Recent Minor Ischemic Stroke with an NIHSS Score of 0 in Neurologic Outpatients: Prevalence, Risk Factors and Outcome

Research Article

Austin J Cerebrovasc Dis & Stroke. 2020; 7(1): 1083.

Recent Minor Ischemic Stroke with an NIHSS Score of 0 in Neurologic Outpatients: Prevalence, Risk Factors and Outcome

Tong DM1*, Zhou YT2, Chen XD3, Wang YW1 and Wang Y1

1Department of Neurology, Affiliated Shuyang Hospital, Xuzhou Medical University, Jiangsu, China

2Department of Clinical Research, Affiliated Shuyang Hospital, Xuzhou Medical University, Jiangsu, China

3Department of Neurology, Suqian First Hospital, Jiangsu, China

*Corresponding author: Tong DM, Department of Neurology, Affiliated Shuyang Hospital, Xuzhou Medical University, No. 9, Yingbin Road, Shu town, Jiangsu 223600, China

Received: December 18, 2019; Accepted: January 28, 2020; Published: February 04, 2020


Background: Recent minor ischemic stroke (MIS) with a National Institutes of Health Stroke Scale (NIHSS) score of 0 was previously unstudied. Our aim was to identify the prevalence, outcomes of, and risk factors for recent MIS with an NIHSS score of 0.

Methods: A prospective cohort of neurologic outpatients treated from 2012- 2016 was selected for study. We diagnosed patients with recent MIS using magnetic resonance imaging (MRI) and categorized them based on whether they had NIHSS scores of 0 or 1-3.

Results: Among 3209 patients with minor brain events, 42.8% (1372/3209) had recent MIS verified by MRI. While, 34.3% (1102/3209) had recent MIS with an NIHSS scores of 0, and 8.4% had an NIHSS scores of 1-3. Middle age (Odds ratio [OR], 1.10; 95% confidence interval [CI], 1.05-1.18), nonfocal neurologic symptoms (OR, 0.51; 95% CI, 0.30- 0.67), and increased systolic blood pressure (OR, 1.04; 95% CI, 1.02-1.17) were significantly associated with recent MIS with an NIHSS score of 0. During the 3-month follow-up, recent MIS with an NIHSS score of 0 had more favorable outcomes compared with those with an NIHSS score of 1-3 (Rankin Scale score 0 to 2, 99.6% vs. 71.3%, p< 0.001), but the recurrence events was 22.3% in recent MIS with an NIHSS score of 0 and 28.3% in recent MIS with an NIHSS score of 1-3 (p=0.043).

Conclusions: The disability rate of MIS with an NIHSS score of 0 is very low, but its high prevalent rate and high recurrence events seriously threatens the health of middle-aged.

Keywords: Minor ischemic stroke; Prevalence; risk factors; Outcomes; Magnetic resonance imaging


Since the second half of the twentieth century, the clinicopathologic features of minor ischemic stroke (MIS) have been described in the medical literature [1]. A previous study reported that lacunar infarcts and partial anterior circulation stroke are attributable to MIS [2], but most recent studies have considered small infarcts or small lacunes associated with minor symptoms in patients with very low baseline National Institutes of Health Stroke Scale (NIHSS) scores (≤3) to be mainly ascribed to MIS [3-7]. Deep brain gray and white matter is typically involved, as well as white matter near the cortex. Moreover, MIS is not limited to traditional lacunar infarcts; other stroke subtypes can also be attributed to MIS, including arteriothrombotic, cardioembolic, and non-small vessel disease (non-SVD) due to other etiology [2,5]. Unfortunately, some MIS patients are hospitalized and have a worse prognosis [3,6-9] due to atheromatous stenosis or acute occlusion of larger arteries, such as the basilar or middle cerebral artery. However, the face validity of NIHSS scores of 0-3 in the investigations of patients with recent MIS with an NIHSS score of 0 is not well known. We hypothesized that at the first-ever visit, the presence of symptoms accounting for an NIHSS score of 0 would indicate a health-threatening MIS due to its high prevalent rate and high recurrence events. We tested these hypotheses by conducting a study of neurologic outpatient admissions in Northern China over the past 4 years. The aim of this study was to investigate the prevalence, outcomes of, and risk factors for MIS in patients with an NIHSS score of 0.


Study population

A prospective cohort of consecutive patients was selected for the study between January 2012 and January 2016. All patients were registered neurologic outpatients (including stroke and nonstroke patients) treated at a tertiary teaching hospital; thus, the sample consisted of males and females aged >25 years or older residing in 38 villages or towns and one urban population in Shuyang, Northern China. The inclusion criteria for recent MIS were defined as follows [3,4,7]: (1) First-ever visit indicating recent mild brain symptoms, no positive signs or only minor positive signs, measured as a score of 0-3 on the NIHSS at the time of the initial visit; (2) Magnetic resonance imaging (MRI) study with evidence of recent MIS. We excluded patients with a previous history of stroke, transient ischemic attack (TIA), or peripheral vertigo and patients with ischemic stroke with NIHSS scores >3. The study was approved by the ethical committee on clinical research of the Affiliated Shuyang Hospital of Xuzhou Medical University. Because the study involved only a review of records obtained as a part of routine medical care, did not require all patients to write the information consent.

Image analysis

All patients underwent MRI of the brain within 6 hours of the first visit. MRI was performed with 1.5-T equipment (Siemens), including diffusion-weighted imaging (DWI) or fluid-attenuated inversion recovery (FLAIR) images, T2- and T1-weighted images. For the purposes of this study, the radiographic inclusion criteria for recent MIS were defined as follows: DWI increased signal, reduced signal on apparent diffusion coefficient map (ADC), and as an acute small infarction or lacunar lesion (usually ≤20mm in diameter) located in cerebral cortex, subcortical white matter, basal ganglia, thalamus, brainstem, or cerebellum [10,11].

All MRI studies were reviewed by a neuroradiologist and a neurologist who were blinded to the study. The examiners looked specifically for lesions on DWI, FLAIR/T2, and ADC maps and measured the maximum diameters (in mm). The maximum diameters of the lesions, number of lesions and lesion location on DWI and FLAIR were recorded in detail for each patient.

Clinical assessment

The NIHSS was used to assess the severity of stroke. The NIHSS scores were calculated for all MIS patients and were measured within 1 hour of the time of the initial neurologic outpatient visit. According to the findings of the initial NIHSS score, the study population was divided into two groups: MIS with an NIHSS score of 0 and with NIHSS scores of 1-3.

The following risk factors and symptoms were recorded by an experienced neurologist: gender, age, body mass index (BMI), history of hypertension, diabetes mellitus, or heart disease, alcohol use, smoking, systolic blood pressure (SBP), diastolic blood pressure, headache/migraine, dizziness/vertigo, dizziness with headache, numbness or sensory abnormality, and weakness or motor hemiparesis. The periodic duration of symptoms in all patients was also recorded.

For outcome analyses, the modified Rankin Scale (mRS) scores at 90 days of follow-up were assessed (scores range from 0 to 6; no symptoms=0, slight symptoms=1, restriction=2, slight disability=3, moderate disability=4, severe disability=4-5, death=6). All patients with recurrence events in the first 90 days after initial event were assessed by a neurological specialist. The recurrence events included TIA-like symptoms, nonfocal neurological symptoms, and recurrence stroke. The follow-up information was gathered by a neurological specialist who conducted inquiries by phone (90 days after the initial visit).

Related definitions

A minor brain symptom was defined as a neurological symptom without distinct disability. We define an NIHSS score of 0 according to a total score on NIHSS equal to 0, including from onset to initial visit no focal symptoms and signs rather than asymptomatic MIS. Asymptomatic MIS was defined as a small stroke with high intensity on T2-weighted images without clinical symptoms, which included nonfocal symptoms and focal symptoms.

In the present study, we defined a TIA as an episode of <24 hours of neurologic dysfunction caused by focal brain, spinal cord, or retinal ischemia without new infarction.

We identified these nonlocal neurological symptoms based on the National Institute of Neurological Disorders and Stroke (NINDS) criteria and related documents [12,13]. Transient symptoms with infarction (TSI) indicated transient symptoms associated with abnormal lesions on DWI [14]. Transient nonfocal neurological symptoms indicated an attack with temporary (<24 hours) nonfocal neurological symptoms including TIA-like symptoms or TSI.

Nonfocal neurological symptoms could be attributed to a recent MIS and were based on the following medical documents: dizziness or vertigo is associated with an increased risk of developing vascular events [15]; dizziness is a posterior circulation symptom but is also an anterior circulation symptom [12,14,16] that can be attributed to central causes. Migraine/headache is a common symptom and risk factor for cerebrovascular disease [17]. Other nonfocal neurological syndromes, such as numbness or tingling, slurred speech, dysarthria, and confusion, as well as common focal neurological syndromes, such as motor hemiparesis and hemidysesthesia, were also included in this study.

Statistical analysis

Numeric variables were expressed as the mean ± standard deviation (SD) or median (interquartile range [IQR]). Continuous variables were compared using the t-test. Fisher’s exact test and Mann-Whitney U test were used to explore the relationship among baseline patient variables. Multivariate-adjusted Odds ratios (ORs) and 95% confidence intervals (CIs) were estimated with the use of a logistic regression model if they were significant in the univariate analysis. The disability rate in the first 90 days was also compared between groups. Statistical calculations were performed using SPSS version 17.0 (SPSS Inc., Chicago, IL, USA), with the level of significance set at P<0.005.


Patient population

A total of 3209 patients who presented for an initial visit due to minor brain symptoms were admitted to our neurologic outpatient department between January 1, 2012, and January 1, 2016. We excluded 1015 patients with a final diagnosis of TIA, 410 patients with primary migraine without infarction, 307 patients with peripheral vertigo, 42 patients with cervical vertebral disease, 32 patients with other brain episodes, and 31 patients with infarction and initial NIHSS scores >3. Ultimately, 1372 (42.8%) patients satisfied the inclusion criteria for this validation cohort study. Among them, we diagnosed 1102 (34.3%, 1102/3209) patients with recent MIS with an NIHSS score of 0 events and 270 (8.4%, 270/3209) patients with recent MIS with NIHSS scores of 1-3 events. 70% of MIS patients who had an NIHSS of 0 were received alone antiplatelet treatment at home, rest 30% of these patients with more frequent symptoms were admitted to stroke ward. Yet, most of MIS patients who had an NIHSS of 1-3 were admitted to stroke ward, but no patients received intravenous thrombolysis because this hospital did not implement thrombolytic treatment at that time.

The baseline characteristics of neurologic outpatients with recent MIS are shown in Table 1. The median time from symptom onset to assessment, NIHSS score and MRI was 5 days (range: 0.16-19.8 days). The mean age was 60.7 ±11.3 years. Furthermore, the prevalence of recent MIS increased with younger age, and there were differences among patients with an NIHSS score of 0 compared with those with NIHSS scores of 1-3 (p<0.001). The prevalence peaked in the age group of patients who were 40-59 years and had NIHSS scores of 0, while the incidence peaked in the group of patients with NIHSS scores of 1-3 in the subgroup of patients aged 70-79 years (Figure 1).