Predictive value of serum total bilirubin, neutrophil-to-total bilirubin ratio in evaluating the condition of ulcerative colitis

doi:10.3969/j.issn.1004-583X.2024.07.004

Abstract

Abstract:

Objective To analyze the correlation of serum total bilirubin (TBIL), indirect bilirubin (IBIL), direct bilirubin (DBIL), neutrophil-to- total bilirubin ratio (NBR) with ulcerative colitis (UC) with the severity and lesion range. Methods This was a retrospective case-control study involved 250 active UC patients and 250 healthy participants hospitalized in the First Hospital of Shanxi Medical University from June 2018-June 2023. The clinical data of the patients were collected and NBR was calculated. SPSS 26.0 software was performed to analyze the differences in TBIL, IBIL, DBIL, and NBR between healthy individuals and UC with different severity, lesion scope, and clinical types. Spearson correlation analysis was used to analyze the correlation between the above indicators with hemoglobin (Hb), albumin (ALB), C-reactive protein (CRP), erythrocyte sedimentation rate (ESR), and clinical Mayo scores. The binary logistic regression analysis were performed to assess the odds ratio (OR) values of TBIL, IBIL, DBIL, and NBR with UC, severe UC, and E3 type UC. Finally, the predictive value of the above indicators for UC, severe UC, and E3 type UC was determined by plotting receiver operating characteristic (ROC) curves. Results The serum levels of TBIL, IBIL, and DBIL in UC patients were significantly lower than those in healthy individuals, while the levels of NBR were significantly increased. TBIL and IBIL were significantly reduced in patients with severe UC and E3 type UC, while NBR was significantly increased. There was no significant difference in DBIL among different subgroups. There was no statistically significant difference in various indicators between initial type and chronic recurrent type in UC patients. Correlation analysis showed that TBIL, IBIL were significantly positively correlated with Hb and ALB levels, significantly negatively correlated with ESR, CRP, and modified Mayo scores, but NBR was the opposite. Low levels of TBIL, IBIL and high levels of NBR were risk factors for severe UC and E3 type UC. When TBIL≤8.28 μmol/L, IBIL≤6.48 μmol/L and NBR>7.89, the OR values for severe UC were 4.119, 6.550 and 4.947, respectively, and the OR values for E3 type UC were 2.215, 3.087 and 2.244, respectively. ROC curve showed that TBIL, IBIL and NBR had mild predictive value for severe UC and E3 type UC. Conclusion TBIL, IBIL and NBR are correlated with the severity and lesion range of UC, and there is certain predictive value for severe UC and E3 type UC.

Key words: colitis, ulcerative, bilirubin, neutrophils

CLC Number:

R574.62

Chen Xiaotian, Huo Lijuan. Predictive value of serum total bilirubin, neutrophil-to-total bilirubin ratio in evaluating the condition of ulcerative colitis[J]. Clinical Focus, 2024, 39(7): 603-611.

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URL: https://huicui.hebmu.edu.cn/EN/10.3969/j.issn.1004-583X.2024.07.004

https://huicui.hebmu.edu.cn/EN/Y2024/V39/I7/603

Figures/Tables 14

Tab.1 Clinical data between UC group and healthy control group

组别	例数	年龄 (岁)	性别[例(%)]		TBIL (μmol/L)	IBILC (μmol/L)	DBIL (μmol/L)	NEUT%	NBR
组别	例数	年龄 (岁)	男	女	TBIL (μmol/L)	IBILC (μmol/L)	DBIL (μmol/L)	NEUT%	NBR
UC组	250	47.10±14.57	149(59.6)	101(40.4)	11.53±4.56	9.15±3.87	2.36±1.16	61.82±11.23	5.31±5.42
健康对照组	250	50.00±13.76	155(62.0)	95(38.0)	14.73±4.94	11.99±4.17	2.79±1.76	55.27±8.42	5.13±1.83
统计值		$t$ =1.560	χ²=0.302		$t$ =-7.543	$t$ =-7.899	$t$ =-3.178	$t$ =7.375	$t$ =8.947
P值		0.121	0.583		<0.01	<0.01	0.002	<0.01	<0.001

Tab.1 Clinical data between UC group and healthy control group

组别	例数	年龄 (岁)	性别[例(%)]		TBIL (μmol/L)	IBILC (μmol/L)	DBIL (μmol/L)	NEUT%	NBR
组别	例数	年龄 (岁)	男	女	TBIL (μmol/L)	IBILC (μmol/L)	DBIL (μmol/L)	NEUT%	NBR
UC组	250	47.10±14.57	149(59.6)	101(40.4)	11.53±4.56	9.15±3.87	2.36±1.16	61.82±11.23	5.31±5.42
健康对照组	250	50.00±13.76	155(62.0)	95(38.0)	14.73±4.94	11.99±4.17	2.79±1.76	55.27±8.42	5.13±1.83
统计值		$t$ =1.560	χ²=0.302		$t$ =-7.543	$t$ =-7.899	$t$ =-3.178	$t$ =7.375	$t$ =8.947
P值		0.121	0.583		<0.01	<0.01	0.002	<0.01	<0.001

Tab.2 Clinical parameters in UC with different severity levels, lesion ranges, and clinical types( x -±s)

组别	例数	TBIL(μmol/L)	IBIL(μmol/L)	DBIL(μmol/L)	NEUT%	NBR
轻度	55	13.10±4.50	10.74±3.96	2.34±0.76	57.90±9.87	5.04±2.57
中度	119	11.62±4.51	9.41±3.84	2.22±0.92	61.40±10.59	6.11±2.72
重度	76	10.25±4.34	7.69±3.29	2.60±1.63	65.31±12.16	7.48±3.31
统计值		$F$ =6.570	$F$ =11.998	$F$ =2.606	$F$ =7.475	$F$ =11.839
P值		0.002	<0.01	0.076	0.001	0.001
E1	39	13.09±4.74	10.65±4.27	2.43±0.71	57.84±8.47	5.11±2.33
E2	73	11.87±4.73	9.66±3.99	2.21±0.89	61.60±11.09	6.23±3.39
E3	138	10.91±4.31	8.46±3.54	2.42±1.37	63.06±11.77	6.66±12.88
统计值		$F$ =3.834	$F$ =6.020	$F$ =0.853	$F$ =3.377	$F$ =4.223
P值		0.023	0.003	0.427	0.036	0.016
初发型	67	11.40±5.14	8.97±4.36	2.38±1.20	62.57±11.25	6.51±3.08
慢性复发型	183	11.58±4.34	9.22±3.69	2.36±1.15	61.54±11.23	6.22±2.98
统计值		$F$ =-0.271	$F$ =-0.446	$F$ =0.119	$F$ =0.637	$F$ =0.679
P值		0.787	0.656	0.905	0.525	0.498

Tab.2 Clinical parameters in UC with different severity levels, lesion ranges, and clinical types( x -±s)

组别	例数	TBIL(μmol/L)	IBIL(μmol/L)	DBIL(μmol/L)	NEUT%	NBR
轻度	55	13.10±4.50	10.74±3.96	2.34±0.76	57.90±9.87	5.04±2.57
中度	119	11.62±4.51	9.41±3.84	2.22±0.92	61.40±10.59	6.11±2.72
重度	76	10.25±4.34	7.69±3.29	2.60±1.63	65.31±12.16	7.48±3.31
统计值		$F$ =6.570	$F$ =11.998	$F$ =2.606	$F$ =7.475	$F$ =11.839
P值		0.002	<0.01	0.076	0.001	0.001
E1	39	13.09±4.74	10.65±4.27	2.43±0.71	57.84±8.47	5.11±2.33
E2	73	11.87±4.73	9.66±3.99	2.21±0.89	61.60±11.09	6.23±3.39
E3	138	10.91±4.31	8.46±3.54	2.42±1.37	63.06±11.77	6.66±12.88
统计值		$F$ =3.834	$F$ =6.020	$F$ =0.853	$F$ =3.377	$F$ =4.223
P值		0.023	0.003	0.427	0.036	0.016
初发型	67	11.40±5.14	8.97±4.36	2.38±1.20	62.57±11.25	6.51±3.08
慢性复发型	183	11.58±4.34	9.22±3.69	2.36±1.15	61.54±11.23	6.22±2.98
统计值		$F$ =-0.271	$F$ =-0.446	$F$ =0.119	$F$ =0.637	$F$ =0.679
P值		0.787	0.656	0.905	0.525	0.498

Tab.3 Commonly used indicators among patients with UC of different severity levels( x -±s)

组别	例数	Hb(g/L)	ALB(g/L)	ESR(mm/h)	CRP(mg/L)	改良Mayo评分(分)
轻度	55	130.96±10.93	39.81±4.52	12.67±16.10	9.83±21.67	4.96±1.39
中度	119	125.08±22.55	37.79±4.65	22.69±20.91	21.23±33.26	7.90±1.33
重度	76	105.45±31.31	31.34±6.53	42.41±31.64	46.08±41.61	10.46±1.23
统计值		$F$ =20.231	$F$ =50.610	$F$ =27.638	$F$ =20.628	$F$ =280.936
P值		<0.01	<0.01	<0.01	<0.01	<0.01

Tab.3 Commonly used indicators among patients with UC of different severity levels( x -±s)

组别	例数	Hb(g/L)	ALB(g/L)	ESR(mm/h)	CRP(mg/L)	改良Mayo评分(分)
轻度	55	130.96±10.93	39.81±4.52	12.67±16.10	9.83±21.67	4.96±1.39
中度	119	125.08±22.55	37.79±4.65	22.69±20.91	21.23±33.26	7.90±1.33
重度	76	105.45±31.31	31.34±6.53	42.41±31.64	46.08±41.61	10.46±1.23
统计值		$F$ =20.231	$F$ =50.610	$F$ =27.638	$F$ =20.628	$F$ =280.936
P值		<0.01	<0.01	<0.01	<0.01	<0.01

Tab.4 Correlation between TBIL, IBIL and NBR with the above indicators

因变量	TBIL		IBIL		NEUT%		NBR
因变量	$r$ 值	P值	$r$ 值	P值	$r$ 值	P值	$r$ 值	P值
Hb	0.368	<0.01	0.424	<0.01	-0.105	0.097	-0.337	<0.01
ALB	0.303	<0.01	0.386	<0.01	-0.263	<0.01	-0.406	<0.01
ESR	-0.202	<0.01	-0.314	<0.01	0.271	<0.01	0.358	<0.01
CRP	-0.275	<0.01	-0.313	<0.01	0.402	<0.01	0.430	<0.01
改良Mayo评分	-0.277	<0.01	-0.342	<0.01	0.196	<0.01	0.301	<0.01

Tab.4 Correlation between TBIL, IBIL and NBR with the above indicators

因变量	TBIL		IBIL		NEUT%		NBR
因变量	$r$ 值	P值	$r$ 值	P值	$r$ 值	P值	$r$ 值	P值
Hb	0.368	<0.01	0.424	<0.01	-0.105	0.097	-0.337	<0.01
ALB	0.303	<0.01	0.386	<0.01	-0.263	<0.01	-0.406	<0.01
ESR	-0.202	<0.01	-0.314	<0.01	0.271	<0.01	0.358	<0.01
CRP	-0.275	<0.01	-0.313	<0.01	0.402	<0.01	0.430	<0.01
改良Mayo评分	-0.277	<0.01	-0.342	<0.01	0.196	<0.01	0.301	<0.01

Tab.5 Binary logistic regression analysis for UC risk factors

因素	回归系数	标准误	Wald χ²值	P值	$O R$ 值	95% $C I$
因素	回归系数	标准误	Wald χ²值	P值	$O R$ 值	下限	上限
TBIL	-0.146	0.022	45.706	<0.01	0.0864	0.828	0.901
IBIL	-0.182	0.026	49.075	<0.01	0.833	0.792	0.877
DBIL	-0.273	0.084	10.446	0.001	0.761	0.645	0.898
NEUT%	0.066	0.010	44.921	<0.01	1.069	1.048	1.090
NBR	0.385	0.046	70.251	<0.01	1.469	1.343	1.608

Tab.5 Binary logistic regression analysis for UC risk factors

因素	回归系数	标准误	Wald χ²值	P值	$O R$ 值	95% $C I$
因素	回归系数	标准误	Wald χ²值	P值	$O R$ 值	下限	上限
TBIL	-0.146	0.022	45.706	<0.01	0.0864	0.828	0.901
IBIL	-0.182	0.026	49.075	<0.01	0.833	0.792	0.877
DBIL	-0.273	0.084	10.446	0.001	0.761	0.645	0.898
NEUT%	0.066	0.010	44.921	<0.01	1.069	1.048	1.090
NBR	0.385	0.046	70.251	<0.01	1.469	1.343	1.608

Tab.6 Correlation between TBIL, IBIL, DBIL and NEUT% with NBR levels with UC risk

参数	组别	校正后 $O R$ 值	95% $C I$		P值
参数	组别	校正后 $O R$ 值	下限	上限	P值
TBIL(μmol/L)	≤9.50	5.274	2.911	9.552	0.000
	9.51~12.30	2.451	1.430	4.203	0.001
	12.31~16.20	0.978	0.556	1.719	0.978
	>16.20	参考			-
IBIL(μmol/L)	≤7.53	6.169	3.365	11.310	0.000
	7.54~9.9	2.123	1.242	3.627	0.006
	9.91~12.90	1.068	0.610	1.872	0.817
	>12.90	参考			-
DBIL(μmol/L)	≤1.70	2.581	1.476	4.516	0.001
	1.71~2.30	1.748	1.027	2.974	0.040
	2.31~3.0	0.945	0.540	1.656	0.845
	>3.0	参考			-
NEUT%	≤51.03	参考			-
	51.04~57.55	1.055	0.610	1.826	0.847
	57.56~66.08	1.888	1.096	3.251	0.022
	>66.08	4.872	2.720	8.728	0.000
NBR	≤4.22	参考			-
	4.23~5.65	2.183	1.239	3.847	0.007
	5.66~7.83	2.672	1.526	4.680	0.001
	>7.83	14.928	7.582	29.390	0.000

Tab.6 Correlation between TBIL, IBIL, DBIL and NEUT% with NBR levels with UC risk

参数	组别	校正后 $O R$ 值	95% $C I$		P值
参数	组别	校正后 $O R$ 值	下限	上限	P值
TBIL(μmol/L)	≤9.50	5.274	2.911	9.552	0.000
	9.51~12.30	2.451	1.430	4.203	0.001
	12.31~16.20	0.978	0.556	1.719	0.978
	>16.20	参考			-
IBIL(μmol/L)	≤7.53	6.169	3.365	11.310	0.000
	7.54~9.9	2.123	1.242	3.627	0.006
	9.91~12.90	1.068	0.610	1.872	0.817
	>12.90	参考			-
DBIL(μmol/L)	≤1.70	2.581	1.476	4.516	0.001
	1.71~2.30	1.748	1.027	2.974	0.040
	2.31~3.0	0.945	0.540	1.656	0.845
	>3.0	参考			-
NEUT%	≤51.03	参考			-
	51.04~57.55	1.055	0.610	1.826	0.847
	57.56~66.08	1.888	1.096	3.251	0.022
	>66.08	4.872	2.720	8.728	0.000
NBR	≤4.22	参考			-
	4.23~5.65	2.183	1.239	3.847	0.007
	5.66~7.83	2.672	1.526	4.680	0.001
	>7.83	14.928	7.582	29.390	0.000

Tab.7 Binary logistic regression analysis of TBIL, IBIL, NEUT% and NBR with the risk of severe UC and E3 type UC

	因素	回归系数	标准误	Wald χ²值	P值	$O R$ 值	95% $C I$
	因素	回归系数	标准误	Wald χ²值	P值	$O R$ 值	下限	上限
重度UC	TBIL	-0.100	0.035	8.272	0.004	0.905	0.845	0.969
	IBIL	-0.184	0.046	16.289	<0.01	0.832	0.761	0.910
	NEUT%	0.042	0.013	10.157	0.001	1.042	1.016	1.069
	NBR	0.188	0.049	14.866	<0.01	1.207	1.097	1.329
E3型UC	TBIL	-0.068	0.029	5.556	0.018	0.934	0.883	0.989
	IBIL	-0.107	0.035	9.494	0.002	0.898	0.839	0.962
	NEUT%	0.022	0.012	3.742	0.053	1.023	1.000	1.046
	NBR	0.098	0.046	4.559	0.033	1.103	1.008	1.207

Tab.7 Binary logistic regression analysis of TBIL, IBIL, NEUT% and NBR with the risk of severe UC and E3 type UC

	因素	回归系数	标准误	Wald χ²值	P值	$O R$ 值	95% $C I$
	因素	回归系数	标准误	Wald χ²值	P值	$O R$ 值	下限	上限
重度UC	TBIL	-0.100	0.035	8.272	0.004	0.905	0.845	0.969
	IBIL	-0.184	0.046	16.289	<0.01	0.832	0.761	0.910
	NEUT%	0.042	0.013	10.157	0.001	1.042	1.016	1.069
	NBR	0.188	0.049	14.866	<0.01	1.207	1.097	1.329
E3型UC	TBIL	-0.068	0.029	5.556	0.018	0.934	0.883	0.989
	IBIL	-0.107	0.035	9.494	0.002	0.898	0.839	0.962
	NEUT%	0.022	0.012	3.742	0.053	1.023	1.000	1.046
	NBR	0.098	0.046	4.559	0.033	1.103	1.008	1.207

Tab.8 Correlation between TBIL, IBIL, NEUT% and NBR with the risk of severe UC and E3 type UC

	组别	重度				E3
		校正后OR	95% $C I$		P值	校正后OR	95% $C I$		P值
		校正后OR	下限	上限	P值	校正后OR	下限	上限	P值
TBIL(μmol/L)	≤8.28	4.119	1.747	9.712	0.001	2.215	1.045	4.695	0.038
	8.29~10.70	2.163	0.924	5.062	0.075	2.329	1.120	4.844	0.024
	10.71~13.73	1.669	0.679	4.103	0.264	1.265	0.603	2.654	0.534
	>13.73	参考			-	-			-
IBIL(μmol/L)	≤6.48	6.550	2.636	16.274	0.000	3.087	1.437	6.633	0.004
	6.49~8.45	2.781	1.108	6.979	0.029	2.910	1.370	6.183	0.005
	8.46~11.20	2.198	0.852	5.672	0.104	1.527	0.729	3.196	0.262
	>11.20	参考			-	-			-
NEUT%	≤54.30	参考			-	-			-
	54.31~62.30	0.835	0.343	2.030	0.690	-			-
	62.31~69.28	1.496	0.650	3.444	0.344	-			-
	>69.28	2.863	1.255	6.534	0.012	-			-
NBR	≤4.22	参考			-	-			-
	4.23~5.60	1.961	0.786	4.888	0.149	1.259	0.611	2.594	0.149
	5.61~7.89	2.679	1.099	6.528	0.030	1.969	0.947	4.093	0.030
	>7.89	4.947	2.060	11.876	0.000	2.244	1.056	4.766	0.000

Tab.8 Correlation between TBIL, IBIL, NEUT% and NBR with the risk of severe UC and E3 type UC

	组别	重度				E3
		校正后OR	95% $C I$		P值	校正后OR	95% $C I$		P值
		校正后OR	下限	上限	P值	校正后OR	下限	上限	P值
TBIL(μmol/L)	≤8.28	4.119	1.747	9.712	0.001	2.215	1.045	4.695	0.038
	8.29~10.70	2.163	0.924	5.062	0.075	2.329	1.120	4.844	0.024
	10.71~13.73	1.669	0.679	4.103	0.264	1.265	0.603	2.654	0.534
	>13.73	参考			-	-			-
IBIL(μmol/L)	≤6.48	6.550	2.636	16.274	0.000	3.087	1.437	6.633	0.004
	6.49~8.45	2.781	1.108	6.979	0.029	2.910	1.370	6.183	0.005
	8.46~11.20	2.198	0.852	5.672	0.104	1.527	0.729	3.196	0.262
	>11.20	参考			-	-			-
NEUT%	≤54.30	参考			-	-			-
	54.31~62.30	0.835	0.343	2.030	0.690	-			-
	62.31~69.28	1.496	0.650	3.444	0.344	-			-
	>69.28	2.863	1.255	6.534	0.012	-			-
NBR	≤4.22	参考			-	-			-
	4.23~5.60	1.961	0.786	4.888	0.149	1.259	0.611	2.594	0.149
	5.61~7.89	2.679	1.099	6.528	0.030	1.969	0.947	4.093	0.030
	>7.89	4.947	2.060	11.876	0.000	2.244	1.056	4.766	0.000

Fig.1 ROC curves of TBIL, IBIL, DBIL, NEUT% and NBR for predicting UC value

Tab.9 Predictive value of TBIL, IBIL, DBIL, NEUT% and NBR for UC

指标	AUC	标准误	P值	95% $C I$		敏感度	特异度	约登指数	界值
指标	AUC	标准误	P值	下限	上限	敏感度	特异度	约登指数	界值
TBIL	0.700	0.023	<0.01	0.654	0.746	0.648	0.688	0.336	12.05
IBIL	0.707	0.023	<0.01	0.662	0.752	0.628	0.708	0.336	9.65
DBIL	0.619	0.025	<0.01	0.570	0.669	0.584	0.628	0.212	2.25
NEUT%	0.681	0.024	<0.01	0.634	0.728	0.532	0.784	0.316	61.8
NBR	0.744	0.022	<0.01	0.701	0.787	0.496	0.896	0.392	7.28

Tab.9 Predictive value of TBIL, IBIL, DBIL, NEUT% and NBR for UC

指标	AUC	标准误	P值	95% $C I$		敏感度	特异度	约登指数	界值
指标	AUC	标准误	P值	下限	上限	敏感度	特异度	约登指数	界值
TBIL	0.700	0.023	<0.01	0.654	0.746	0.648	0.688	0.336	12.05
IBIL	0.707	0.023	<0.01	0.662	0.752	0.628	0.708	0.336	9.65
DBIL	0.619	0.025	<0.01	0.570	0.669	0.584	0.628	0.212	2.25
NEUT%	0.681	0.024	<0.01	0.634	0.728	0.532	0.784	0.316	61.8
NBR	0.744	0.022	<0.01	0.701	0.787	0.496	0.896	0.392	7.28

Fig.2 ROC curves of TBIL, IBIL, NEUT% and NBR for the predictive value of severe UC

Tab.10 Predictive value of TBIL, IBIL, NEUT% and NBR for severe UC

指标	AUC	标准误	P值	95% $C I$		敏感度	特异度	约登指数	界值
指标	AUC	标准误	P值	下限	上限	敏感度	特异度	约登指数	界值
TBIL	0.632	0.029	0.001	0.555	0.709	0.592	0.632	0.224	10.05
IBIL	0.680	0.037	<0.001	0.608	0.753	0.671	0.621	0.292	8.15
NEUT%	0.634	0.040	0.001	0.555	0.712	0.737	0.511	0.248	60.45
NBR	0.668	0.038	<0.001	0.594	0.741	0.763	0.511	0.275	5.15

Tab.10 Predictive value of TBIL, IBIL, NEUT% and NBR for severe UC

指标	AUC	标准误	P值	95% $C I$		敏感度	特异度	约登指数	界值
指标	AUC	标准误	P值	下限	上限	敏感度	特异度	约登指数	界值
TBIL	0.632	0.029	0.001	0.555	0.709	0.592	0.632	0.224	10.05
IBIL	0.680	0.037	<0.001	0.608	0.753	0.671	0.621	0.292	8.15
NEUT%	0.634	0.040	0.001	0.555	0.712	0.737	0.511	0.248	60.45
NBR	0.668	0.038	<0.001	0.594	0.741	0.763	0.511	0.275	5.15

Fig.3 ROC curves of TBIL, IBIL and NBR for the predictive value of E3 type UC

Tab.11 Predictive value of TBIL, IBIL and NBR for E3 type UC

指标	AUC	标准误	P值	95% $C I$		敏感度	特异度	约登指数	界值
指标	AUC	标准误	P值	下限	上限	敏感度	特异度	约登指数	界值
TBIL	0.593	0.036	0.011	0.523	0.664	0.565	0.643	0.208	10.35
IBIL	0.617	0.036	0.002	0.547	0.687	0.580	0.652	0.231	8.25
NBR	0.608	0.036	0.003	0.538	0.679	0.652	0.563	0.215	5.21

Tab.11 Predictive value of TBIL, IBIL and NBR for E3 type UC

指标	AUC	标准误	P值	95% $C I$		敏感度	特异度	约登指数	界值
指标	AUC	标准误	P值	下限	上限	敏感度	特异度	约登指数	界值
TBIL	0.593	0.036	0.011	0.523	0.664	0.565	0.643	0.208	10.35
IBIL	0.617	0.036	0.002	0.547	0.687	0.580	0.652	0.231	8.25
NBR	0.608	0.036	0.003	0.538	0.679	0.652	0.563	0.215	5.21

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