTR was 0.72 (95% CI, 0.69–0.75; P < 0.001). Among patients in the highest quartile of DTR, the combined predictive values in the risk factor models with and without serum calcium concentration were 0.81 (95% CI, 0.76–0.84; P < 0.001) and 0.76 (95% CI, 0.72–0.79, P < 0.001), respectively.

Figure 4
figure 4

The area under the receiver operating characteristic curve (ROCAUC) of serum calcium concentration in the prediction of in-hospital mortality among patients with acute myocardial infarction stratified by quartiles of DTR (A). Compared with other quartiles of DTR, the independent ROCAUC for serum calcium concentration in the highest quartile of DTR was 0.72 (95% CI, 0.69–0.75; P < 0.001). Multivariate combined ROCAUC, which was estimated using a regression model that included age, gender, current smoking, current alcohol use, diabetes mellitus, high-density lipoprotein cholesterol, uric acid, serum phosphate, serum potassium, left ventricular ejection fraction and left atrial diameter, with or without serum calcium among patients in the highest DTR quartile (B). The combined predictive values with and without serum calcium concentration were 0.81 (95% CI, 0.76–0.84; P < 0.001) and 0.76 (95% CI, 0.72–0.79; P < 0.001), respectively. AUC, area under the curve; CI, confidence interval.

In addition, we also performed NRI analyses to reveal whether the inclusion of serum calcium concentration would improve the reclassification ability of the model. Among patients in the highest quartile of DTR, the results showed that 2.9% of the individuals who survived and 28.6% of those who died in hospital would be correctly reclassified when the clinical model (including the above risk factors) included serum calcium concentration (Table 4). These reclassification rates led to an estimated NRI of 20.2% (95% CI, 7.5–32.9; P = 0.001). In addition, statistically significant NRI was not observed among patients in other quartiles of DTR.


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