Nonocclusive mesenteric ischemia secondary to spinal cord injury: an autopsy case

Abstract

Introduction

Spinal cord injury (SCI) is a major direct cause of accidental death. Cervical SCI can lead to death in a short time period by neurogenic shock. Prompt vasopressor administration is recommended for patients with SCI accompanied by hypotension (systolic blood pressure < 90 mmHg). We herein present the first fatal case of nonocclusive mesenteric ischemia (NOMI) secondary to cervical SCI in a patient who suddenly died 1 week after an accidental fall.

Case presentation

A 72-year-old man without medical history of cardiovascular disease suffered tetraplegia with a neurological level at C4 after a fall accident. He was fully conscious with stable respiratory ability, and the systolic blood pressure was maintained at >90 mmHg without vasopressor agents. High fever occurred 7 days after the accident and he died in the next morning. Autopsy revealed segmental intestinal necrosis from the ileum to the ascending colon, without mesenteric embolism, or severe arteriosclerosis.

Discussion

This case implies that maintenance of >90-mmHg systolic blood pressure can insufficiently keep the blood flow to prevent NOMI, and the mean arterial blood pressure of >85 mmHg can be more plausible as suggested in the guideline. Monitoring the mean arterial blood pressure in acute SCI is useful not only for neurological recovery but also for the maintenance of vital intestinal perfusion.

Introduction

The annual estimated global incidence of traumatic spinal cord injury (SCI) is 20–40/1,000,000 [1]. SCI is a major direct cause of death associated with falls and traffic and sports accidents [2, 3]. Cervical injury above the C4 level can impair respiration because of the paralysis of the phrenic nerve and can be a cause of instant death [4–6]. Moreover, SCI at any level higher than T6 can provoke neurogenic shock and lead to death in a short time period [6–8]. Neurogenic shock is characterized by hypotension, bradycardia, and peripheral vasodilation, which can be particularly severe in patients with cervical injury [7, 9]. Prompt vasopressor administration is recommended for patients with SCI accompanied by hypotension (systolic blood pressure < 90 mmHg) [10, 11].

In this case report, we present a fatal case of nonocclusive mesenteric ischemia (NOMI) secondary to cervical SCI without blood loss in a patient who suddenly died 1 week after an accidental fall. Although a systolic blood pressure of >90 mmHg was maintained without vasopressor treatment, NOMI as a lethal complication of neurogenic shock was identified at autopsy.

Case presentation

Clinical history

A 72-year-old man without medical history of cardiovascular disease accidentally fell from the cliff of 3-m height. The witness immediately called the ambulance, and the patient was transported to the emergency hospital. Although the systolic blood pressure was ~60 mmHg at the scene, it recovered to >120 mmHg upon hospital arrival after the initial infusion of Ringer’s lactate. The peripheral neurological assessment confirmed tetraplegia (AIS-A) with neurological level of C4. Computed tomography indicated a fracture of the C4 spinal process, and magnetic resonance imaging indicated SCI from C4 to C6 (Fig. 1). He was fully conscious with stable respiratory ability, and the paralysis area was unchanged throughout the hospitalization. His clinical data during hospitalization are shown in Fig. 2.

Fig. 1. Axial images of the neck on admission.

a Computed tomography shows fracture of C4 spinal process (yellow arrowhead). b Magnetic resonance imaging shows spinal cord injury from C4 to C6 (yellow arrow bracket).

Fig. 2. Clinical charts during hospitalization.

Blood pressures were measured noninvasively four to six times a day and were averaged in each day. The mean arterial pressure was calculated form the noninvasive blood pressure: diastolic blood pressure +0.412 (systolic blood pressure–diastolic blood pressure) [14].

The patient was initiated on tube feeding with a concentrated fluid diet and on passive exercise for the maintenance of range of motion the day after the accident. He had pain in the neck and shoulders, so took NSAIDs occasionally. The first passage at post-admission was solid feces 3 days at post-accident, and the feces changed to watery on the next day; however, gross hematochezia was not observed. Bowel sounds were normal during the period.

Abdominal distension, which was initially noticed on the fifth night after the accident, progressed the next day, and the patient developed fever, with worsening consciousness on post-accident day 7. Computed tomography demonstrated portal venous gas invasion, intestinal tract dilation with gas, pneumatosis intestinalis, and ascites fluid (Fig. 3). Due to the extremely large affected intestinal area, resection was not performed. Cephem antibiotics were administered after blood and fecal samples were collected for bacterial culture. Anticoagulants and opioids were not administered. The patient died on the morning of post-accident day 8. No bacteria grew from the blood sample culture, and only resident flora grew from the fecal sample culture.

Fig. 3. Computed tomography images of the abdomen.

a Massive gas is observed in the hepatic portal veins (yellow arrowhead). Gastric tube is inserted in the fluid accumulation. b The intestinal tract is dilated with gas. Pneumatosis intestinalis is prominent at the right side of the abdominal cavity (red arrowhead).

Autopsy findings

A forensic autopsy was performed 26 h after death to determine the relationship between trauma and cause of death. The nutritional condition of the body was normal with body mass index of 21.2. He had a healing contused-lacerated wound on the left frontal region, and slight fracture of the left frontal bone without brain contusion. The fourth cervical spine was fractured with SCI: the right funiculus dorsalis at C4 level was mildly damaged and the large part of the parenchyma at C5 level was severely damaged (Fig. 4).

Fig. 4. Morphological changes of the cervical cords.

a The right funiculus dorsalis at C4 level is mildly damaged. b The dorsal region including both funiculus dorsalis at C5 level is severely damaged, and the remaining ventral parenchyma largely shows vacuolar degeneration. Bar is 1 mm. Kluver–Barrera stain.

About 340 ml of purulent ascites fluid was detected. From the ileum to the ascending colon measuring 3.3 m, the intestinal tract was regionally necrotized, and the purulent matter diffusely adhered to the lumen with patchy thickened wall, which was most prominent in the ascending colon (Fig. 5). Pathological changes were scattered discontinuously, and the degradation severity locally varied (Fig. 6). Epithelial sloughing and severe congestion in the submucosa were mainly observed in the jejunum and transverse colon. Transmural necrosis with bleeding and submucosal gas was observed mainly in the caudal ileum. Neutrophil infiltration into the epithelium and focal wall thickness with granulation tissue were detected mainly in the ascending colon. No thrombus or embolus was detected in the superior mesenteric artery, and the systematic atherosclerosis was mild level without obstruction.

Fig. 5. Macroscopic changes of the intestinal tract.

a Necrotic area (arrow) and mild damaged area (arrowhead) are inconsecutively observed in large parts of the small intestine. b The schema of the intestinal tract. Black is the necrotic area, gray is the mild damaged area, and yellow is the intact intestine. c Purulent matter segmentally adhered in the intestinal tract lumen, and the intestinal wall is thickened mainly in the ascending colon. IC junction ileocecal junction.

Fig. 6. Microscopic changes of the intestinal tract.

a Epithelial sloughing and severe congestion in the submucosa are detected in the jejunum. The intestinal wall thickness is relatively maintained without inflammation. b Necrosis and bleeding spread in all layers of the wall, and submucosal gas is prominent in the caudal ileum. c Neutrophil aggregation in the epithelium and focal wall thickness with granulation tissue are observed mainly in the ascending colon. Bar is 200 μm. Elastica–Masson stain.

Discussion

Neurogenic shock accompanied by severe hypotension and bradycardia is frequently observed following the loss of supraspinal control of sympathetic nervous system in patients with cervical or high-thoracic SCI [12]. In cervical SCI, axonal damage within the dorsal aspects of the lateral funiculus, which includes the descending vasomotor pathway, directly contributes to significant cardiovascular dysfunction [13]. The present patient suffered severe cervical SCI, including the dorsal aspects of the lateral funiculus. Although the systolic blood pressure was maintained above 90 mmHg without the need for vasopressor treatment, the patient was clearly at risk for fatal neurogenic shock. The American Association of Neurological Surgeons and the Congress of Neurological Surgeon’s guidelines recommend that a mean arterial blood pressure (MAP) of 85–90 mmHg should be maintained during the first seven days after SCI [10]. In the present case, MAP monitoring with an intra-arterial line was not performed and the MAP, which was determined by noninvasive blood pressure measurement [14], was maintained above 85 mmHg between post-accident day 3 until death.

NOMI is characterized by ischemia, inflammation, and infarction of the intestinal wall. In contrast to acute mesenteric obstruction that occurs following superior mesenteric arterial embolism, NOMI is characterized by patent arteries and veins [15]. The symptoms of NOMI are often insidious and nonspecific at the bed side, resulting in delayed diagnosis with mortality rates of 70–90% [16]. NOMI incidence in the general population is as low as 0.001% [17], which however increases up to 9% after cardiac surgery in elderly patients [18–20]. Moreover, NOMI can sometimes develop in the context of other stressful conditions, such as burn injury [21] and methamphetamine use [22]. The precise mechanism of NOMI remains unclear; however, intestinal hypoperfusion is assumed to arise in the setting of systemic hypotension, mesenteric vasoconstriction, ischemia-reperfusion injury, and supply-demand mismatch, all of which cooperatively lead to NOMI [15, 23, 24]. The entire small intestine and ascending colon are susceptible for NOMI, and intestinal necrosis occurs in a segmental and intermittent manner [25–27]. An early diagnosis of NOMI and emergency excision of the necrotic intestine are necessary for survival.

To date, only one case report of NOMI secondary to SCI has been reported in a patient with moderate blood loss due to gunshot; the patient was rescued by exploratory laparotomy for visceral trauma [28]. An animal study reported that blood flow in the superior mesenteric artery was reduced, with mild intestinal inflammation observed 3 days after SCI at the T3 level [29]. It remains unclear whether mesenteric vasoconstriction, which physiologically occurs to maintain perfusion of vital organs at the expense of mesenteric perfusion during cardiogenic shock [15, 23], is the primary mechanism for NOMI secondary to SCI because visceral sympathetic nervous system is also dysregulated in SCI. However, the clinical history and histological changes in this case confirm the intermittent intestinal ischemia for some days along with systematic hypotension that contribute to the NOMI progression. Some kinds of uncontrolled peripheral vasoconstriction such as localized autonomic dysreflexia possibly promote to the NOMI pathology after SCI [30, 31].

The guideline recommendation about MAP maintenance between 85 and 90 mmHg is widely accepted in the USA [10, 11]; however, no international consensus has been established on the use of arterial lines for the management of acute SCI [32, 33]. The present case implies that maintenance of MAP at >85 mmHg can be a more plausible target than the systolic blood pressure of >90 mmHg to prevent NOMI secondary to SCI. MAP monitoring in acute SCI is useful not only for neurological recovery [34] but also for the maintenance of vital intestinal perfusion.

Compliance with ethical standards

Conflict of interest

The authors declare no competing interests.