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Abstract

The intestine, as a crucial organ of the human body, has remained enigmatic despite the remarkable advancements in modern medical technology. Over the past decades, the invention of endoscopic technology has made the noninvasive intervention of the intestine a reality, expanding diagnostic and therapeutic options for diseases. However, due to the single-treatment feature of endoscopic procedures, continuous or repeated medication administration, sampling, and decompression drainage within the intestine have yet to be fulfilled. These limitations persisted until the invention of colonic transendoscopic enteral tubing (TET) in 2014, which realized repeated fecal microbiota transplantation, medication administration, and decompression drainage for the treatment of colon perforation and intestinal obstruction, as well as in situ dynamic sampling. These breakthroughs have not gone unnoticed, gaining global attention and recommendations from guidelines and consensuses. TET has emerged as a novel microbial research tool that offers new paradigms for human microbiome research. This review aims to update the research progress based on TET.

Keywords

fecal microbiota transplant obstruction perforation sampling transendoscopic enteral tube

Introduction

With the concept that “all diseases begin in the intestine” put forth by Hippocrates, the importance of the intestine is self-evident. Since the first application of rigid endoscopy in 1868,¹ interventional endoscopy has expanded from diagnosis to therapy, including the removal of lesions and management of strictures.² Despite advancements, comprehensive management of intestinal diagnosis and treatment still presents clinical challenges, including diagnosing intestinal strictures and complex fistulas via retrograde radiography, treating obstructions caused by Crohn’s disease (CD), and addressing iatrogenic colonoscopy perforations.

Recent studies have underscored the pivotal role of microbiota in various diseases, encompassing infections, inflammation, malnutrition, and cancer.^3–7 Targeting the microbiome for disease treatment has spurred a series of groundbreaking technologies, especially in fecal microbiota transplantation (FMT),⁸ which gained approval as a standard therapy for recurrent Clostridioides difficile (CDI) by official guidelines in 2013.⁹ Since then, FMT has been reported to address 85 diseases over the past decade effectively.¹⁰ An improved method of FMT, known as washed microbiota transplantation (WMT), has been developed based on an automatic washing process and related delivery decisions.¹¹ A consensus on WMT has been established by the FMT-standardization Study Group in China in 2020.¹² Traditional FMT delivery methods include upper gut delivery through oral-fecal microbiota capsules, mid-gut delivery through trans-nasojejunal tube or jejunostomy, and lower gut delivery through enema or colonoscopy.¹³ However, these delivery methods have significant limitations, as they do not allow for convenient, repeated infusions of fresh microbiota suspension while ensuring whole-colon coverage.^14,15

To address these issues, Zhang’s group introduced the concept of colonic transendoscopic enteral tubing (TET) in 2014.¹⁶ Colonic TET has since been widely used in clinical practice for treatment, diagnosis, and microbiome research, benefiting lots of individuals by 2023.¹⁷ The development of multidisciplinary combination therapy, a technology-driven model that integrates the needs of multidisciplinary advancements, is gradually transforming traditional medicine. Colonic TET has evolved from its initial focus on delivery route to its current application in various clinical settings.^18,19 This article aims to update recent advancements in colonic TET research.

The concept and techniques of colonic TET

TET is an interventional therapeutic procedure for the intestine, typically including colonic TET and mid-gut TET.^20,21 The colonic TET tubes (FMT Medical, Nanjing, China) feature three separate line loops for affixing the tube to the intestinal wall using endoscopic clips. The tube wall has side openings to optimize medication infusion and fluid drainage. The colonic TET procedure involves two colonoscope insertions: the first positions the TET tube at the target location via the endoscopic channel, and the second secures it to the intestinal wall with endoscopic clips (Figure 1). Although two endoscope insertions are required, a study suggests that using a transparent cap can notably reduce the time of the second insertion (2.8 vs 2.2 min, p < 0.001).²² The tube’s position and the number of endoscopic clips are determined by the mucosal condition and expected retention time. Wen et al. reported a median retention time of 9.3 ± 3.8 days for the TET tube, using an average of 3.5 ± 1.0 endoscopic clips. The type of clips was identified as an independent factor influencing retention time, with larger clips associated with longer retention (n = 3, 9.3 ± 2.9 vs 5.4 ± 2.0 days, p = 0.000; n = 4, 11.3 ± 4.3 vs 6.6 ± 2.0 days, p = 0.001).¹⁵ Notably, increasing the number of endoscopic clips beyond 4 did not extend the retention time of the TET tube. No further endoscopic procedures are necessary, as the tube can either be naturally dislodged with intestinal movement after the clips are released from the intestinal wall, or it can be actively removed by a physician. Preoperative evaluation of anesthesia is critical. During the operation, there have been no reports of bleeding or perforation happened. Postoperative bending and violent pulling of the TET tube can cause abdominal pain in some patients. In such cases, manually re-inserting the TET tube into the intestine can effectively resolve the issue. Overall, the procedure carries a low risk.

Figure 1.

The procedure of colonic TET operation.

The application of colonic TET

Multiple treatments via colonic TET

The historical significance of rectal enema in ancient China is profound, with its origins dating back to the Dong Jin Dynasty. Around 310 AD, Hong Ge’s book “Zhou Hou Bei Ji Fang” documented the use of “Tu Gua Gen” to treat constipation via enema,²³ a practice that remains a crucial method for administering Chinese medicine even today.²⁴ Enema treatments were also documented in ancient Egypt and India during the 5th century BC.²⁵ Subsequent studies published in various journals confirmed the feasibility of administering medication via enema.^26–28 However, a study indicated that administering chlortetracycline via enema failed to reach the desired therapeutic level in 1952.²⁹

In addition, issues such as insufficient medication coverage and limited retention times persisted, with retention lasting less than an hour in 25% of cases.²⁹ Furthermore, enema-related equipment and techniques posed severe risks, as Roland and Rogers³⁰ reported in 1958, with four patients dying from infections caused by perforation following an enema. Despite efforts by doctors to compensate for insufficient coverage through endoscopy, these attempts were limited to single treatments. Philip documented that repeatedly administering FMT via a Foley catheter for severe and complicated CDI, instead of a colonoscope, also carries the risk of catheter slippage.³¹ These challenges were maintained until the emergence of TET technology allowing for safe, convenient, repeated, and extensive medication delivery of the deep colon or terminal ileum.

Colonic TET for frequent delivery

Several studies on WMT delivery via colonic TET have demonstrated high efficacy. Zhang’s group conducted the first clinical evaluation of colonic TET, revealing its benefits in providing whole-colon coverage, repeatable administrations, and precise delivery. The cohort study¹⁶ involved 54 patients aged 10–70 years, reporting a 100% success rate with a procedure duration of 14.8 ± 5.8 min. Each patient was repeatedly delivered purified microbiota suspension by the automatic system (GenFMTer; FMT Medical).¹¹ In addition, some patients received multiple whole-colon therapies with mesalazine or glucocorticoid via colonic TET tubes. No discomfort was reported during the retention period (12.4 ± 2.3 days), and 98.1% (53/54) of patients expressed satisfaction with TET.

Two additional studies assessed the feasibility, safety, and satisfaction of TET in pediatric populations aged 3–10 years.^32,33 Parental acceptance for colonic TET tubes significantly increased from 29.8% to 70.2% after WMT treatment (p < 0.001), indicating the safety and comfort of colonic TET.³² In the latest multi-center questionnaire survey,³⁴ the acceptability of colonic TET increased from 63.2% in 2020³⁵ to 76.6%, and the satisfaction consistently of colonic TET remained above 95%. These results indicate a comprehensive evaluation considering both the simplicity of the procedure and its impact on the patient’s quality of life. Compared to conventional nasojejunal tubes, mid-gut TET demonstrated a low displacement probability due to endoscopic clip fixation and eliminated the need for X-ray verification of tube position. Therefore, mid-gut TET may be a better choice for patients with upper gut lesions or those requiring prolonged enteral nutrition.²⁰ However, Zheng et al.’s³⁶ study stated that the mid-gut TET group showed a longer operation time and a higher average cost compared with the manual nasojejunal tube group. Therefore, the clinical application of mid-gut TET should consider the specific condition and willingness of the patient.

Moreover, various studies have demonstrated the feasibility of utilizing TET for WMT treatment across different diseases. He’s group and Liu’s group reported promising results in diabetic patients who received WMT via TET.^37,38 A randomized controlled trial in 2023 by Yang et al.³⁹ showed that mid-gut TET could be used for FMT in diabetic peripheral neuropathy. Beyond metabolic disease, TET has also been applied to treat central nervous system diseases, such as supranuclear palsy-Richardson’s syndrome⁴⁰ and amyotrophic lateral sclerosis.⁴¹ Additional studies, including a case report on FMT for IgA nephropathy⁴² and a retrospective cohort study on WMT for chronic kidney disease,⁴³ have also utilized TET. Recently, Wang et al.⁴⁴ highlighted the potential of microbiota-based treatments via TET for radiation injury. Since 2015, numerous clinical studies on TET as a delivery route for WMT have been conducted in China.^45–47 In 2019, Wang et al.⁴⁸ first reported the fixation of a colonic TET tube at the terminal ileum for FMT. Between 2019 and 2021, TET gained endorsements from several expert consensus statements as a safe and effective novel technology for WMT delivery.^12,49,50

Notably, subgroup analysis showed that highly experienced endoscopists had significantly shorter mean operation times compared to their less professional counterparts (3.3 ± 0.9 vs 5.5 ± 2.4 min, p = 0.002). Operation time for less experienced endoscopists significantly decreased after the first 10 cases (7.0 ± 2.4 vs 4.0 ± 1.0 min, p = 0.015), indicating the broad feasibility of incorporating TET into routine clinical practice.²⁰

Zhang et al.²³ highlighted the significant impact of the delivery method on WMT efficacy. Compared to 81.5% with lyophilized oral capsules,⁵¹ Wu et al.⁵² reported a 90.7% clinical cure rate for CDI patients treated with WMT via colonic TET. Allegrett et al.⁵³ commented on colonic TET as a promising WMT delivery way in The Lancet. Similarly, Gulati et al.⁵⁴ commented on TET as an effective FMT delivery route.

Furthermore, Kassam et al.⁵⁵ and Narula et al.⁵⁶ suggested that colonic administration is more effective than mid-gut delivery for treating CDI. In addition, patients undergoing WMT via colonic TET experienced a significantly lower incidence of adverse events (6.0% vs 23.3%, p = 0.017).⁵⁷ Based on these findings, Zhang and Liu⁵⁸ identified four key factors that influence the selection of WMT delivery route in clinical practice: safety, efficacy, cost-effectiveness, and patients’ willingness.

Colonic TET is applied for drainage

In the early 20th century, segmental resection stood as the cornerstone of treatment for intestinal perforation,^59,60 marking a significant milestone in the history of gastroenterology. The year 1953 witnessed a breakthrough with the introduction of peritoneal catheterization, a minimally invasive procedure that revolutionized the approach to this condition.^61,62 The subsequent development of laparoscopic technology further accelerated the integration of diagnosis and treatment for intestinal perforations,⁶³ marking a new era in surgical techniques. The advent of minimally invasive endoscopic techniques, as demonstrated by Binmoeller et al.⁶⁴’s successful case of treating an intestinal perforation with metal clips via endoscopy in 1993. However, despite the gradual advancement of over-the-scope clip technology in modern medicine,^65,66 patients with delayed bowel perforation still face risks such as abdominal infection, perforation enlargement, surgical intervention, and increased costs.

Effective decompression and drainage remain central to treating intestinal obstruction. Despite rectal catheters and endoscopy-guided catheters having been used in recent decades,^67–69 their limited length hinders effective drainage at the upper end of the obstruction. In addition, the potential risk of displacement has also been noted, leading to attempts at invasive suturing of the distal end onto the skin. However, such attempts significantly compromise patient comfort and satisfaction. Completely avoiding emergency surgery remains challenging, with outcomes as uncertain as Schrödinger’s cat—both alive and dead. Therefore, new technologies are needed to support doctors in decision-making.

Endoscopy-associated perforation: To achieve zero transfer to surgery

An expert review published by AGA in 2021⁶⁶ emphasized the importance of thorough preoperative preparation for endoscopists managing high-risk perforations. Typically, iatrogenic perforations in patients with inflammation bowel disease (IBD) are considered for surgery if endoscopic repair fails.⁷⁰ Timely prediction and effective treatment are crucial for managing endoscopy-associated perforations. In 2021, a case involving a CD patient with an intestinal stricture who developed a perforation after endoscopic balloon dilation initially confirmed the therapeutic efficacy of colonic TET in treating endoscopic perforations.¹⁹ In addition, in 2023, Jiang et al.⁷¹ suggested that combining TET drainage with endoscopic clip closure is a new and straightforward method for treating various types of iatrogenic endoscopy perforation. To achieve the goal of zero transfer to surgery, the TET Study Group made the following recommendations in 2023¹⁷: (1) Proper, timely, and accurate placement of the TET tube is crucial, along with conventional decompression, drainage, and antibiotic treatment; (2) gas and fluid should be suctioned out through the TET with a syringe every 4 h; and (3) the 3.3 mm colonic TET tube is advantageous for efficient decompression and drainage.

Obstruction: To achieve adequate decompression and drainage

For CD patients with intestinal obstruction, perioperative management remains a consistent concern for surgeons.⁷² A recent case report in Endoscopy highlights the use of colonic TET to delay surgery in CD patients with incomplete intestinal obstruction, and adequate perioperative preparation was obtained for the patient.⁷³ This case presented the first description of employing colonic TET through the intestinal stricture, achieving short-term continuous and adequate drainage of proximal intestinal pressure. In addition, retrograde imaging of the upper end of the stricture using colonic TET fully delineated the location and extent of the lesion, providing valuable preoperative information for the surgery. Ultimately, the patient underwent successful one-stage resection and anastomosis of the affected intestinal segment. Beyond pathological intestinal obstruction, Wen et al.⁷⁴ recently reported a case of successful management of fecalith impaction in the distal ileum using the TET for targeted drug delivery in Endoscopy.

However, it is imperative to note that these findings are based on case reports. Larger sample sizes and high-quality clinical studies on colonic TET for treating deep intestinal complications are essential to establish more robust evidence. In conclusion, the exploration of colonic TET as a novel and promising intervention for intestinal treatment is an area of ongoing progress.

Clinical diagnosis via colonic TET

Diagnosing deep intestinal diseases relies on the development of endoscopic technology and radiography. Although attempts to combine these methods for retrograde imaging, diagnosing complex digestive system diseases remains challenging. This challenge is particularly evident in patients with IBD who present complex gut lesions, including obstruction, fistula, and gastrointestinal diversion surgery, where surgical intervention must be carefully considered. Surgeons aiming for one-stage anastomosis must gather sufficient clinical information to support their decisions. However, the lack of research evidence often places them in a dilemma. In 2023, Yu et al.⁷³ reported that retrograde imaging of the upper end of the stricture via colonic TET fully delineated the location and extent of the lesion, offering a basis for expanding TET’s clinical diagnostic applications and a reason for optimism. A recent case reported that retrograde colon imaging through colonic TET helped identify the cause of a difficult colonoscopy.⁷⁵ In addition, colonic TET can be used to diagnose complex intestinal fistulas via contrast agent injection. Despite these promising findings, larger-scale clinical trials and robust methodologies are necessary to strengthen the evidence supporting colonic TET for diagnosing deep intestinal complications.

Microbiome research via colonic TET

In the past, the human gut microbiome was predominantly examined through fecal samples, limiting our understanding of microbial dynamics across different gastrointestinal sites. The intermittent availability of fecal samples also posed challenges for analyzing microbial changes with finer temporal resolutions. Recently, Waimin et al.⁷⁶ and Shalon et al.⁷⁷ reported a smart capsule that collects samples from various regions of the human intestinal tract during normal digestion. Through multi-omics analyses, a comprehensive approach that combines multiple “omics” technologies such as genomics, transcriptomics, proteomics, and metabolomics, they identified significant differences in bacteria, phages, host proteins, and metabolites between the intestinal tract and stool samples. Despite this advancement, the collected samples may remain in the intestinal tract for several hours or even days, during which the microbiota undergo dynamic changes, making real-time reflection of the in vivo environment difficult. Furthermore, detailed spatial and temporal analysis of deep intestine microbes is challenged by uncertainties in sample collection sites and capsule discharge times.

Through colonic TET, researchers can accurately access the terminal ileum and deep colon for real-time dynamical sampling of intestinal specimens, which is crucial for addressing scientific questions. Building on this, Wang’s group and Zhang’s group were the first to report deep intestinal sampling via colonic TET under various spatial and temporal conditions, investigating microbial changes in the human intestine.¹⁸ In their study, circadian rhythms of human intestinal microbes were initially documented through in situ samples. In addition, Cao et al.⁷⁸ developed a model in 2022 aimed at unraveling the spatial variation in microbial interactions and quantifying the causal relationships between microbiome variability and disease progression. TET sampling offers a more feasible and convenient approach than previous methods for analyzing the impact of spatial microbial distributions on host disease and treatment in the gut.

Microbial metabolites can interact with distant organs through enterohepatic and blood circulation, but the composition of intestinal microbes in situ differs significantly from fecal samples. Relying solely on fecal analysis for metabolite assessment only provides indirect measurements. As the first noninvasive method for dynamic deep intestinal sampling, TET technology shows significant potential for advancing research in pharmaco-microbiomics, host-microbial dynamics, gut microbial circadian rhythms, and other crucial areas.

Conclusion

This article updates the diverse applications of colonic TET, ranging from microbiota delivery, perforation rescue, and intestinal obstruction relief, to colon sampling, demonstrating its expanding utility (Figure 2). As an emerging technology and interventional concept, colonic TET is bridging the gap between the microbiome and various disciplines, reshaping medical practice. Colonic TET serves as a key driver of progress in the growing field of microbiota medicine (Figure 3),⁷⁹ a new clinical medical discipline. It has evolved beyond its original purpose, influencing current clinical practice and research paradigms. Future studies with larger sample sizes and rigorous designed are crucial to further establish its value in clinical practice and research.

Figure 2.

The diagram of colonic TET in clinical practice and research. Delivering: different types of medications via colonic TET for treatment and retrograde imaging; sampling: real time and in situ sampling for microbiome research; drainage: treatment for colonic complications.

Figure 3.

The important events of colonic TET.

Footnotes

Acknowledgements

The authors thank the following investigators who participated in this study: You Yu (The Second Affiliated Hospital of Nanjing Medical University), Sibusiso Luthuli, and Jianyu Wu (The Second Affiliated Hospital of Nanjing Medical University).

Declarations

ORCID iD

Faming Zhang

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Colonic transendoscopic enteral tubing is revolutionizing intestinal therapeutics,diagnosis,and microbiome research

Abstract

Keywords

Introduction

The concept and techniques of colonic TET

The application of colonic TET

Multiple treatments via colonic TET

Colonic TET for frequent delivery

Colonic TET is applied for drainage

Endoscopy-associated perforation: To achieve zero transfer to surgery

Obstruction: To achieve adequate decompression and drainage

Clinical diagnosis via colonic TET

Microbiome research via colonic TET

Conclusion

Footnotes

Acknowledgements

Declarations

ORCID iD

References