Effects of exoskeleton-assisted walking on bowel function in motor-complete spinal cord injury patients: involvement of the brain-gut axis, a pilot study

Abstract

Evidence has demonstrated that exoskeleton robots can improve intestinal function in patients with spinal cord injury (SCI). However, the underlying mechanisms remain unelucidated. This study investigated the effects of exoskeleton-assisted walking (EAW) on intestinal function and intestinal flora structure in T2-L1 motor complete paraplegia patients. The results showed that five participants in the EAW group and three in the conventional group reported improvements in at least one bowel management index, including an increased frequency of bowel evacuations, less time spent on bowel management per day, and less external assistance (manual digital stimulation, medication, and enema usage). After 8 weeks of training, the amount of glycerol used in the EAW group decreased significantly (p <0.05). The EAW group showed an increasing trend in the neurogenic bowel dysfunction (NBD) score after 8 weeks of training, while the conventional group showed a worsening trend. Patients who received the EAW intervention exhibited a decreased abundance of Bacteroidetes and Verrucomicrobia, while Firmicutes, Proteobacteria, and Actinobacteria were upregulated. In addition, there were decreases in the abundances of Bacteroides, Prevotella, Parabacteroides, Akkermansia, Blautia, Ruminococcus 2, and Megamonas. In contrast, Ruminococcus 1, Ruminococcaceae UCG002, Faecalibacterium, Dialister, Ralstonia, Escherichia-Shigella, and Bifidobacterium showed upregulation among the top 15 genera. The abundance of Ralstonia was significantly higher in the EAW group than in the conventional group, and Dialister increased significantly in EAW individuals at 8 weeks. This study suggests that EAW can improve intestinal function of SCI patients in a limited way, and may be associated with changes in the abundance of intestinal flora, especially an increase in beneficial bacteria. In the future, we need to further understand the changes in microbial groups caused by EAW training and all related impact mechanisms, especially intestinal flora metabolites. Clinical trial registration: https://www.chictr.org.cn/.

Keywords: bowel function; constipation; exoskeleton; gut microbiota; spinal cord injury.

Figure 1

AIDER powered robotic exoskeleton (Buffalo Robot Technology Co. Ltd., Chengdu, China).

Figure 2

CONSORT diagram of enrolment of the study participants.

Figure 3

Results of the two groups at baseline. (A) Results pertaining age; (B) results pertaining weight; (C) results pertaining height; independent samples t-test; (D) results pertaining DOI; Wilcoxon Mann–Whitney U rank sum test; (E) results pertaining LOI; (F) results pertaining AIS grade; Fisher’s precision probability test; ^*p < 0.05. DOI, duration of injury; LOI, level of injury; AIS, International Standards for Neurological Classification of SCI.

Figure 4

Results of the two groups at baseline and 8 weeks later. (A) Result of frequency; (B) result of time spent per bowel day; (C) result of manual digital stimulation for each bowel evacuation; (D) oral medication for each bowel evacuation; (E) Glycerine Enema each bowel evacuation; (F) result of NBD; the Wilcoxon Mann–Whitney U rank sum test was used for comparison between groups; The Wilcoxon signed rank sum test was used for intra-group comparison; ^*p < 0.05. NBD, neurogenic bowel dysfunction.

Figure 5

Results of Chao1, Shannon, and Simpson index; The abundance (assessed by Chao Index) and diversity (assessed by Shannon and Simpson index) of intestinal flora in the two groups were compared based on ASV levels. Kruskal–Wallis H test; ^*p < 0.05.

Figure 6

(A) ANOSIM analysis, reflecting beta diversity, was used to compare differences in intestinal flora community structure between SCI patients and healthy men; (B) STAMP analysis was used to compare the difference in intestinal flora species abundance between SCI patients and healthy people.

Figure 7

Changes in phylum levels and top 15 genus levels of intestinal flora in both groups at baseline and 8 weeks later. (A) Changes in phylum levels in the EAW group at baseline and after 8 weeks of intervention; (B) changes in phylum levels in the Conventional group at baseline and after 8 weeks of intervention; (C) changes in top 15 genus levels in the EAW group at baseline and after 8 weeks of intervention; (D) changes in top 15 genus levels in the conventional group at baseline and after 8 weeks of intervention; (E) the difference of top 15 genus levels between the two groups after 8-week intervention was compared. ^*p < 0.05. HM, healthy men; Pre- or Post-C, pre- or post- conventional intervention; Pre- or Post-E, pre- or post-EAW intervention.

Figure 8

Spearman correlations between intestinal flora and clinical indicators including NBD, external assistance, time spent and bowel frequency. (A) Spearman correlation between phylum levels and clinical indicators; (B) Spearman correlation between top 15 genus levels and clinical indicators; ^*p < 0.05, ^**p < 0.01, ^***p < 0.001.