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International Wound Journal logoLink to International Wound Journal
. 2012 Jun 14;10(4):411–417. doi: 10.1111/j.1742-481X.2012.00998.x

Blood flow response in small intestinal loops at different depths during negative pressure wound therapy of the open abdomen

Sandra Lindstedt 1,, Joanna Hlebowicz 2
PMCID: PMC7950948  PMID: 22698003

Abstract

High closure rates of the open abdomen have been reported following negative pressure wound therapy (NPWT). However, the method has occasionally been associated with increased development of intestinal fistulae. We have previously shown that the application of NPWT to the open abdomen causes a decrease in microvascular blood flow in the small intestinal loop and the omentum adjacent to the visceral protective layer of the dressing. In this study we investigate whether the negative pressure affects only small intestinal loops lying directly below the dressing or if it also affects small intestinal loops that are not in direct contact with the dressing. Six pigs underwent midline incision and application of NPWT to the open abdomen. The microvascular blood flow was measured in four intestinal loops at different depths from the visceral protective layer, at two different locations: beneath the dressing and at the anterior abdominal wall, before and after the application of NPWT of −50, −70, −100, −120, −150 and −170 mmHg, using laser Doppler velocimetry. Negative pressures between −50 and −170 mmHg caused a significant decrease in the microvascular blood flow in the intestinal loops in direct contact with the visceral protective layer. A slight, but significant, decrease in blood flow was also seen in the intestinal loops lying beneath these loops. The decrease in microvascular blood flow increased with the amount of negative pressure applied. No difference in blood flow was seen in the intestinal loops lying deeper in the abdominal cavity. A decrease in blood flow was seen in the upper two intestinal loops located apically and anteriorly, but not in the lower two, indicating that this is a local effect and that pressure decreases with distance from the source. A long‐term decrease in blood flow in the intestinal wall may induce ischaemia and secondary necrosis in the intestinal wall, which could promote the development of intestinal fistulae. We believe that NPWT of the open abdomen is a very effective treatment, but that it could be improved by gaining more knowledge on the mechanisms involved.

Keywords: Intestinal wall, Microvascular blood flow, Negative pressure wound therapy, Open abdomen

Introduction

Laparostomy, or open abdomen, has developed over the past 20 years as a life‐saving intervention in surgical emergencies such as abdominal compartment syndrome, wound dehiscence, trauma and intra‐abdominal sepsis 1, 2, 3, 4, 5. Various materials have been used to dress the open abdomen, including intravenous fluid bags, Gore‐Tex, Bogota bags and sandwiched gauze dressings (6). Temporary closure of the abdominal cavity with plastic bags, silicone sheets, absorbable and non‐absorbable meshes sutured to the fascial or skin edges does not facilitate definitive closure of the abdominal wall. Skin‐only closure or split‐thickness skin grafting may be used to cover the bowels and omentum 1, 6, 7. The major drawback of these techniques is the formation of extensive ventral hernias which must be remedied at a later date. The use of negative pressure wound therapy (NPWT) for treating the open abdomen has improved care and increased the possibility of closure of the open abdomen. However, the method has occasionally been associated with increased development of intestinal fistulae 8, 9, 10, 11, 12. The reason for this is unknown. A decrease in intestinal wall blood flow caused by NPWT has been suggested as a possible reason (13). However, the patient group is often extremely complex, and it is therefore possible that there are multiple reasons for the development of fistulae. We believe that NPWT of the open abdomen is a reliable form of treatment, but that it could be improved by increased knowledge of the mechanisms governing its effects.

There have been several reports over the years showing excellent clinical results of NPWT 8, 10, 14, 15, 16, 17, 18, 19. However, in November 2009, the US Food and Drug Administration (FDA) issued a preliminary warning as a result of reports of rare but serious complications associated with the use of NPWT. The warning was issued after the FDA received reports of 6 deaths and 77 injuries associated with NPWT over a period of 2 years. Bleeding was the most serious complication, and was reported in 6 deaths and 17 cases of injury. Twenty‐seven reports indicated infection from original open infected wounds or from small pieces of dressing remaining in the wound. Small pieces of foam dressing and foam adhering to tissues or imbedded in the wound were noted in 32 injury reports. The majority of these patients required surgical procedures for the removal of these remnants, wound debridement and the treatment of wound dehiscence, as well as additional hospitalisation and treatment with antibiotics.

We have recently shown that NPWT applied to the open abdomen resulted in a decrease in microvascular blood flow in the small intestinal loop and the omentum in direct contact with the dressing, that is, vacuum source (20). We have also shown that layers of paraffin gauze placed between the intestines and the vacuum source could not prevent ischaemia in the intestinal wall lying closest to the dressing (21). An extended period of ischaemia in the small intestinal wall or in an intestinal anastomosis may promote the development of intestinal and/or enteroatmospheric fistulae.

In this study we investigate whether negative pressure affects only the small intestinal loop lying next to the dressing or if it also affects small intestinal loops deeper in the abdominal cavity. We measured the microvascular blood flow using fiberoptic laser Doppler probes. Changes in blood flow were studied in four different intestinal loops at four different depths, at locations apically beneath the dressing and at the anterior abdominal wall, during exposure to negative pressures between −50 and −170 mmHg. To the best of our knowledge no such study has previously been conducted.

Materials and methods

Experimental animals

Six domestic pigs of both sexes with a median weight of 60 kg were used. The animals were fasted overnight but given free access to water. The investigation complied with the ‘Guide for the Care and Use of Laboratory Animals' recommended by the US National Institutes of Health, and published by the National Academies Press (1996).

Anaesthesia

All animals were pre‐medicated intramuscularly with ketamine (30 mg/kg) before being brought into the laboratory. Before commencing surgery, sodium thiopental (5 mg/kg), atropine (0·02 mg/kg) and pancuronium (0·5 mg/kg) were given intravenously. Intubation was performed with a Portex endotracheal tube (7·5 mm internal diameter, Medcompare, South San Francisco, CA). A servo‐ventilator (Siemens Elema 300A, Stockholm, Sweden) was used for mechanical ventilation throughout the experiments. The ventilator settings used were: minute volume = 100 ml/kg, FiO2 = 0·5, breathing frequency = 16 breaths/minute, and positive end expiratory pressure = 5 cmH2O. Anaesthesia and muscular paralysis were maintained by continuous intravenous infusion of 8–10 mg/kg/hour propofol (Diprivan, AstraZeneca, Sweden), 0·15 mg/kg/hour fentanyl (Leptanal, Lilly, France), and 0·6 mg/kg/hour pancuronium (Pavulon, Organon Teknika, Boxtel, the Netherlands).

Data acquisition

Heart frequency and ventilator parameters were recorded throughout the experiments.

Surgical procedure

A 30‐cm‐long midline incision was performed on each pig. The V.A.C.[checkregistered] Granu Foam™ abdominal dressing system (KCI, San Antonio, TX), was used. The visceral protective layer was cut to the appropriate size, extending into the paracolic gutters on both sides (about 35 cm wide and 35 cm long). A layer of polyurethane Granu Foam was placed on top of the visceral protective layer between the edges of the wound. The wound was covered with a self‐adhesive polyethylene drape, a track pad was inserted through the drape (both from V.A.C., KCI, San Antonio, TX), and then connected to a continuous vacuum source.

Microvascular blood flow was measured using laser Doppler velocimetry (Transonic[checkregistered] Laser Doppler Monitor, BLF21, Maastricht, the Netherlands), a technique that quantifies red blood cell flow in a specific volume. This method is applied extensively in plastic surgery procedures and uses a fiberoptic probe carrying a beam of light. Light impinging on cells in motion undergoes a change in wavelength (Doppler shift), while light impinging on static objects remains unchanged. The magnitude and frequency distributions of the changes are directly related to the number and velocity of red blood cells. The information is collected by a returning fibre, converted into an electronic signal and analysed (22).

Laser Doppler probes were inserted into the intestinal walls of eight ileac loops at different depths; four located apically beneath the dressing, and four located close to the anterior abdominal wall. The experimental setup is illustrated in Figure 1. The locations of the probes were confirmed upon completion of the experiments.

Figure 1.

Figure 1

Illustration of the open abdomen setup and the location of the laser Doppler probes. Probe location was checked after every experiment.

Experimental protocol

The microvascular blood flow was measured continuously. Recordings were made before NPWT (baseline = 0 mmHg) and during exposure to NPWT at −50, −70, −100, −120, −150 and −170 mmHg. Baseline was restored between each pressure setting. The pressures were applied in random order to prevent systematic effects.

Calculations and statistics

Laser Doppler velocimetry measurements were performed on six pigs. The output was recorded continuously using the Transonic[checkregistered] Laser Doppler Monitor. Microvascular blood flow was expressed in terms of perfusion units (PU) in percent change (%) relative to the baseline (100%). Calculations and statistical analysis were performed using GraphPad 5.0 software (San Diego, CA). The Mann–Whitney test was used when comparing two groups. Significance was defined as P < 0·05 (*), P < 0·01 (**), P < 0·001 (***) and P > 0·05 (not significant, n.s.). The values given are the mean of six measurements and the standard error on the mean (SEM).

Results

Microvascular blood flow in the small intestinal loops located apically below the dressing

The microvascular blood flow was measured in four small intestinal loops of the abdomen, apically, immediately below the dressing. The blood flow in the intestinal loop in direct contact with the dressing is shown in Figure 2A. A significant reduction in microvascular blood flow was observed at all pressures between −50 and −170 mmHg. In the intestinal loop lying immediately under the first loop, a slight but significant reduction in blood flow was observed at all pressures between −50 and −170 mmHg. These results are shown in Figure 2B. No change in microvascular blood flow was observed in deeper intestinal loops, as can be seen in Figure 2C,D.

Figure 2.

Figure 2

Microvascular blood flow measured using laser Doppler velocimetry in the small intestinal wall exposed to negative pressure wound therapy (NPWT) between −50 and −170 mmHg in four loops apically below the dressing. The results for the intestinal loop in direct contact with the dressing are shown in (A), where a significant reduction in blood flow can be seen when the negative pressure is applied. The second intestinal loop showed a slight decrease in blood flow (B). The third and fourth intestinal loops (C and D, respectively) showed no change in blood flow. Significance was defined as * P < 0·05, ** P < 0·01, *** P < 0·001 and P > 0·05 (not significant, n.s.). Values are presented as means ± the standard error on the mean (SEM) of six experiments.

Microvascular blood flow in the small intestinal loops located beside the anterior abdominal wall

The microvascular blood flow was measured in four different small intestinal loops located at different depths close to the anterior abdominal wall. The results are shown in Figure 3. A significant reduction in microvascular blood flow was observed at all pressures between −50 and −170 mmHg in the uppermost loop below the dressing (A). A slight, but significant, reduction in blood flow was observed at all pressures between −50 and −170 mmHg in the second loop lying under the first loop (B), while no change in microvascular blood flow was observed in the two lower loops (C and D).

Figure 3.

Figure 3

Microvascular blood flow measured using laser Doppler velocimetry in the small intestinal wall exposed to negative pressure wound therapy (NPWT) between −50 and −170 mmHg in four loops close to the anterior abdominal wall. The results for the intestinal loop under the dressing are shown in (A). Note the significant reduction in blood flow when the negative pressure is applied. The second intestinal loop showed a slight decrease in blood flow (B), while no change was seen in the third and fourth intestinal loops (C and D, respectively). Significance was defined as * P < 0·05, ** P < 0·01, *** P < 0·001 and P > 0·05 (not significant, n.s.). Values are presented as means ± the standard error on the mean (SEM), of six experiments.

Discussion

We have recently shown that application of NPWT in open abdomen in pigs causes a decrease in microvascular blood flow in the wall of the small intestine lying closest to the NPWT dressing (20). We also found that the blood flow could not be restored by inserting layers of paraffin gauze between the intestines and the vacuum source (21). The decrease in blood flow was found to be greater with increasing negative pressure 20, 21. We have also shown that the application of conventional NPWT to the open abdomen of pigs produces areas of petechial bleeding in the small intestinal wall, and that the area of petechial bleeding could be significantly reduced by inserting a protective plastic disc between the intestines and the vacuum source (23). (The areas of petechial bleeding in the small intestinal wall were significantly larger following conventional NPWT after 12, 24 and 48 hours, than when using NPWT with a protective disc between the intestines and the vacuum source.)

The management of the open abdomen in severely injured patients or those with serious intra‐abdominal infections poses a significant challenge to the surgeon, and may include treatment of abdominal compartment syndrome, effects on respiration, cardiovascular and renal function and even ‘damage‐control’ laparotomy. Life‐sustaining emergency surgery in patients with severe abdominal injuries are often accompanied by visceral oedema, retroperitoneal haematoma or packing of the abdominal cavity. The pressure of a forced abdominal wall closure or an abdominal infection may lead to ischaemia and necrosis of the abdominal fascia. The latter may result in abdominal rupture with subsequent development of an abdominal wall hernia 1, 2, 3, 5, 14, 24, 25, 26, 27, 28. With the development of damage‐control techniques and the understanding of abdominal compartment syndrome, the open abdomen has become more commonplace. If the abdomen is not closed in the early postoperative period, the combination of adhesions and fascial retraction frequently makes primary fascial closure impossible, and a planned ventral hernia is often required.

NPWT is one technique that can be used to manage the open abdomen. NPWT has shown a very good drainage effect, facilitating the reduction of peritoneal fluid and bacteria. High closure rates of the abdomen have been reported following NPWT compared with other techniques 4, 14, 15, 18, 28, 29. However, the method has occasionally been associated with increased development of intestinal and enteroatmospheric fistulae 9, 11, 12, 18, 19, 30, 31. The mechanical effects of NPWT may result in ischaemia, which in turn may promote the development of these fistulae.

In this study, we have shown that negative pressures between −50 and −170 mmHg cause a significant decrease in the microvascular blood flow in the intestinal loop lying in direct contact with the visceral protective layer and in the intestinal loop lying beneath this intestinal loop. The decrease in blood flow was significant but considerably less pronounced in the second intestinal loop than that in direct contact with the visceral protective layer, showing that the effect decreases with distance from the negative pressure source. The decrease in microvascular blood flow was also shown to increase with the magnitude of the negative pressure applied. The microvascular blood flow in the intestinal loops lying beneath the two fist loops was not affected by the negative pressure, indicating that the effect is local. The intestinal loops lying even deeper (the third and fourth intestinal loops) in the abdominal cavity were not affected by the negative pressure applied.

The decrease in blood flow was slightly greater in the loops located apically, than in those located at the anterior abdominal wall. This is probably a result of the greater transmission of pressure to the intestinal loops in contact with the visceral protective layer and the foam, as these are closer to the vacuum source than the intestinal loops at the anterior abdominal wall. The negative pressure probably also decreased with increasing distance from the vacuum source. It would have been of interest to measure the pressure gradient at different locations to ascertain whether the different regions were indeed exposed to different negative pressures. However this was not performed in this study.

One can only speculate that reduced blood flow in the intestinal wall over an extended period of time may induce ischaemia and secondary necrosis in the intestinal wall, which could promote the development of intestinal fistulae.

We have previously shown that NPWT induces an increase in the blood flow in the peristernal soft tissue (i.e. skeletal muscular and subcutaneous tissue), and also that the change is local as the blood flow at a distance of 4·5 cm from the wound edge was not affected by the application of negative pressure. The blood flow increased with elevated negative pressure in both subcutaneous and skeletal muscular tissue. When the area under the flow–distance curve was analysed, covering a distance of 0·5–4·5 cm from the wound edge, maximal net increase in blood flow was observed at −75 and −100 mmHg in muscular tissue. A difference in the profiles of the blood flow response was observed between subcutaneous and muscular tissue; the distance from the wound edge to the point at which the blood flow increased was shorter in muscular than in subcutaneous tissue. This may indicate that pressure is transduced differently in soft and dense tissue and that a less dense tissue collapses more easily when pressure is applied. A zone of relative hypoperfusion was observed in the immediate proximity of the wound edge. This zone was larger at higher negative pressures and was especially prominent in subcutaneous tissue. The size of the hypoperfused zone depended on the pressure applied and expanded with increasing negative pressure. In summary, the changes in the peristernal wound blood flow caused by topical negative pressure vary with the distance from the wound edge. A few centimetres away from the wound edge, the blood flow increased when negative pressure was applied. Conversely, in the immediate proximity of the wound, the negative pressure induced relative hypoperfusion (32). Similar physiological changes may also take place in the intestinal wall during exposure to NPWT. However, the increase in blood flow seen in muscular tissue and subcutaneous tissue was not observed in the intestinal loops lying below the loops in which a decrease in blood flow was observed.

Conclusion

The application of negative pressure to the open abdomen causes a significant decrease in blood flow in the uppermost intestinal loops in contact with the visceral protective layer, apically and close to the anterior abdominal wall. Only a slight but significant decrease was seen in the loops below these. No decrease in blood flow was observed in the intestinal loops lying deeper in the abdominal cavity. We suggest that a decreased blood flow in the intestinal wall over a period of time may induce ischaemia and secondary necrosis in the intestinal wall, which could promote the development of intestinal and enteroatmospheric fistulae. It is, however, uncertain what kind of clinical repercussions these findings might have.

Despite these findings, we still believe that NPWT of the open abdomen is a very effective treatment, mainly because of its draining effect, but that it could probably be improved by a better understanding of the mechanisms involved. Inserting a protective disc over the intestines could offer protection from local ischaemia, while still providing effective drainage. Further experimental studies will have to be conducted to confirm this.

Acknowledgement

We would like to thank our funding source Region Skåne.

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