Imaging characteristics of brain microstructure and cerebral perfusion in Crohn’s disease patients with anxiety: A prospective comparative study

Table 1 Demographic and clinical characteristics of the participants

Variable	CD with anxiety (n = 16)	CD without anxiety (n = 21)	Healthy controls (n = 20)	P value
Demographic
Age (years)	37.44 ± 7.89	36.24 ± 9.26	35.75 ± 9.06	0.8461
Sex (n, male/female)	7/9	12/9	10/10	0.7182
Education (years)	15 (12,16)	12 (9,15)	12.00 ± 4.03	0.1713
Height (m)	1.65 ± 0.87	1.72 (1.58,1.75)	1.65 ± 0.09	0.3583
Weight (kg)	59.08 ± 10.92	60.14 ± 12.22	55 (50.25,71.5)	0.8573
Clinical characteristics
HADS-A score	13.88 ± 3.86	2.95 ± 1.26	3.26 ± 1.66	< 0.0011,a
SES-CD	13.82 ± 2.73	5.71 ± 1.97	-	< 0.0014,a
WBC, 109/L	11.39 ± 2.62	6.06 ± 1.48	-	< 0.0014,a
Hemoglobin, g/L	136.69 ± 18.86	131 (122.5,140)	-	0.6423
ESR, mm/hour	29.10 ± 18.21	25.88 ± 17.59		0.5924
CRP (mg/dL)	11.78 ± 5.81	5.9 (5,10.18)		0.0593
Duration of disease (years)	3.36 ± 1.59	2.10 ± 0.57		0.465

¹One-way analysis of variance.

²χ² test.

³Non-parametric test.

⁴Independent sample t-test.

^aP < 0.05.

CD: Crohn’s disease; HADS-A: Hospital Anxiety and Depression Scale – Anxiety dimension; SES-CD: Simplified endoscopic score for Crohn’s disease; WBC: White blood cells; ESR: Erythrocyte sedimentation rate; CRP: C-reactive protein level.

Table 2 Slow apparent diffusion coefficient values in the participants

Brain ROI	ADCslow value (10-3 mm2/second)			P value1
	CD with anxiety (n = 16)	CD without anxiety (n = 21)	Healthy controls (n = 20)
Left frontal lobe	0.876 ± 0.071	0.871 ± 0.028	0.820 ± 0.014	< 0.001a
Left parietal lobe	0.819 ± 0.084	0.827 ± 0.010	0.753 ± 0.065	0.128
Left temporal lobe	0.703 ± 0.038	0.716 ± 0.034	0.648 ± 0.028	< 0.001a
Left occipital lobe	0.656 ± 0.044	0.711 ± 0.026	0.645 ± 0.069	0.052
Left insular lobe	0.743 ± 0.050	0.682 ± 0.025	0.656 ± 0.029	< 0.001a
Right frontal lobe	0.872 ± 0.068	0.852 ± 0.017	0.821 ± 0.028	0.001a
Right parietal lobe	0.818 ± 0.084	0.828 ± 0.011	0.754 ± 0.058	0.142
Right temporal lobe	0.664 ± 0.038	0.671 ± 0.023	0.629 ± 0.044	0.001a
Right occipital lobe	0.684 ± 0.054	0.694 ± 0.047	0.676 ± 0.059	0.193
Right insular lobe	0.758 ± 0.061	0.687 ± 0.024	0.658 ± 0.056	< 0.001a

¹One-way analysis of variance.

^aP < 0.05.

ADC_slow: Slow apparent diffusion coefficient; ROI: Region of interest; CD: Crohn’s disease.

Table 3 Fast apparent diffusion coefficient values in the participants

Brain ROI	ADCfast Value (10-2 mm2/second)			P value1
	CD with anxiety (n = 16)	CD without anxiety (n = 21)	Healthy controls (n = 20)
Left frontal lobe	0.183 ± 0.017	0.171 ± 0.083	0.150 ± 0.025	< 0.001a
Left parietal lobe	0.189 ± 0.031	0.181 ± 0.027	0.216 ± 0.010	0.372
Left temporal lobe	0.186 ± 0.035	0.176 ± 0.085	0.153 ± 0.013	< 0.001a
Left occipital lobe	0.159 ± 0.019	0.169 ± 0.017	0.186 ± 0.033	0.437
Left insular lobe	0.198 ± 0.013	0.181 ± 0.011	0.153 ± 0.024	< 0.001a
Right frontal lobe	0.183 ± 0.017	0.181 ± 0.019	0.164 ± 0.011	0.001a
Right parietal lobe	0.184 ± 0.036	0.193 ± 0.024	0.254 ± 0.017	0.142
Right temporal lobe	0.197 ± 0.033	0.182 ± 0.015	0.164 ± 0.019	< 0.001a
Right occipital lobe	0.159 ± 0.019	0.169 ± 0.017	0.163 ± 0.019	0.437
Right insular lobe	0.122 ± 0.014	0.154 ± 0.019	0.178 ± 0.027	< 0.001a

¹One-way analysis of variance.

^aP < 0.05.

ADC_fast: Fast apparent diffusion coefficient; ROI: Region of interest; CD: Crohn’s disease.

Table 4 Perfusion fraction values in the participants

Brain ROI	f value			P value1
	CD with anxiety (n = 16)	CD without anxiety (n = 21)	Healthy controls (n = 20)
Left frontal lobe	0.136 ± 0.026	0.140 ± 0.023	0.140 ± 0.017	0.116
Left parietal lobe	0.120 ± 0.021	0.113 ± 0.018	0.124 ± 0.021	0.614
Left temporal lobe	0.113 ± 0.021	0.104 ± 0.013	0.097 ± 0.011	0.190
Left occipital lobe	0.111 ± 0.038	0.101 ± 0.026	0.097 ± 0.021	0.517
Left insular lobe	0.110 ± 0.021	0.106 ± 0.027	0.092 ± 0.017	0.160
Right frontal lobe	0.142 ± 0.033	0.131 ± 0.014	0.122 ± 0.015	0.148
Right parietal lobe	0.113 ± 0.033	0.106 ± 0.019	0.101 ± 0.020	0.548
Right temporal lobe	0.099 ± 0.024	0.101 ± 0.012	0.096 ± 0.034	0.782
Right occipital lobe	0.102 ± 0.036	0.094 ± 0.018	0.094 ± 0.024	0.719
Right insular lobe	0.109 ± 0.037	0.111 ± 0.028	0.088 ± 0.024	0.267

¹One-way analysis of variance.

f: Perfusion fraction; ROI: Region of interest; CD: Crohn’s disease.

Table 5 Brain regions with significant differences in diffusion kurtosis imaging parameters between the Crohn’s disease and healthy control groups

Indexes	Brain regions	AAL	MNI coordinates			P value
			X	Y	Z
AK	Right insula	30	46	2	-4	0.019a
	Left superior temporal	82	64	20	12	0.002a
	Right thalamus	78	0	2	22	0.001a
	Right insula	30	32	0	-8	0.023a
	Left superior temporal	82	56	0	-2	0.015b
	Right thalamus	78	8	28	0	0.031b
	Left medial temporal	85	56	4	-26	0.006b
	Right inferior temporal	90	44	10	44	0.001b
	Left lingual gyrus	47	28	80	-16	0.007b
	Right insula	30	42	0	8	0.002c
	Right anterior cuneate lobe	68	8	52	6	0.017c
RK	Right cerebellar region 6	100	4	32	40	0.021a
	Right cerebellar region 6	100	4	0	4	0.012b
	Left hippocampus	37	14	6	-14	0.004b

^aP < 0.05 for the Crohn’s disease (CD) without anxiety group vs the healthy control group.

^bP < 0.05 for the CD with anxiety group vs the healthy control group.

^cP < 0.05 for the CD with anxiety group vs the CD without anxiety group.

CD: Crohn’s disease; AAL: Automatic anatomical marking; MNI: Montreal Neurological Institute; AK: Axial diffusion kurtosis; RK: Radial diffusion kurtosis.