Association of plasma free triiodothyronine levels with contrast-induced acute kidney injury and short-term survival in patients with acute myocardial infarction

in Endocrine Connections
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  • 1 Department of Cardiology, The Affiliated Changzhou No.2 People’s Hospital of Nanjing Medical University, Changzhou, Jiangsu, China
  • | 2 Section of Pacing and Electrophysiology, Division of Cardiology, The First Affiliated Hospital of Nanjing Medical University, Nanjing, Jiangsu, China
  • | 3 Department of Cardiology, Xuzhou Central Hospital, Xuzhou Clinical School of Nanjing Medical University, Xuzhou, Jiangsu, China
  • | 4 Dalian Medical University, Dalian, Liaoning, China

Contributor Notes

Correspondence should be addressed to X Zhou or Q Wang or F Zhang: xzzyx2008@sina.com or wang-qingjie@hotmail.com or njzfx6@njmu.edu.cn

*(L Sun, W Zhu and Y Ji contributed equally to this work)

Open access

Objective

Post-treatment contrast-induced acute kidney injury (CI-AKI) is associated with poor outcomes in patients with acute myocardial infarction (AMI). A lower free triiodothyronine (FT3) level predicts a poor prognosis of AMI patients. This study evaluated the effect of plasma FT3 level in predicting CI-AKI and short-term survival among AMI patients.

Methods

Coronary arteriography or percutaneous coronary intervention was performed in patients with AMI. A 1:3 propensity score (PS) was used to match patients in the CI-AKI group and the non-CI-AKI group.

Results

Of 1480 patients enrolled in the study, 224 (15.1%) patients developed CI-AKI. The FT3 level was lower in CI-AKI patients than in non-CI-AKI patients (3.72 ± 0.88 pmol/L vs 4.01 ± 0.80 pmol/L, P < 0.001). Compared with those at the lowest quartile of FT3, the patients at quartiles 2–4 had a higher risk of CI-AKI respectively (P for trend = 0.005). The risk of CI-AKI increased by 17.7% as FT3 level decreased by one unit after PS-matching analysis (odds ratio: 0.823; 95% CI: 0.685–0.988, P = 0.036). After a median of 31 days of follow-up (interquartile range: 30–35 days), 78 patients died, including 72 cardiogenic deaths and 6 non-cardiogenic deaths, with more deaths in the CI-AKI group than in the non-CI-AKI group (53 vs 25, P < 0.001). Kaplan–Meier survival analysis showed that patients at a lower FT3 quartile achieved a worse survival before and after matching.

Conclusion

Lower FT3 may increase the risk of CI-AKI and 1-month mortality in AMI patients.

Abstract

Objective

Post-treatment contrast-induced acute kidney injury (CI-AKI) is associated with poor outcomes in patients with acute myocardial infarction (AMI). A lower free triiodothyronine (FT3) level predicts a poor prognosis of AMI patients. This study evaluated the effect of plasma FT3 level in predicting CI-AKI and short-term survival among AMI patients.

Methods

Coronary arteriography or percutaneous coronary intervention was performed in patients with AMI. A 1:3 propensity score (PS) was used to match patients in the CI-AKI group and the non-CI-AKI group.

Results

Of 1480 patients enrolled in the study, 224 (15.1%) patients developed CI-AKI. The FT3 level was lower in CI-AKI patients than in non-CI-AKI patients (3.72 ± 0.88 pmol/L vs 4.01 ± 0.80 pmol/L, P < 0.001). Compared with those at the lowest quartile of FT3, the patients at quartiles 2–4 had a higher risk of CI-AKI respectively (P for trend = 0.005). The risk of CI-AKI increased by 17.7% as FT3 level decreased by one unit after PS-matching analysis (odds ratio: 0.823; 95% CI: 0.685–0.988, P = 0.036). After a median of 31 days of follow-up (interquartile range: 30–35 days), 78 patients died, including 72 cardiogenic deaths and 6 non-cardiogenic deaths, with more deaths in the CI-AKI group than in the non-CI-AKI group (53 vs 25, P < 0.001). Kaplan–Meier survival analysis showed that patients at a lower FT3 quartile achieved a worse survival before and after matching.

Conclusion

Lower FT3 may increase the risk of CI-AKI and 1-month mortality in AMI patients.

Introduction

Thyroid hormone level changes with the development of acute myocardial infarction (AMI) in patients without prior thyroid disease (1, 2, 3). Low triiodothyronine (T3) syndrome (LT3S), manifested as serum T3 level and normal levels of thyroid-stimulating hormone (TSH) and thyroxine (T4), is a common thyroid dysfunction (4, 5). Free T3 (FT3) plays various roles in the cardiovascular system (6, 7). Many publications have reported that a low FT3 is associated with a poor prognosis in patients with heart disease (8, 9, 10, 11). This suggests that cardiovascular function declines as FT3 level drops in AMI patients.

In patients receiving percutaneous coronary intervention (PCI), 5.2–59% of them may suffer from contrast-induced acute kidney injury (CI-AKI) (12, 13, 14). CI-AKI is associated with increased dialysis odds and 1-year mortality (15, 16, 17).

However, no studies have been conducted to assess whether lower FT3 could predict CI-AKI risk in patients with aggressive AMI. In this study, we aimed to investigate the association of FT3 level with CI-AKI risk and short-term survival in AMI patients undergoing PCI or coronary arteriography (CAG).

Methods

Study participants

The research program was formulated in accordance with the ethical guidelines of the 1975 Declaration of Helsinki and approved by the Ethics Committee of the Affiliated Changzhou No. 2 People’s Hospital of Nanjing Medical University. Each patient signed informed consent before enrollment in this study. This trial was registered in the Chinese Clinical Trials Registry (ChiCTR1800014583).

As shown in Fig. 1, a total of 2381 participants aged over 18 years and diagnosed with AMI between January 2010 and January 2018 in the Affiliated Changzhou Second People’s Hospital of Nanjing Medical University were recruited. The diagnosis of AMI was based on symptom, cardiac troponin, renal dysfunction, and electrocardiographic changes (18). A total of 512 patients were excluded because they had (i) refused CAG or PCI therapy; (ii) been diagnosed with myocarditis, pericarditis, valvular disease, severe infection, or old myocardial infarction; (iii) received emergency coronary artery bypass grafting. Of the remaining 1869 patients, 389 patients were further excluded for (i) absence of postoperative creatinine, baseline creatinine, value of FT3; (b) FT3 >6.8 pmol/L; (iii) perioperative dialysis treatment; (iv) past history of thyroid diseases; (v) history of medication for thyroid diseases, or medication causing thyroid dysfunction (e.g. amiodarone, glucocorticoid, interferon-alpha). Finally, 1480 subjects were enrolled.

Figure 1
Figure 1

Study flow chart. AMI, acute myocardial infarction; CAG, coronary angiography; PCI, percutaneous coronary intervention.

Citation: Endocrine Connections 11, 7; 10.1530/EC-22-0120

AKI definition

Baseline serum creatinine level was measured at 24 h before operation. AKI was defined as serum creatinine with an absolute increase ≥0.3 mg/dL (26.4 µmol/L) or ≥ 150% higher than the baseline level within 48 h after CAG or PCI treatment according to the Kidney Disease Improving Global Outcomes (KDIGO) criteria (19). Serum creatinine was detected within 48 h after intervention treatment.

PCI and CAG

For CAG or PCI, the Seldinger technique was conducted by physicians experienced in digital subtraction angiography. The procedural characteristics were recorded (20).

Blood collection and plasma thyroid hormone assays

Blood was sampled and tested for thyroid hormone within 24 h after AKI onset. Serum TSH level was tested by enhanced chemiluminescence assay (21). The reference range was 3.1–6.8 pmol/L for FT3, 12–22 pmol/L for free thyroxine (FT4), and 0.27–4.2 µIU/mL for TSH in adults. Hyperthyroidism was diagnosed as elevated FT3 and (or) FT4 levels with reduced serum TSH level; hypothyroidism as decreased FT3 and (or) FT4 levels with increased TSH level; subclinical hyperthyroidism as decreased serum TSH level and normal serum FT4 and FT3 levels (22); and subclinical hypothyroidism as elevated serum TSH level and normal FT3 and FT4 levels (23).

Endpoints

According to the incidence of AKI, patients were divided into the CI-AKI group and the non-CI-AKI group with a propensity score (PS). The abbreviated MDRD equation was used to estimate glomerular filtration rate (eGFR) according to the baseline serum creatinine concentration (24). The primary endpoint was set as the development of CI-AKI after CAG or PCI, and the secondary endpoint was set as all-cause mortality within 30 days after coronary intervention.

Statistical analysis

Continuous variables were expressed as means with s.d. or median and interquartile range 25–75%. Discrete variables were expressed as percentage. Mann–Whitney U-test and Student’s t-test were used to evaluate continuous variables, and chi-squared test and Fisher’s exact test were used to evaluate categorical variables about demographic and clinical characteristics.

Restricted cubic spline regression models were used to determine the continuous changes in CI-AKI risk and FT3 level. Multivariate analysis (binary logistic regression), comprising factors of clinical interest and all significant covariates in univariate analysis, was performed to investigate the association between CI-AKI and FT3. The results were presented as odds ratios (OR) and 95% CIs.

After that, a PS-matched cohort was generated to minimize the impact of selection bias and control potential confounding factors. Two similar groups (CI-AKI group and non-CI-AKI group) were constructed. Since there were more patients in the non-CI-AKI group, each patient in the CI-AKI group was matched to three patients in the non-CI-AKI group (1:3 matching). The greedy nearest-neighbor method, with no replacement, was used with a caliper of 0.4 of PS in order to match. Absolute standardized difference (ASD) was used to evaluate the balance of baseline characteristics between the two groups. An ASD of ≤ 0.2 (20%) was regarded as a negligible difference in each covariate between the two groups. When the ASD was greater than 0.15 (15%), the covariate was included in the logistic regression model. The association between FT3 and short-term survival was analyzed by Kaplan–Meier survival analysis and log-rank test. PS-matching analysis was carried out using the statistical package R (the R Foundation; http://www.r-project.org; version 3.4.3).

To maximize the statistical ability and minimize bias that may occur in eliminating missing data in analysis, multivariate multiple imputation with chained equations was used to impute the missing values. Each analysis was repeated in the complete data cohort for comparison.

All statistical tests were two-sided, and P values less than 0.05 were considered to be statistically significant.

Results

Among the 1480 patients enrolled in the study, 224 (15.1%) developed new CI-AKI after CAG or PCI. Among the enrolled patients, 6 (0.4%) had hyperthyroidism, 24 (1.6%) had hypothyroidism, 84 (5.7%) had subclinical hyperthyroidism, and 66 (4.5%) had subclinical hypothyroidism. There were no significant difference in the incidence of thyroid and subclinical thyroid diseases between the CI-AKI group and the non-CI-AKI group (P  > 0.05). Older age and more hypertensive patients were observed in the CI-AKI group than in the non-CI-AKI group (P  < 0.001) (Table 1). More male patients were found in the non-CI-AKI group than in the CI-AKI group (P  < 0.001). There were significant differences in heart rate, left ventricular ejection fraction (LVEF), number of smokers, Killip classification, neutrophil percentage, hemoglobin, serum album, and brain natriuretic peptide between the two groups (P all < 0.05). The FT3 level in the CI-AKI group was lower than that in the non-CI-AKI group (3.72 ± 0.88 pmol/L vs 4.01 ± 0.80, P < 0.001). After matching, variables except for Killip classification and FT3 level presented no significant differences between the two groups.

Table 1

Baseline characteristics before and after matching. Mean ± s.d. or median and 25th and 75th percentiles were used to represent continuous variables. The categorical variable is represented by absolute value (percent).

CharacteristicsBefore matchingAfter matching
No CI-AKI (n  = 1256)CI-AKI (n  = 224)P valueNo CI-AKI (n  = 672)CI-AKI (n  = 224)P value
Age, years66.09 ± 13.7369.58 ± 14.15<0.00169.07 ± 12.9769.58 ± 14.150.62
Male, n (%)912 (72.61%)143 (63.84%)0.008437 (65%)143 (63.84%)0.809
Body mass index, kg/m223.76 ± 3.7823.32 ± 3.770.12623.46 ± 3.7923.32 ± 3.770.766
Hypertension, n (%)819 (65.21%)169 (75.45%)0.003493 (73.4%)169 (75.45%)0.598
Diabetes, n (%)330 (26.27%)68 (30.36%)0.204207 (30.8%)68 (30.36%)0.967
Current or former smoker, n (%)642 (51.11%)94 (41.96%)0.012296 44.0%)94 (41.96%)0.641
Alcohol consumption, n (%)162 (12.90%)19 (8.48%)0.06354 (8.0%)19 (8.48%)0.944
STEMI, n (%)795 (63.30%)138 (61.61%)0.629406 (60.4%)138 (61.61%)0.813
NSTEMI, n (%)461 (36.70%)86 (38.39%)0.629266 (39.6%)86 (38.39%)0.813
LVEF, %49.92 ± 8.9148.31 ± 8.930.01348.45 ± 9.3548.31 ± 8.930.847
Killip class III or IV, n%)108 (8.60%)46 (20.54%)<0.00197 (14.4%)46 (20.54%)0.04
SBP, mmHg132.59 ± 24.67131.28 ± 25.410.465132.59 ± 25.06131.28 ± 25.410.5
DBP, mmHg79.41 ± 16.3978.03 ± 17.330.24879.36 ± 16.6378.03 ± 17.330.305
Heart rate, bpm80.14 ± 16.0484.91 ± 20.43<0.00182.94 ± 16.7584.91 ± 20.430.151
WBC, 109/L8.93 (6.95, 11.47)9.12 (7.22, 11.98)0.2029.80 ± 3.959.92 ± 3.960.708
Neutrophil percentage, %75.30 ± 10.7477.83 ± 10.830.00177.44 ± 10.3477.83 ± 10.830.634
Hemoglobin, g/L134.60 ± 19.46127.46 ± 22.87<0.001129.50 ± 19.80127.46 ± 22.870.199
Serum creatinine, µmol/L78.90 (65.20, 96.62)75.60 (61.32, 103.20)0.4476.40 (62.45, 95.98)75.60 (61.18, 103.60)0.843
Serum albumin, g/L37.90 ± 4.3036.31 ± 5.00<0.00136.71 ± 4.0436.31± 5.000.231
LogBNP2.95 ± 0.753.14 ± 0.820.0013.08 ± 0.763.14 ± 0.820.337
TNI, ng/mL1.85 (0.43, 7.53)1.50 (0.45, 4.70)0.3212.13 (0.50, 8.05)1.52 (0.45, 5.06)0.094
FT3, pmol/L4.01 ± 0.803.72 ± 0.88<0.0013.87 ± 0.813.72 ± 0.880.021
FT4, pmol/L15.43 ± 2.8215.50 ± 2.850.71315.35 ± 2.9515.50 ± 2.850.5
TSH, µIU/mL1.03 (0.60, 1.82)1.13 (0.62, 2.12)0.2191.07 (0.60, 1.81)1.13(0.62, 2,12)0.313

AKI, acute kidney injury; BNP, brain natriuretic peptide; DBP, diastolic blood pressure; FT3, free triiodothyronine; FT4, free thyroxine; LVEF, left ventricular ejection fraction; NSTEMI, non-ST segment elevation myocardial infarction; SBP, systolic blood pressure; STEMI, ST segment elevation myocardial infarction; TNI, cardiac troponin I; TSH, thyroid-stimulating hormone; WBC, white blood cell.

Table 2 shows medications and procedural characteristics in two groups. In the CI-AKI group, more patients used diuretics (P  < 0.05) and fewer received PCI therapy (P  = 0.009). There were significant differences in contrast volume and use of iso-osmolar contrast media (P all < 0.05). After matching, no significant differences in medications and procedural characteristics existed between two groups.

Table 2

Medication and procedural characteristics in relation to CI-AKI before and after matching.

CharacteristicsBefore matchingAfter matching
No CI-AKI (n  = 1256)CI-AKI (n  = 224)P valueNo CI-AKI (n  = 672)CI-AKI (n  = 224)P value
Medication before procedures, n (%)
 Aspirin1217 (96.9%)213 (95.1%)0.168653 (97.2%)213 (95.1%)0.198
 Clopidogrel451 (35.9%)88 (39.3%)0.333235 (35.0%)88 (39.3%)0.278
 Ticagrelor805 (64.1%)136 (60.7%)0.333435 (64.7%)136 (60.7%)0.345
 ACEI/ARB736 (58.6%)137 (61.2%)0.473402 (59.8%)137 (61.2%)0.783
 β-blocker738 (58.8%)144 (64.3%)0.12438 (65.2%)144 (64.3%)0.872
 Statins1127 (89.7%)195 (87.1%)0.232599 (89.1%)195 (87.1%)0.466
 Low molecular heparin1233 (98.2%)216 (96.4%)0.094653 (97.2%)216 (96.4%)0.735
 Tirofiban hydrochloride606 (48.2%)112 (50.00%)0.629331 (49.3%)112 (50.0%)0.908
 Digoxin12 (1.0%)4 (1.79%)0.2857 (1.0%)4 (1.8%)0.599
 Diuretics230 (18.3%)55 (24.6%)0.029153 (22.8%)55 (24.6%)0.648
Procedural characteristics, n (%)
 Contrast volume >100 mL382 (30.4%)98 (43.8%)<0.001251(37.4%)98 (43.8%)0.105
 Contrast exposure time >60 min163 (13.0%)34 (15.2%)0.372100 (14.9%)34 (15.2%)1
 Use of IOCM386 (30.7%)50 (22.3%)0.011169(25.1%)50 (23.3%)0.445
 Hydration therapy291 (23.2%)53 (23.7%)0.872143 (21.3%)53 (23.7%)0.514
 PCI1201 (95.6%)205 (91.5%)0.009629 (93.6%)205 (91.5%)0.362
 Only CAG55 (4.4%)19 (8.5%)0.00943 (6.4%)19 (8.5%)0.362
Number of stents with each vessel
 Left main coronary artery0.0050.093
  01250 (99.5%)218 (97.3%)666 (99.1%)218 (97.3%)
  ≥16 (0.5%)6 (2.7%)6 (0.9%)6 (2.7%)
 Left anterior descending artery0.8320.878
  0630 (50.2%)112 (50.0%)342 (50.9%)112 (50.0%)
  ≥1626 (49.8%)112 (50.0%)330 (49.1%)112 (50.0%)
 Left circumflex artery0.3380.063
  01076 (85.7%)185 (82.6%)590 (87.8%)185 (82.6%)
  ≥1180 (14.3%)39 (17.4%)82 (12.2%)39 (8.5%)
 Right coronary artery0.1580.166
  0866 (69.0%)165 (73.7%)460 (68.5%)165 (73.7%)
  ≥1390 (31.0%)59 (26.3%)212 (31.5%)59 (26.3%)

ACEI/ARB, angiotensin-converting enzyme inhibitors/angiotensin receptor blockers; CAG, coronary angiography; IOCM, iso-osmolar contrast media; PCI, percutaneous coronary intervention.

Table 3 shows the risk of CI-AKI in patients at different quartiles of FT3 level. Three adjusted logistic models were constructed: model 1 adjusted with age and gender; model 2 adjusted with age, gender, and all variables with P < 0.1 before matching in Table 1; model 3 adjusted with all variables in model 2 plus variables with P < 0.1 before matching in Table 2. According to FT3 quartiles, patients were divided into four groups. A lower FT3 level was associated with a higher risk of CI-AKI (ORunadjusted = 0.39, 95% CI: 0.26–0.59 for quartile 4 vs quartile 1, P trend < 0.001; ORmodel 3= 0.51, 95% CI: 0.32–0.81 for quartile 4 vs quartile 1, P trend = 0.005). To be specific, the risk of CI-AKI decreased by 18.9% when FT3 level increased by one s.d. (95%CI: 0.69–0.95, P = 0.011) after multivariable adjustment. Restricted cubic splines showed a similar result. The OR declined dramatically as FT3 rose to 4 pmol/L, but then flattened out (Fig. 2).

Figure 2
Figure 2

Restricted cubic spines analysis of the association of FT3 levels and risk of CI-AKI. X-axis represents plasma FT3 concentrations. Y-axis represents the probability of CI-AKI. Dashed lines indicate 95% CI. From left to right, the triangles indicate the 20th, 40th, 60th, and 80th percentile.

Citation: Endocrine Connections 11, 7; 10.1530/EC-22-0120

Table 3

FT3 level and risk of CI-AKI in entire population. Model 1 adjusted for age and sex; model 2 adjusted for covariates in model 1 plus current or former smoker, alcohol consumption, hypertension, heart rate, neutrophil percentage, hemoglobin, albumin, eGFR, HbA1c, LVEF, LogBNP, and Killip class III or IV; model 3 adjusted for covariates in model 2 plus left main coronary artery, contrast volume >100 mL, use of IOCM, PCI therapy, use of diuretics, and use of low molecular heparin.

FT3 (range)Odds ratio (95% CI) and P value
UnadjustedModel 1Model 2Model 3
FT3 (per 1 s.d.)(1.1–6.8)0.704 (0.611–0.813)0.754 (0.646–0.881)0.807 (0.687–0.947)0.811 (0.689–0.954)
<0.001<0.0010.0090.011
FT3 quartiles
 Q1≤3.51111
ReferenceReferenceReferenceReference
 Q23.5<FT3≤4.00.454 (0.308–0.668)0.488 (0.329–0.723)0.569 (0.377–0.857)0.564 (0.371–0.856)
<0.001<0.0010.0070.007
 Q34.0<FT3≤4.50.484 (0.329–0.713)0.550 (0.367–0.826)0.651(0.426–0.993)0.624 (0.406–0.961)
<0.0010.0040.0460.032
 Q44.5<FT3≤6.80.388 (0.257–0.586)0.458 (0.295–0.710)0.504 (0.319–0.796)0.507 (0.319–0.808)
<0.001<0.0010.0030.004
P for trend<0.001<0.0010.0040.005

eGFR, estimated glomerular filtration rate.

Finally, 672 patients without CI-AKI were PS-matched to 224 patients with CI-AKI. Between-group balance was checked (Fig. 3). After matching, standardized differences of all variables were less than 20%. Tables 1 and 2 show the data characteristics matched between the CI-AKI group and the non-CI-AKI group. Logistic regression analysis was then performed for paired groups. The risk of CI-AKI increased by 17.7% as FT3 level fell by one unit after PS matching (ORadjusted: 0.823, 95% CI: 0.685–0.988, P = 0.036). The lower FT3 level was also associated with the higher risk of CI-AKI in the matched cohort (ORadjusted= 0.618, 95% CI: 0.398–0.959 for quartile 4 vs quartile 1, P < 0.05, Ptrend = 0.025) (Supplementary Table 1, see section on supplementary materials given at the end of this article).

Figure 3
Figure 3

Balance checks of each variable after propensity score matching analysis. Standardized differences of all the variables were illustrated. AKI, acute kidney injury; BNP, brain natriuretic peptide; DBP, diastolic blood pressure; FT3, free triiodothyronine; FT4, free thyroxine; LVEF, left ventricular ejection fraction; NSTEMI, non-ST segment elevation myocardial infarction; SBP, systolic blood pressure; STEMI, ST segment elevation myocardial infarction; TNI, cardiac troponin I; TSH, thyroid-stimulating hormone; WBC, white blood cell.

Citation: Endocrine Connections 11, 7; 10.1530/EC-22-0120

After a median follow-up of 31 days (interquartile range: 30–35 days), 78 (6.93%) patients died, including 72 from cardiogenic and 6 from non-cardiogenic causes. The 78 deaths included 53 in the CI-AKI group and 25 in the non-CI-AKI group (P  < 0.001). Kaplan–Meier survival analysis showed that patients at the lowest FT3 quartile displayed the worst survival than patients at other quantiles before and after matching (Q1 vs Q2 and Q3 and Q4; both P < 0.05; Fig. 4A and C). The prognosis was significantly worse in CI-AKI group than in the non-CI-AKI group (both P < 0.05; Fig. 4B and D).

Figure 4
Figure 4

Survival analyses according to FT3 quartiles and the prevalence of CI-AKI before and after matching. (A) Short-term survival rate according to FT3 quartiles before matching (Q1 vs Q2 and Q3 and Q4); (B) Survival rate between CI-AKI group and non-CI-AKI group before matching; (C) Short-term survival rate according to FT3 quartiles after matching (Q1 vs Q2 and Q3 and Q4); (D) Survival rate between the CI-AKI group and the non-CI-AKI group after matching.

Citation: Endocrine Connections 11, 7; 10.1530/EC-22-0120

Subgroup analysis was performed according to age, gender, eGFR, LVEF, and hypertension. The results are shown in Fig. 5. A high FT3 was further proved to be associated with a reduced risk of CI-AKI in each subgroup.

Figure 5
Figure 5

Subgroup analysis of the association between FT3 and CI-AKI. Odds ratios (OR) with 95% CI of CI-AKI per unit increase of FT3 concentration.

Citation: Endocrine Connections 11, 7; 10.1530/EC-22-0120

Sensitive analysis

As five data sets were generated after multiple imputations, we performed multivariate regression analysis for the other four sets of data sets. In addition, we performed multivariate regression analysis for the entire set (n  = 1480) without adjusting missing variables. The multivariate regression results were affected due to high values of some missing variables. After removing these variables, we re-analyzed the rest cohort (n  = 1256), and the results remained consistent (Supplementary Table 2), confirming that a lower FT3 level was associated with a higher risk of CI-AKI.

Discussion

Our study confirmed that the incidence of AKI was 15.1% in AMI patients, higher than most in previous studies (25, 26). Meanwhile, a study has reported an AKI incidence of 26% in AMI patients (25). This inconsistency may arise from (i) differences in enrolled patients because we enrolled patients with ST segment elevation myocardial infarction and non-ST segment elevation myocardial infarction in our study; (ii) differences in baseline age and renal function of enrolled patients; (iii) differences in diagnostic criteria for AKI; (iv) differences in serum creatinine detection methods.

In this study, we found that low FT3 level was associated with elevated AKI risk and mortality after AMI. The association between FT3 level and prognosis of AMI has also been evaluated in several studies (27, 28, 29). Gulzar et al reported that FT3 level deceased in patients with AMI, and was related to the duration of illness (30). In a prospective cohort study, Yu et al reported that the FT3/FT4 ratio was an independent predictor of 1e year all-cause mortality. The prognostic performance of the FT3/FT4 ratio is similar to that of the GRACE score (31). In another PS-matching study in AMI patients, low FT3 was associated with severe myocardial injury and high mortality. In addition, a combination of FT3 with TIMI risk score is more accurate to predict the risk of cardiovascular death in AMI backyard (9). Moreover, the lower FT3 level is significantly associated with the worse left ventricular mechanics in AMI patients (32).

In this study, we found that the risk of CI-AKI increased by 19.1% for each unit of FT3 decrease in the matched cohort. Survival analysis also showed that patients at a lower FT3 quartile achieved a worse survival rate than those at other quantiles before and after matching. Several biological mechanisms can explain the association between circulating FT3 and CI-AKI in AMI patients. As an adaptive response to acute diseases, the FT3 level drops to reduce catabolism and energy consumption (33). In a pilot study, supplementation of T3 improved cardiac function in AMI patients with LT3S (34).

T3 and T4 are two main iodinated hormones that can regulate the activities of the cardiovascular system. T3 is transformed from T4 but has a higher affinity to thyroid hormone receptors than T4. In our study, we evaluated the clinical value of FTI in predicting the fate of AMI patients. However, the clinical effect and mechanism of T3-based therapy in patients with AMI need to be further studied.

Limitations

This retrospective study is mainly limited by the bias originating from confounding factors related to CI-AKI occurrence in patients with AMI. So, we tried to collect as many as factors which may influence the risk of CI-AKI and conducted logistic regression analysis. Moreover, we conducted PS matching to balance the variables at baseline. After matching, a highly comparable control group was created. Nonetheless, a prospective, multicenter, larger-sample-size and long-term follow-up study is needed to assess the impact of plasma FT3 on CI-AKI and prognosis.

Conclusions

A low FT3 level was associated with an increased risk of CI-AKI and 1-month all-cause mortality in patients with AMI after coronary intervention.

Supplementary materials

This is linked to the online version of the paper at https://doi.org/10.1530/EC-22-0120.

Declaration of interest

The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.

Funding

This study was supported by grants from the National Natural Science Foundation of China (Grant No. 81901410), Young Talent Development Plan of Changzhou Health Commission (CZQM2020060), the Major Research Plan of Changzhou Health Commission (CZQM2020060), the Major Research Plan of Changzhou Health Commission (ZD202020) and Changzhou Sci&Tech Program (Grant No. CJ20210059).

Acknowledgement

The authors thank all local center study personelle for data collection and entry in this study.

References

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    • Export Citation
  • 2

    Abdulaziz Qari F Thyroid hormone profile in patients With acute coronary syndrome. Iranian Red Crescent Medical Journal 2015 17 e26919. (https://doi.org/10.5812/ircmj.26919v2)

    • Search Google Scholar
    • Export Citation
  • 3

    Pingitore A, Nicolini G, Kusmic C, Iervasi G, Grigolini P, Forini F. Cardioprotection and thyroid hormones. Heart Failure Reviews 2016 21 391399. (https://doi.org/10.1007/s10741-016-9545-8)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Gao R, Chen RZ, Xia Y, Liang JH, Wang L, Zhu HY, Zhu Wu J, Fan L, Li JY & Yang T et al.Low T3 syndrome as a predictor of poor prognosis in chronic lymphocytic leukemia. International Journal of Cancer 2018 143 466477. (https://doi.org/10.1002/ijc.31327)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Liu J, Wang D, Xiong Y, Yuan R, Tao W, Liu M. Low free triiodothyronine levels are related to symptomatic intracranial hemorrhage and poor functional outcomes after intravenous thrombolysis in acute ischemic stroke patients. Neurological Research 2016 38 429433. (https://doi.org/10.1080/01616412.2016.1178480)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Kannan L, Shaw PA, Morley MP, Brandimarto J, Fang JC, Sweitzer NK, Cappola TP, Cappola AR. Thyroid dysfunction in heart failure and cardiovascular outcomes. Circulation: Heart Failure 2018 11 e005266. (https://doi.org/10.1161/CIRCHEARTFAILURE.118.005266)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Jabbar A, Pingitore A, Pearce SH, Zaman A, Iervasi G, Razvi S. Thyroid hormones and cardiovascular disease. Nature Reviews: Cardiology 2017 14 3955. (https://doi.org/10.1038/nrcardio.2016.174)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    She J, Feng J, Deng Y, Sun L, Wu Y, Guo M, Liang X, Li J, Xia Y, Yuan Z. Correlation of triiodothyronine level with in-hospital cardiac function and long-term prognosis in patients with acute myocardial infarction. Disease Markers 2018 2018 5236267. (https://doi.org/10.1155/2018/5236267)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Su W, Zhao XQ, Wang M, Chen H, Li HW. Low T3 syndrome improves risk prediction of in-hospital cardiovascular death in patients with acute myocardial infarction. Journal of Cardiology 2018 72 215219. (https://doi.org/10.1016/j.jjcc.2018.02.013)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Chen YY, Shu XR, Su ZZ, Lin RJ, Zhang HF, Yuan WL, Wang JF, Xie SL. A low-normal free triiodothyronine level is associated with adverse prognosis in euthyroid patients with heart failure receiving cardiac resynchronization therapy. International Heart Journal 2017 58 908914. (https://doi.org/10.1536/ihj.16-477)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Iervasi G, Pingitore A, Landi P, Raciti M, Ripoli A, Scarlattini M, L’Abbate A, Donato L. Low-T3 syndrome: a strong prognostic predictor of death in patients with heart disease. Circulation 2003 107 708713. (https://doi.org/10.1161/01.cir.0000048124.64204.3f)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Kaltsas E, Chalikias G, Tziakas D. The incidence and the prognostic impact of acute kidney injury in acute myocardial infarction patients: current preventive strategies. Cardiovascular Drugs and Therapy 2018 32 8198. (https://doi.org/10.1007/s10557-017-6766-6)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Zhou X, Sun Z, Zhuang Y, Jiang J, Liu N, Zang X, Chen X, Li H, Cao H & Sun L et al.Development and validation of nomogram to predict acute kidney injury in patients with acute myocardial infarction treated invasively. Scientific Reports 2018 8 9769. (https://doi.org/10.1038/s41598-018-28088-4)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Sun L, Zhou X, Jiang J, Zang X, Chen X, Li H, Cao H, Wang Q. Growth differentiation factor-15 levels and the risk of contrast induced nephropathy in patients with acute myocardial infarction undergoing percutaneous coronary intervention: a retrospective observation study. PLoS ONE 2018 13 e0197609. (https://doi.org/10.1371/journal.pone.0197609)

    • Search Google Scholar
    • Export Citation
  • 15

    Kuji S, Kosuge M, Kimura K, Nakao K, Ozaki Y, Ako J, Noguchi T, Yasuda S, Suwa S & Fujimoto K et al.Impact of acute kidney injury on in-hospital outcomes of patients with acute myocardial infarction – results from the Japanese registry of acute myocardial infarction diagnosed by universal definition (J-MINUET) substudy. Circulation Journal 2017 81 733739. (https://doi.org/10.1253/circj.CJ-16-1094)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Yang Y, George KC, Luo R, Cheng Y, Shang W, Ge S, Xu G. Contrast-induced acute kidney injury and adverse clinical outcomes risk in acute coronary syndrome patients undergoing percutaneous coronary intervention: a meta-analysis. BMC Nephrology 2018 19 374. (https://doi.org/10.1186/s12882-018-1161-5)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Otsuka K, Shimada K, Katayama H, Nakamura H, Ishikawa H, Takeda H, Fujimoto K, Kasayuki N, Yoshiyama M. Prognostic significance of renal dysfunction and its change pattern on outcomes in patients with acute coronary syndrome treated with emergent percutaneous coronary intervention. Heart and Vessels 2019 34 735744. (https://doi.org/10.1007/s00380-018-1291-5)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Thygesen K, Alpert JS, Jaffe AS, Simoons ML, Chaitman BR & White HD Writing Group on the Joint ESC/ACCF/AHA/WHF Task Force for the Universal Definition of Myocardial Infarction, Thygesen K, Alpert JS, White HD, et al.Third universal definition of myocardial infarction. European Heart Journal 2012 33 25512567. (https://doi.org/10.1093/eurheartj/ehs184)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Lameire N, Kellum JA & KDIGO AKI Guideline Work Group. Contrast-induced acute kidney injury and renal support for acute kidney injury: a KDIGO summary (Part 2). Critical Care 2013 17 205. (https://doi.org/10.1186/cc11455)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Taggart DP, Boyle R, de Belder MA, Fox KA. The 2010 ESC/EACTS guidelines on myocardial revascularisation. Heart 2011 97 445446. (https://doi.org/10.1136/hrt.2010.216135)

  • 21

    Gagandeep K, Kuldeep CM, Bhargava P, Deepak KM, Sharda S & Chaturvedi P. Insignificant correlation between thyroid hormone and antithyroid peroxidase antibodies in Alopecia areata patients in northern Rajasthan. International Journal of Trichology 2017 9 149153. (https://doi.org/10.4103/ijt.ijt_32_17)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Gharib H, Cobin RH, Dickey R. Subclinical hypothyroidism during pregnancy: position statement from the American Association of Clinical Endocrinologists. Endocrine Practice 1999 5 367368.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Kabadi UM ‘Subclinical hypothyroidism’. Natural course of the syndrome during a prolonged follow-up study. Archives of Internal Medicine 1993 153 957961. (https://doi.org/10.1001/archinte.153.8.957)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Stevens LA, Coresh J, Greene T, Levey AS. Assessing kidney function – measured and estimated glomerular filtration rate. New England Journal of Medicine 2006 354 24732483. (https://doi.org/10.1056/NEJMra054415)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Wang C, Pei YY, Ma YH, Ma XL, Liu ZW, Zhu JH, Li CS. Risk factors for acute kidney injury in patients with acute myocardial infarction. Chinese Medical Journal 2019 132 16601665. (https://doi.org/10.1097/CM9.0000000000000293)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Shacham Y, Leshem-Rubinow E, Steinvil A, Assa EB, Keren G, Roth A, Arbel Y. Renal impairment according to acute kidney injury network criteria among ST elevation myocardial infarction patients undergoing primary percutaneous intervention: a retrospective observational study. Clinical Research in Cardiology 2014 103 525532. (https://doi.org/10.1007/s00392-014-0680-8)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Brozaitiene J, Mickuviene N, Podlipskyte A, Burkauskas J, Bunevicius R. Relationship and prognostic importance of thyroid hormone and N-terminal pro-B-type natriuretic peptide for patients after acute coronary syndromes: a longitudinal observational study. BMC Cardiovascular Disorders 2016 16 45. (https://doi.org/10.1186/s12872-016-0226-2)

    • Search Google Scholar
    • Export Citation
  • 28

    Kuchta R, Choudhury A, Scholz T. Asian fish tapeworm: the most successful invasive parasite in freshwaters. Trends in Parasitology 2018 34 511523. (https://doi.org/10.1016/j.pt.2018.03.001)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Iltumur K, Olmez G, Ariturk Z, Taskesen T, Toprak N. Clinical investigation: thyroid function test abnormalities in cardiac arrest associated with acute coronary syndrome. Critical Care 2005 9 R416R424. (https://doi.org/10.1186/cc3727)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Gulzar R, Bukhari MH, Dar R, Sajjad H. Levels of serum thyroxine, triidothyronine and thyrotropin in patients with acute myocardial infarction. Pakistan Journal of Medical Sciences 2018 34 950954. (https://doi.org/10.12669/pjms.344.14705)

    • Search Google Scholar
    • Export Citation
  • 31

    Yu T, Tian C, Song J, He D, Wu J, Wen Z, Sun Z, Sun Z. Value of the fT3/fT4 ratio and its combination with the GRACE risk score in predicting the prognosis in euthyroid patients with acute myocardial infarction undergoing percutaneous coronary intervention: a prospective cohort study. BMC Cardiovascular Disorders 2018 18 181. (https://doi.org/10.1186/s12872-018-0916-z)

    • Search Google Scholar
    • Export Citation
  • 32

    Jankauskiene E, Orda P, Barauskiene G, Mickuviene N, Brozaitiene J, Vaskelyte JJ, Bunevicius R. Relationship between left ventricular mechanics and low free triiodothyronine levels after myocardial infarction: a prospective study. Internal and Emergency Medicine 2016 11 391398. (https://doi.org/10.1007/s11739-015-1370-x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33

    Xu H, Brusselaers N, Lindholm B, Zoccali C, Carrero JJ. Thyroid function test derangements and mortality in dialysis patients: a systematic review and meta-analysis. American Journal of Kidney Diseases 2016 68 923932. (https://doi.org/10.1053/j.ajkd.2016.06.023)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34

    Pingitore A, Mastorci F, Piaggi P, Aquaro GD, Molinaro S, Ravani M, De Caterina A, Trianni G, Ndreu R & Berti S et al.Usefulness of triiodothyronine replacement therapy in patients with ST elevation myocardial infarction and borderline/reduced triiodothyronine levels (from the THIRST Study). American Journal of Cardiology 2019 123 905912. (https://doi.org/10.1016/j.amjcard.2018.12.020)

    • Crossref
    • Search Google Scholar
    • Export Citation

Supplementary Materials

 

     European Society of Endocrinology logo

     Society for Endocrinology logo

  • View in gallery

    Study flow chart. AMI, acute myocardial infarction; CAG, coronary angiography; PCI, percutaneous coronary intervention.

  • View in gallery

    Restricted cubic spines analysis of the association of FT3 levels and risk of CI-AKI. X-axis represents plasma FT3 concentrations. Y-axis represents the probability of CI-AKI. Dashed lines indicate 95% CI. From left to right, the triangles indicate the 20th, 40th, 60th, and 80th percentile.

  • View in gallery

    Balance checks of each variable after propensity score matching analysis. Standardized differences of all the variables were illustrated. AKI, acute kidney injury; BNP, brain natriuretic peptide; DBP, diastolic blood pressure; FT3, free triiodothyronine; FT4, free thyroxine; LVEF, left ventricular ejection fraction; NSTEMI, non-ST segment elevation myocardial infarction; SBP, systolic blood pressure; STEMI, ST segment elevation myocardial infarction; TNI, cardiac troponin I; TSH, thyroid-stimulating hormone; WBC, white blood cell.

  • View in gallery

    Survival analyses according to FT3 quartiles and the prevalence of CI-AKI before and after matching. (A) Short-term survival rate according to FT3 quartiles before matching (Q1 vs Q2 and Q3 and Q4); (B) Survival rate between CI-AKI group and non-CI-AKI group before matching; (C) Short-term survival rate according to FT3 quartiles after matching (Q1 vs Q2 and Q3 and Q4); (D) Survival rate between the CI-AKI group and the non-CI-AKI group after matching.

  • View in gallery

    Subgroup analysis of the association between FT3 and CI-AKI. Odds ratios (OR) with 95% CI of CI-AKI per unit increase of FT3 concentration.

  • 1

    Wiersinga WM, Lie KI, Touber JL. Thyroid hormones in acute myocardial infarction. Clinical Endocrinology 1981 14 367374. (https://doi.org/10.1111/j.1365-2265.1981.tb00622.x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Abdulaziz Qari F Thyroid hormone profile in patients With acute coronary syndrome. Iranian Red Crescent Medical Journal 2015 17 e26919. (https://doi.org/10.5812/ircmj.26919v2)

    • Search Google Scholar
    • Export Citation
  • 3

    Pingitore A, Nicolini G, Kusmic C, Iervasi G, Grigolini P, Forini F. Cardioprotection and thyroid hormones. Heart Failure Reviews 2016 21 391399. (https://doi.org/10.1007/s10741-016-9545-8)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4

    Gao R, Chen RZ, Xia Y, Liang JH, Wang L, Zhu HY, Zhu Wu J, Fan L, Li JY & Yang T et al.Low T3 syndrome as a predictor of poor prognosis in chronic lymphocytic leukemia. International Journal of Cancer 2018 143 466477. (https://doi.org/10.1002/ijc.31327)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5

    Liu J, Wang D, Xiong Y, Yuan R, Tao W, Liu M. Low free triiodothyronine levels are related to symptomatic intracranial hemorrhage and poor functional outcomes after intravenous thrombolysis in acute ischemic stroke patients. Neurological Research 2016 38 429433. (https://doi.org/10.1080/01616412.2016.1178480)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Kannan L, Shaw PA, Morley MP, Brandimarto J, Fang JC, Sweitzer NK, Cappola TP, Cappola AR. Thyroid dysfunction in heart failure and cardiovascular outcomes. Circulation: Heart Failure 2018 11 e005266. (https://doi.org/10.1161/CIRCHEARTFAILURE.118.005266)

    • Search Google Scholar
    • Export Citation
  • 7

    Jabbar A, Pingitore A, Pearce SH, Zaman A, Iervasi G, Razvi S. Thyroid hormones and cardiovascular disease. Nature Reviews: Cardiology 2017 14 3955. (https://doi.org/10.1038/nrcardio.2016.174)

    • Search Google Scholar
    • Export Citation
  • 8

    She J, Feng J, Deng Y, Sun L, Wu Y, Guo M, Liang X, Li J, Xia Y, Yuan Z. Correlation of triiodothyronine level with in-hospital cardiac function and long-term prognosis in patients with acute myocardial infarction. Disease Markers 2018 2018 5236267. (https://doi.org/10.1155/2018/5236267)

    • Search Google Scholar
    • Export Citation
  • 9

    Su W, Zhao XQ, Wang M, Chen H, Li HW. Low T3 syndrome improves risk prediction of in-hospital cardiovascular death in patients with acute myocardial infarction. Journal of Cardiology 2018 72 215219. (https://doi.org/10.1016/j.jjcc.2018.02.013)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Chen YY, Shu XR, Su ZZ, Lin RJ, Zhang HF, Yuan WL, Wang JF, Xie SL. A low-normal free triiodothyronine level is associated with adverse prognosis in euthyroid patients with heart failure receiving cardiac resynchronization therapy. International Heart Journal 2017 58 908914. (https://doi.org/10.1536/ihj.16-477)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Iervasi G, Pingitore A, Landi P, Raciti M, Ripoli A, Scarlattini M, L’Abbate A, Donato L. Low-T3 syndrome: a strong prognostic predictor of death in patients with heart disease. Circulation 2003 107 708713. (https://doi.org/10.1161/01.cir.0000048124.64204.3f)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12

    Kaltsas E, Chalikias G, Tziakas D. The incidence and the prognostic impact of acute kidney injury in acute myocardial infarction patients: current preventive strategies. Cardiovascular Drugs and Therapy 2018 32 8198. (https://doi.org/10.1007/s10557-017-6766-6)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Zhou X, Sun Z, Zhuang Y, Jiang J, Liu N, Zang X, Chen X, Li H, Cao H & Sun L et al.Development and validation of nomogram to predict acute kidney injury in patients with acute myocardial infarction treated invasively. Scientific Reports 2018 8 9769. (https://doi.org/10.1038/s41598-018-28088-4)

    • Search Google Scholar
    • Export Citation
  • 14

    Sun L, Zhou X, Jiang J, Zang X, Chen X, Li H, Cao H, Wang Q. Growth differentiation factor-15 levels and the risk of contrast induced nephropathy in patients with acute myocardial infarction undergoing percutaneous coronary intervention: a retrospective observation study. PLoS ONE 2018 13 e0197609. (https://doi.org/10.1371/journal.pone.0197609)

    • Search Google Scholar
    • Export Citation
  • 15

    Kuji S, Kosuge M, Kimura K, Nakao K, Ozaki Y, Ako J, Noguchi T, Yasuda S, Suwa S & Fujimoto K et al.Impact of acute kidney injury on in-hospital outcomes of patients with acute myocardial infarction – results from the Japanese registry of acute myocardial infarction diagnosed by universal definition (J-MINUET) substudy. Circulation Journal 2017 81 733739. (https://doi.org/10.1253/circj.CJ-16-1094)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Yang Y, George KC, Luo R, Cheng Y, Shang W, Ge S, Xu G. Contrast-induced acute kidney injury and adverse clinical outcomes risk in acute coronary syndrome patients undergoing percutaneous coronary intervention: a meta-analysis. BMC Nephrology 2018 19 374. (https://doi.org/10.1186/s12882-018-1161-5)

    • Search Google Scholar
    • Export Citation
  • 17

    Otsuka K, Shimada K, Katayama H, Nakamura H, Ishikawa H, Takeda H, Fujimoto K, Kasayuki N, Yoshiyama M. Prognostic significance of renal dysfunction and its change pattern on outcomes in patients with acute coronary syndrome treated with emergent percutaneous coronary intervention. Heart and Vessels 2019 34 735744. (https://doi.org/10.1007/s00380-018-1291-5)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Thygesen K, Alpert JS, Jaffe AS, Simoons ML, Chaitman BR & White HD Writing Group on the Joint ESC/ACCF/AHA/WHF Task Force for the Universal Definition of Myocardial Infarction, Thygesen K, Alpert JS, White HD, et al.Third universal definition of myocardial infarction. European Heart Journal 2012 33 25512567. (https://doi.org/10.1093/eurheartj/ehs184)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Lameire N, Kellum JA & KDIGO AKI Guideline Work Group. Contrast-induced acute kidney injury and renal support for acute kidney injury: a KDIGO summary (Part 2). Critical Care 2013 17 205. (https://doi.org/10.1186/cc11455)

    • Search Google Scholar
    • Export Citation
  • 20

    Taggart DP, Boyle R, de Belder MA, Fox KA. The 2010 ESC/EACTS guidelines on myocardial revascularisation. Heart 2011 97 445446. (https://doi.org/10.1136/hrt.2010.216135)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Gagandeep K, Kuldeep CM, Bhargava P, Deepak KM, Sharda S & Chaturvedi P. Insignificant correlation between thyroid hormone and antithyroid peroxidase antibodies in Alopecia areata patients in northern Rajasthan. International Journal of Trichology 2017 9 149153. (https://doi.org/10.4103/ijt.ijt_32_17)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Gharib H, Cobin RH, Dickey R. Subclinical hypothyroidism during pregnancy: position statement from the American Association of Clinical Endocrinologists. Endocrine Practice 1999 5 367368.

    • Search Google Scholar
    • Export Citation
  • 23

    Kabadi UM ‘Subclinical hypothyroidism’. Natural course of the syndrome during a prolonged follow-up study. Archives of Internal Medicine 1993 153 957961. (https://doi.org/10.1001/archinte.153.8.957)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Stevens LA, Coresh J, Greene T, Levey AS. Assessing kidney function – measured and estimated glomerular filtration rate. New England Journal of Medicine 2006 354 24732483. (https://doi.org/10.1056/NEJMra054415)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Wang C, Pei YY, Ma YH, Ma XL, Liu ZW, Zhu JH, Li CS. Risk factors for acute kidney injury in patients with acute myocardial infarction. Chinese Medical Journal 2019 132 16601665. (https://doi.org/10.1097/CM9.0000000000000293)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Shacham Y, Leshem-Rubinow E, Steinvil A, Assa EB, Keren G, Roth A, Arbel Y. Renal impairment according to acute kidney injury network criteria among ST elevation myocardial infarction patients undergoing primary percutaneous intervention: a retrospective observational study. Clinical Research in Cardiology 2014 103 525532. (https://doi.org/10.1007/s00392-014-0680-8)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Brozaitiene J, Mickuviene N, Podlipskyte A, Burkauskas J, Bunevicius R. Relationship and prognostic importance of thyroid hormone and N-terminal pro-B-type natriuretic peptide for patients after acute coronary syndromes: a longitudinal observational study. BMC Cardiovascular Disorders 2016 16 45. (https://doi.org/10.1186/s12872-016-0226-2)

    • Search Google Scholar
    • Export Citation
  • 28

    Kuchta R, Choudhury A, Scholz T. Asian fish tapeworm: the most successful invasive parasite in freshwaters. Trends in Parasitology 2018 34 511523. (https://doi.org/10.1016/j.pt.2018.03.001)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29

    Iltumur K, Olmez G, Ariturk Z, Taskesen T, Toprak N. Clinical investigation: thyroid function test abnormalities in cardiac arrest associated with acute coronary syndrome. Critical Care 2005 9 R416R424. (https://doi.org/10.1186/cc3727)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Gulzar R, Bukhari MH, Dar R, Sajjad H. Levels of serum thyroxine, triidothyronine and thyrotropin in patients with acute myocardial infarction. Pakistan Journal of Medical Sciences 2018 34 950954. (https://doi.org/10.12669/pjms.344.14705)

    • Search Google Scholar
    • Export Citation
  • 31

    Yu T, Tian C, Song J, He D, Wu J, Wen Z, Sun Z, Sun Z. Value of the fT3/fT4 ratio and its combination with the GRACE risk score in predicting the prognosis in euthyroid patients with acute myocardial infarction undergoing percutaneous coronary intervention: a prospective cohort study. BMC Cardiovascular Disorders 2018 18 181. (https://doi.org/10.1186/s12872-018-0916-z)

    • Search Google Scholar
    • Export Citation
  • 32

    Jankauskiene E, Orda P, Barauskiene G, Mickuviene N, Brozaitiene J, Vaskelyte JJ, Bunevicius R. Relationship between left ventricular mechanics and low free triiodothyronine levels after myocardial infarction: a prospective study. Internal and Emergency Medicine 2016 11 391398. (https://doi.org/10.1007/s11739-015-1370-x)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33

    Xu H, Brusselaers N, Lindholm B, Zoccali C, Carrero JJ. Thyroid function test derangements and mortality in dialysis patients: a systematic review and meta-analysis. American Journal of Kidney Diseases 2016 68 923932. (https://doi.org/10.1053/j.ajkd.2016.06.023)

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34

    Pingitore A, Mastorci F, Piaggi P, Aquaro GD, Molinaro S, Ravani M, De Caterina A, Trianni G, Ndreu R & Berti S et al.Usefulness of triiodothyronine replacement therapy in patients with ST elevation myocardial infarction and borderline/reduced triiodothyronine levels (from the THIRST Study). American Journal of Cardiology 2019 123 905912. (https://doi.org/10.1016/j.amjcard.2018.12.020)

    • Crossref
    • Search Google Scholar
    • Export Citation