Intraoperative Diagnostics of Ischemic Damage to the Small Intestine: Current Opportunities and Unsolved Challenges

  • Authors: Baleev M.1, Sizov M.2, Romanov I.2, Mokeev O.2, Vorobiev A.2, Baleeva M.3, Kozharinov V.4
  • Affiliations:
    1. ГБУЗ НО «Городская клиническая больница № 30 Московского района г. Нижний Новгород»
    2. Государственное бюджетное учреждение здравоохранения Нижегородской области «Городская Клиническая Больница № 30 Московского Района г. Нижнего Новгорода», г. Нижний Новгород, Россия
    3. Государственное бюджетное учреждение здравоохранения Нижегородской области «Городская поликлиника № 4 Канавинского Района г. Нижнего Новгорода», г. Нижний Новгород, Россия
    4. Государственное бюджетное учреждение здравоохранения «Пензенская областная клиническая больница имени Н.Н. Бурденко», г. Пенза, Россия
  • Issue: Vol 13, No 3 (2020)
  • Pages: 285-292
  • Section: Review of literature
  • URL:
  • DOI:
  • Cite item


Management of patients with acute intestinal ischemia remains a serious challenge for specialists involved in urgent surgery. The paper presents current trends review on the intraoperative assessment of the intestinal microvasculature during its ischemic damage, including the initial intervention and re-examination operations. The pros and cons of X-ray angiography, spiral computed tomography (CT), magnetic resonance imaging (MRI), laser Doppler flowmetry, methods based on the use of exogenous fluors and photosensitizers are described in details. The features of second-look operations in open and laparoscopic modes, their advantages and disadvantages, possible complications, indications and contraindications to each of these methods are closely examined. Particular attention is paid to the perspectives of using optical coherence tomography in surgery. However, despite all the achievements of modern surgery in the treatment of patients with acute intestinal ischemia, the problem of surgical tactics has not been completely resolved. Novel knowledge about the development of necrosis in the intestinal wall will reduce the volume of its resection and the incidence rate of postoperative complications.

Acute intestinal ischemia (OII) is a group of diseases that are similar in course and prognosis due to acute circulatory disturbance in the intestine [1]. Acute intestinal ischemia develops as a result of occlusion of the mesenteric vessel with an embolus or blood clot, infringement of blood vessels supplying the intestine [1,2], traumatic damage to mesenteric vessels, strangulated intestinal obstruction [3,4,5], non-exclusive spasm of mesenteric arteries, redistribution of blood flow during massive blood flow 6].
The total number of patients with OII in surgical hospitals ranges from 0.2 to 7% [7]. The proportion of patients with the most severe form of OII - acute mesenteric arterial thrombosis - in the structure of patients hospitalized in domestic surgical hospitals over the past fifty years has been from 0.2% to 0.4% [1]. Abroad, thrombosis of mesenteric arteries is diagnosed in 0.25% of cases of all admissions to the hospital. The number of patients with acute intestinal ischemia caused by its infringement is 4-7% of those operated on an emergency basis and has not decreased over the past 20 years. Based on the main mechanism for the development of circulatory disorders in the intestine, OII are traditionally divided into occlusive and non-inclusive types. The most difficult clinical problem is the timely diagnosis and treatment of occlusive forms of OII, which are diagnosed in 90-95% of cases of OII and develop as a result of complete cessation of blood flow and / or outflow due to obstruction in the lumen of blood vessels, compression from the outside or their traumatic damage. Predisposing factors of occlusal OII are atherosclerosis of the aortic branches, reconstructed operations with occlusive stenotic lesions of arteries, history of arterial embolism, congenital or acquired disorders in the hemostatic system [7]. Mortality from OIs of the occlusive type, depending on the scale of the lesion and the nosological form, ranges from 10 to 95% [8]. Ischemic damage to the loop of the intestine, restrained in a hernia, leads to death in 10% of cases [9]. The frequency of fatal outcomes in case of abdominal vascular injury ranges from 28 to 59%, with a peak in mortality occurring on the first day after an emergency operation. With thrombosis and embolism of the mesenteric arteries, the number of adverse outcomes varies between 59–89% [10], and according to some reports, it reaches 95–100%.
The introduction of emergency endovascular interventions made it possible to slightly improve the results of treatment in the group of patients with local occlusive lesion of I-II segments of the superior mesenteric artery, and to reduce mortality
in the group of operated patients up to 15-37%. However, with OIs of an occlusive type, the severity of the positive clinical effect of thrombus removal decreases with every hour of the disease. Ischemic alteration leads to irreversible changes in the structure of the intestinal wall within 2-12 hours, depending on the individual characteristics of the vascular architecture, the state of the vascular wall, the extent of the lesion, and the general condition of the body [11,12]. The physiological peculiarity of the intestinal mucosa - a high sensitivity to reperfusion injury, significantly limits the effectiveness of intravascular operations.
It should be noted that the proportion of patients with OIs of the occlusive type hospitalized earlier than 8 hours from the onset of the disease does not exceed 30%. Other patients hospitalized later than 6-8 hours from the onset of the disease do not usually receive endovascular interventions (removal of blood clots, emboli from the arterial lumen). In most such cases, an operation is performed that reduces the likelihood of a quick fatal outcome - an extensive resection of the intestine affected by the ischemic process. Moreover, extensive intervention increases the severity of the operating injury, the duration of paresis, can lead to renal dysfunction, short bowel syndrome, liver dystrophy, renal failure [13,14]. At the same time, insufficiently radical resection becomes the cause of the failure of the intestinal anastomoses, ischemic stress ulcers, peritonitis [15]. The situation is aggravated by the fact that modern clinical recommendations and guidelines are very controversial in the question of choosing the boundaries of the intestinal resection in patients with acute intestinal infections. Recommended boundaries range widely: “within healthy tissues, 1 cm departing from the necrosis line” [16], departing from the border of non-viable tissues in the proximal and distal directions by 9-24 and 5-10 cm, respectively [17], 15-18 cm [18], with a retreat of 30 cm in the direction of the adducting and discharge sections of the intestine, 40 cm adducting and 20 cm of the abduction sections [19]. Since the boundaries of viability are determined on the basis of subjective data, and the recommendations for retreating from the borders of necrosis are contradictory, the result of bowel resection is prone to systemic errors [13]. They, in turn, are a predictor of the failure of the intestinal anastomoses, the occurrence of ischemic ulcers, peritonitis, and intestinal paresis [20].
New data on the physiology of segments subtly the intestine became the basis for changing the traditional paradigm, in which the generally accepted way to reduce the risk of postoperative complications is to expand the boundaries of the intestinal resection. Currently, it is known that extensive removal of part of the small intestine leads to general complications in the form of organ dysfunction [11], and resection of individual segments of the intestine, even a relatively small extent, is accompanied by a violation of the motor, digestive, regulatory, and other functions of the entire gastrointestinal tract . So, resection of the proximal segments of the jejunum leads to the loss of fluid, electrolytes, nutrients necessary for the full functioning of the body. After resection of the proximal segments of the jejunum, the duration of hypersecretory activity of the stomach increases, which contributes to ulceration of the proximal sections of the small intestine and enhances malabsorption [18]. It is very important that the ileum, namely its distal 100 cm, is the only area in which bile acids and vitamin B12 are absorbed. In general, the incidence of complications after emergency operations for acute intestinal ischemia ranges from 16 to 62%. It is crucial that even after the surgical removal of mesenteric vessel occlusion, reperfusion syndrome and physiological release of catecholamines for a long time support vasoconstriction in the intestinal wall. This pathogenetic mechanism, similar to the mechanism of non-inclusive alteration of the intestine, but developing a second time after surgery, is, apparently, the basis of ongoing ischemic alteration and the most important cause of resections in the postoperative period [19,21,22]. To increase the safety and effectiveness of medical interventions in case of acute respiratory infections, the surgeon is obliged to determine as accurately as possible the prevalence of intestinal wall lesions, the stage of the ischemic process, and the state of the mesenteric and intramural vessels. Attention should be focused on objects through which the mechanisms of intestinal infarction — the intramural vascular bed, layers of the intestinal wall, and foci of nonviable tissues in them — are realized first of all [23,24].
In scientific and practical works devoted to the fundamental mechanisms of intramural microcirculatory disturbance and patterns of the spread of ischemic necrosis in acute respiratory infections, the choice of methods for studying the intestinal wall plays a fundamental role [25]. The main trend is the use of intravital, minimally invasive diagnostic methods, as well as the development of processing algorithms for the information received to minimize errors in visual assessment [8]. X-ray angiography, the most widespread modern method for the study of blood vessels, does not yet demonstrate a high level of efficiency with occlusion-type OII: it does not allow visualization of the intramural channel of the intestinal blood flow with the diameter of the affected vessels less than 500 microns. The disadvantages of angiography also include a high degree of invasiveness, nephrotoxicity, radiation exposure, and the duration of the procedure, which sharply limit its use in real conditions of emergency surgery. Spiral computed tomography (CT), some authors define as the method of choice for lesions of the trunks of mesenteric vessels [23]. The sensitivity and specificity of SKT are maximal in cases of lesions of the first and second segments of the superior mesenteric artery (IBA), with the onset of late manifestations of OII - dilated intestinal loops, thickening of the intestinal wall, and mesenteric edema [26]. According to some authors, the intraparietal gas of the intestine (22-73%), the gas in the portal and mesenteric venous systems (9-86%) with high probability indicate precisely acute violation of mesenteric circulation [26,27]. Moreover, the possibilities of SKT in the diagnosis of non-inclusive forms of intestinal ischemia and occlusive lesions of the distal arteries are very limited. In many ways, similar to CT, magnetic resonance imaging (MRI) is able to identify areas of necrotic and viable tissues, but their resolution does not allow visualization of objects less than 500 microns, in particular, the most important of them are intramural intestinal vessels [19]. For this reason, SKT and MRI technologies, as a rule, are not applied intraoperatively, repeatedly, specifically to assess the viability of a particular section of the intestine [26,28], which means that they cannot be useful in solving the problem of reducing the volume of intestinal resection.
The use of exogenous fluors and photosensitizers has become a promising direction in the intravital diagnosis of intestinal microcirculation [29]. In particular, the in vivo assessment of microcirculation in vessels with a diameter of several hundred micrometers is carried out using fluorescein and indocyanin green. This method has been successfully used for 30-40 years in various fields of medicine (oncology, ophthalmology, neurosurgery, etc.), including in surgery of the small and large intestines. The analysis carried out by coloproctologists, along with an indication of some positive results, states that the prospects are far the smallest study [30].
Of particular interest among modern technologies that meet the requirements of non-invasiveness, sufficient resolution and depth of research, the possibility of multiple intraoperative applications, researchers are interested in optical coherence tomography (OCT) and optical coherent angiography (OCA). The effectiveness of ACA in assessing the state of the microvascular bed of various tissues, including in conditions of ischemia, is undeniable [31,32]. The method has already demonstrated effectiveness in visualizing microvessels and tissue microstructure in ophthalmology [31,33], dermatology, cardiology, abdominal surgery [34], endoscopic gastroenterology [35].
Widespread use in experimental and clinical bowel surgery has received the method of laser Doppler flowmetry (LDF). The method is based on non-invasive tissue sensing by laser radiation and allows one to assess the state of microcirculation due to the reflection of laser radiation from moving red blood cells [36]. The main criteria for assessing the state of microcirculation of the intestinal wall are indicators of neurogenic and myogenic vascular tone [37]. For intravital imaging of microcirculation, microscopy methods based on the sidestream dark field imaging (SDF) method and orthogonal polarized spectral imaging (OPS) are actively developed and technologically improved. However, these methods are limited by the shallow depth of tissue imaging. In fact, they are able to reproduce only images of the surface of the intestine, which is completely insufficient, given the case of its structure and the degree of ischemic alteration differentiated in depth and width [38]. Histomorphometric study, being the "gold standard" in verification of necrotic changes and other disorders of the morphological structure of tissues, in principle, does not imply the study of native tissue in vivo, which is absolutely necessary for determining intraoperative tactics in acute mesenteric ischemia.
The author's methods for studying the microvascular channel of the intestine, tested in limited single studies, are of interest, however, their inclusion in the clinical diagnosis algorithm is not always advisable due to incomplete information on sensitivity and specificity [39]. Pigmented vasoscopy is based on the introduction of a 1% solution of methylene blue into the vascular bed, 15 minutes after this, staining of the intestinal wall is evaluated [38]. Seagal Z.M. To diagnose intestinal viability, he suggested measuring the amplitude of pulse oscillations and the rate of tissue oxygenation. Amplitude values ​​below 2 mm and tissue oxygenation data of less than 80% were regarded as a sign of a non-viable area of ​​the intestine [40].
The clinical task of performing operations of repeated examination of the abdominal cavity and its rehabilitation in the early postoperative period with an unhealed laparotomy wound is relevant for a large group of patients with acute intestinal ischemia. The gold standard for re-examination operations remains programmed laparotomy [41,42]. Dynamic video laparoscopic monitoring of the state of the small intestine and the formed small intestinal anastomoses allows in some cases to avoid the implementation of programmed relaparotomies in these patients. Some authors propose to abandon programmed relaparotomies as a factor of surgical aggression, and after instrumental assessment of the microvasculature of the intestine to form an intestinal anastomosis after resection during the primary and only operation. Postoperative endoscopic monitoring of acute abdominal-ischemic syndrome and mesenteric vessel thrombosis allows early visual assessment of the dynamics of the disease, the development of complications, and to avoid unreasonable reoperation [13]. A feature and advantage of using the programmable relaparotomy method, according to some authors, is that this operation allows timely diagnosis and elimination of complications, as well as preventing the development of compartment syndrome [20,43]. An obvious technical drawback of traditional relaparotomy is the need for multiple temporary closure of the relaparotomy wound, which increases the risk of local septic and general postoperative complications [44].
The generally accepted modern technology for minimally traumatic reoperations - interventions under laparoscopic control. Programmed relaparoscopy in comparison with relaparotomy minimizes surgical trauma, accelerates the recovery of peristalsis, reduces the number of adhesive postoperative complications, reduces the time taken for taking analgesic drugs and the patient’s hospital stay [19]. The standard laparoscopy technique allows you to visually assess the viability of the intestine, the presence of pathological exudate, visualize peristalsis, and assess the size of the intestinal loop. If the value of laparoscopy in the diagnosis of the early stages of acute respiratory infections by most authors is called into question, its use in the diagnosis of extensive intestinal infarction is widely recognized [10]. The laparoscopic picture of OII in the stage of intestinal infarction is very characteristic: hemorrhagic effusion, swelling of the intestinal wall and mesentery, purple color of the intestinal wall and mesentery, hemorrhage in the intestinal wall and mesentery, absence of intestinal motility, inflammatory changes in the visceral peritoneum [12,36]. However, such vivid manifestations of non-viability appear only in the stage of heart attack, necrosis, and are absent in the stage of intestinal ischemia [20]. It is fundamentally important from the point of view of prognosis for patients with OII that the need for carboxyperitoneum in the traditional laparoscopy technique compromises intramural blood flow and increases the risk of developing intra-abdominal hypertension syndrome [20,46]. Carboxyperitoneum exacerbates discirculation in the intestinal wall, significantly increases the risk of organ dysfunction [34]. Thus, even in the case of successful mechanically tight matching of the edges of an unhealed laparotomic wound, its sealing and creation of conditions for applying pneumoperitoneum, the patient is at risk of spreading and progressing organ failure due to an increase in intraperitoneal pressure provoked by pneumoperitoneum.
The surgical technique of laparoscopy, which avoids the imposition of pneumoperitoneum and does not imply an increase in intra-abdominal pressure, is endovideo surgery with a gas-free laparolift. Devices for lifting the abdominal wall without injecting gas into the abdominal cavity are widely used in planned and emergency surgery, however, most of them do not meet the requirements specific to OII. The features of repeated operations for OII include: a large inspection area, due to the need for revision of the intestine throughout its duration and the relative mobility of the segments of the intestine in the abdominal cavity; high probability of conversion when complications are detected; the need for several repeated operations, the volume of which is unpredictable in advance and ranges from a short examination to extensive intestinal resections [47].
For less traumatic manipulations with the edges of the laparotomy wound during a staged intervention on the abdominal organs, various devices and technologies are used [48]. However, these devices have significant limitations in the treatment of patients with acute ischemia of the intestine: they provide the ability to move the edges of the laparotomy wound only in the frontal plane of the abdomen, that is, they only suggest the reduction and dilution of the edges of the laparotomy wound without moving the abdominal wall in the sagittal plane; do not provide the possibility of safe laparoscopic access to the abdominal cavity, since for the introduction of a laparoscope it is necessary to raise the abdominal wall above the organs of the abdominal cavity; a full revision of the abdominal organs when using such devices is impossible without a complete dilution of the edges of the wound. It should be noted that the pathogenetic basis of several serious complications in patients with acute intestinal ischemia is the abdominal compartment syndrome [36,49,50]. At the same time, the technical conditions for traditional laparoscopy suggest the need to apply pneumoperitoneum with a positive pressure of 10-15 mm RT. Art. [6.51]. The patient is at risk of progression of organ failure due to an increase in intra-abdominal pressure provoked by pneumoperitoneum. At present, there is no doubt that in patients with intestinal ischemia, an increase in intra-abdominal and intestinal pressure is completely unacceptable, and the development of tools and methods to reduce pressure in the lumen of the intestine and around it is an important but unsolved task of modern surgery [52,53,54] .
Thus, in most cases, modern standards for the treatment of occlusion-type OIIs require emergency resection of the damaged part of the intestine, and inaccurate determination of the border of non-viable intestinal tissues leads to specific postoperative complications. The recently discovered unique functions of segments of the small intestine have become an impetus for the search for technologies that can reduce the volume of resection of the small intestine during its acute ischemic lesion. However, a number of unresolved issues do not yet allow the full implementation of the concept of restoration of blood circulation in the borderline with necrotic sections of the intestine: it is not known how wide the area of ​​the bowel lesion due to the non-inclusive spasm of the intramural arteries is, an algorithm for intraoperative diagnosis of sections of the intestine with reversible circulatory disorders has not been developed, the problem has not been solved safe and effective reoperations; insufficient technologies to prevent secondary damage to blood circulation scheniya. The solution of these problems can contribute to a significant reduction in the volume of bowel resection in acute ischemic damage and, in general, to improve the treatment results of patients with occlusive acute intestinal ischemia.

Mikhail Baleev

ГБУЗ НО «Городская клиническая больница № 30
Московского района г. Нижний Новгород»

Author for correspondence.
ORCID iD: 0000-0001-6943-9757

Russian Federation, Россия, г. Нижний Новгород, ул. Берёзовская 85 А. Почтовый индекс: 603157


Mikhail Sizov

Государственное бюджетное учреждение здравоохранения Нижегородской области «Городская Клиническая Больница № 30 Московского Района г. Нижнего Новгорода»,
г. Нижний Новгород, Россия

ORCID iD: 0000-0002-4548-6548

Russian Federation, Россия, г. Нижний Новгород, ул. Берёзовская 85 А. Почтовый индекс: 603157


Ivan Romanov

Государственное бюджетное учреждение здравоохранения Нижегородской области «Городская Клиническая Больница № 30 Московского Района г. Нижнего Новгорода»,
г. Нижний Новгород, Россия

ORCID iD: 0000-0002-4548-6548

Russian Federation, Россия, г. Нижний Новгород, ул. Берёзовская 85 А.

Главный врач

Oleg Mokeev

Государственное бюджетное учреждение здравоохранения Нижегородской области «Городская Клиническая Больница № 30 Московского Района г. Нижнего Новгорода»,
г. Нижний Новгород, Россия

ORCID iD: 0000-0002-7057-251X

Russian Federation, Россия, г. Нижний Новгород, ул. Берёзовская 85 А.

Заместитель Главного врача

Alexander Vorobiev

Государственное бюджетное учреждение здравоохранения Нижегородской области «Городская Клиническая Больница № 30 Московского Района г. Нижнего Новгорода»,
г. Нижний Новгород, Россия

ORCID iD: 0000-0002-0266-2249

Russian Federation, Россия, г. Нижний Новгород, ул. Берёзовская 85 А.


Marina Baleeva

Государственное бюджетное учреждение здравоохранения Нижегородской области «Городская поликлиника № 4 Канавинского Района г. Нижнего Новгорода»,
г. Нижний Новгород, Россия

ORCID iD: 0000-0003-2568-9118

Russian Federation, г. Нижний Новгород» Россия, г. Нижний Новгород, ул. Приокская 14. Почтовый индекс: 603002


Vladislav Kozharinov

Государственное бюджетное учреждение здравоохранения «Пензенская областная клиническая больница имени Н.Н. Бурденко»,
г. Пенза, Россия

ORCID iD: 0000-0002-2918-4654

Russian Federation, Россия, г. Пенза, ул. Лермонтова 28. Почтовый индекс: 440026

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