• View in gallery
    Figure 1

    Box-and-whisker plots of the microcirculatory parameters DBS, PVD (mm/m2), PVD-S (mm/m2), PPV (%), and PPV-S (%; A) and MFI and HI (B) obtained with SDF video microscopy of the sublingual microvasculature at 3 time points (T1, T2, and T3) for 9 healthy horses that underwent anesthesia for elective procedures (arthroscopy, n = 3; cutaneous surgery, 3; abdominal hernia surgery, 2; or castration, 1). The horizontal line within each box represents the median, boxes represent the interquartile (25th to 75th percentile) range, and whiskers indicate the maximum and minimum values. Individual data points are outliers. T1 = 30 minutes after anesthesia induction, before the elective procedure was begun. T2 = 45 minutes later, after the skin was incised. T3 = 15 minutes before the end of anesthesia. *Significant (P < 0.05) difference between time points.

  • View in gallery
    Figure 2

    Box-and-whisker plots of the microcirculatory parameters DBS, PVD, PVD-S, PPV, and PPV-S (A) and MFI and HI (B) obtained at 3 time points (T1, T2, and T3) for 8 horses with colic that underwent anesthesia for emergency intestinal surgery (small intestinal volvulus, n = 3; large colon volvulus, 2; large colon displacement, 1; nephrosplenic entrapment, 1; or large colon impaction, 1). See Figure 1 for remainder of key.

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Evaluation of the sublingual microcirculation with sidestream dark field video microscopy in horses anesthetized for an elective procedure or intestinal surgery

Christelle MansourFrom the APCSe Unit UPSP 2016.A101, VetAgro Sup, University of Lyon, 69280 Marcy-l'Étoile, France

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Jerneja SredensekFrom the Anesthesia Service at the Veterinary Campus of Lyon, VetAgro Sup, University of Lyon, 69280 Marcy-l'Étoile, France

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Bruna SantangeloFrom the Anesthesia Service at the Veterinary Campus of Lyon, VetAgro Sup, University of Lyon, 69280 Marcy-l'Étoile, France

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Abstract

OBJECTIVE

To compare the sublingual microcirculation between healthy horses anesthetized for elective procedures and horses with colic anesthetized for abdominal surgery and to determine the effect of mean arterial blood pressure (MAP) on the microcirculation.

ANIMALS

9 horses in the elective group and 8 horses in the colic group.

PROCEDURES

Sublingual microcirculation was assessed with sidestream dark field video microscopy. Videos were captured at 3 time points during anesthesia. Recorded microvasculature parameters were De Backer score (DBS), total density of perfused vessels (PVD) and small vessels (PVD-S), total proportion of perfused vessels (PPV) and small vessels (PPV-S), vascular flow index (MFI), and heterogeneity index (HI). Blood pressure during hypotensive (MAP < 60 mm Hg) and normotensive (MAP ≥ 60 mm Hg) episodes was also recorded.

RESULTS

During normotensive episodes, the elective group had significantly better PPV and PPV-S versus the colic group (median PPV, 76% vs 50%; median PPV-S, 73% vs 51%). In both groups, PPV decreased during anesthesia (elective group, −29%; colic group, −16%) but significantly improved in the elective group 15 minutes before the end of anesthesia (59%). During hypotensive episodes, PVD-S was better preserved in the colic group (11.1 vs 3.8 mm/mm2). No differences were identified for the microcirculatory parameters between normo- and hypotensive episodes in the colic group.

CONCLUSIONS AND CLINICAL RELEVANCE

Sublingual microcirculation was better preserved in healthy horses anesthetized for elective procedures than in horses with colic anesthetized for abdominal surgery despite resuscitation maneuvers. Results indicated that the macrocirculation and microcirculation in critically ill horses may be independent.

Abstract

OBJECTIVE

To compare the sublingual microcirculation between healthy horses anesthetized for elective procedures and horses with colic anesthetized for abdominal surgery and to determine the effect of mean arterial blood pressure (MAP) on the microcirculation.

ANIMALS

9 horses in the elective group and 8 horses in the colic group.

PROCEDURES

Sublingual microcirculation was assessed with sidestream dark field video microscopy. Videos were captured at 3 time points during anesthesia. Recorded microvasculature parameters were De Backer score (DBS), total density of perfused vessels (PVD) and small vessels (PVD-S), total proportion of perfused vessels (PPV) and small vessels (PPV-S), vascular flow index (MFI), and heterogeneity index (HI). Blood pressure during hypotensive (MAP < 60 mm Hg) and normotensive (MAP ≥ 60 mm Hg) episodes was also recorded.

RESULTS

During normotensive episodes, the elective group had significantly better PPV and PPV-S versus the colic group (median PPV, 76% vs 50%; median PPV-S, 73% vs 51%). In both groups, PPV decreased during anesthesia (elective group, −29%; colic group, −16%) but significantly improved in the elective group 15 minutes before the end of anesthesia (59%). During hypotensive episodes, PVD-S was better preserved in the colic group (11.1 vs 3.8 mm/mm2). No differences were identified for the microcirculatory parameters between normo- and hypotensive episodes in the colic group.

CONCLUSIONS AND CLINICAL RELEVANCE

Sublingual microcirculation was better preserved in healthy horses anesthetized for elective procedures than in horses with colic anesthetized for abdominal surgery despite resuscitation maneuvers. Results indicated that the macrocirculation and microcirculation in critically ill horses may be independent.

Introduction

The microcirculation, vessels with diameters of < 100 μm, is the primary site of oxygen and nutrient exchange between blood and tissues.1 A decrease in capillary density or blood flow may increase the diffusion distance for oxygen, leading to organ dys-function.2 The persistence of microcirculatory disorders in critical human patients despite resuscitation maneuvers is associated with a poor outcome.3 This has led to a novel approach that uses microcirculatory parameters in addition to the traditional macrocirculatory parameters to aid in determining the optimal resuscitation maneuvers, in an attempt to improve outcome.4 Similarly, the microcirculation is likely altered in critical equine patients, and the degree to which the altered microcirculation is ameliorated after resuscitation maneuvers may help veterinarians with determining patient prognosis.

Intestinal microcirculatory alterations are reported in horses undergoing colic surgery, compared with healthy horses.5 However, little information is available regarding the evaluation of the sublingual microcirculation, which is easier to assess, in horses, compared with the evaluation of the intestinal microcirculation.6 Acknowledging the severity of the gastrointestinal disorder, better assessment and characterization of the microcirculation in horses presented for colic surgery may help veterinarians improve treatment, prognosis, and outcome.

Often in the perioperative period, HR, blood pressure, and capillary refill time are used as indicators of cardiovascular function. However, these parameters lack specificity with regard to tissue perfusion.7,8 The latter, specifically tissue microcirculation, may be assessed with SDF video microscopy.9 The technique consists of applying a handheld video microscope that has a lens surrounded by LEDs emitting a green light (wavelength, 530 to 550 nm), which is absorbed by hemoglobin in the tissue of interest.10 With video acquisition by the SDF video microscope of the interrogated tissue, the vessels of the tissue appear dark on a light field.11 The SDF video microscope can be applied to any tissue with a thin epithelial layer but is most commonly applied to the sublingual tissue because this tissue is easily accessible.12 Also, the microcirculation of the sublingual tissue may be a reflection of the splanchnic microcirculation, given their shared embryologic origin.13–15,a,b Compared with other reference methods, such as laser Doppler, that are restricted to providing numerical measures of perfusion, SDF video microscopy also permits direct visualization of the microvessels and estimation of vessel density, heterogeneity, and perfusion.9

In horses, SDF video microscopy has been successfully used on the gingival, rectal, and colonic mucosa to assess the microcirculation.16,c In horses with colonic lesions that required surgical intervention, the microcirculatory perfusion parameters obtained through application of an SDF video microscope on the colonic serosa are correlated with colonic mucosal injury scores, such that the microcirculatory perfusion parameters could be used to predict the severity of colonic injury.5 However, SDF video microscopy has some drawbacks. Secretions, blood, movement, and pressure applied by the video microscope on the tissue can result in artifacts. Moreover, assessing the sublingual microcirculation is feasible only in sedated patients and requires training and much time for data interpretation.17 A recent study18 reveals that the probability of obtaining pressure artifacts and thus erroneous results during the video recording of the sublingual microcirculation of piglets was higher when the arterial blood pressure was low.

The primary objective of the study reported here was to compare the sublingual microcirculatory parameters between healthy horses anesthetized for elective procedures and horses with colic anesthetized for abdominal surgery. The secondary objective was to evaluate the influence of MAP on the micro-vasculature of these horses.

Materials and Methods

Animals

Seventeen client-owned horses were included with owner consent. Horses were allocated into 2 groups as follows: colic group (n = 8), in which horses required emergency intestinal surgery (small intestinal volvulus, 3; large colon volvulus, 2; large colon displacement, 1; nephrosplenic entrapment, 1; or large colon impaction, 1), and elective group (9), in which horses were healthy and admitted for elective procedures (arthroscopy, n = 3; cutaneous surgery, 3; abdominal hernia surgery, 2; or castration, 1). This prospective observational nonrandomized study was performed at the Equine Veterinary Hospital of VetAgro Sup (Lyon, France) with the approval of the local ethical committee of VetAgro Sup (protocol No. 1514).

Anesthesia and instrumentation

Each horse in the colic group was premedicated with xylazined (0.4 mg/kg, IV) and morphinee (0.1 mg/kg, IV). Five minutes later, anesthesia was induced with diazepamf (0.05 mg/kg, IV) and ketamineg (2.2 mg/kg, IV). After orotracheal intubation and connection to a large animal rebreathing system, anesthesia was maintained with sevofluraneh in 60% oxygen. After intra-arterial cannulation for MAP measurement and initiation of macrocirculation monitoring, lidocainei (1.5 mg/kg, IV, over 20 minutes) was administered as a bolus and then as a continuous rate infusion (0.05 mg/kg/min, IV).

Each horse in the elective group was premedicated with acepromazinej (0.04 mg/kg, IM) 1 hour prior to induction of anesthesia. Thereafter, xylazined (0.6 mg/kg, IV) and morphinee (0.1 mg/kg, IV) were administered. Anesthesia was then induced 5 minutes later with diazepamf (0.05 mg/kg, IV) and ketamineg (2.2 mg/kg, IV). After orotracheal intubation, each horse was connected to a large animal rebreathing system and anesthesia was maintained with sevofluraneh in 60% oxygen.

Each horse was positioned in dorsal recumbency and mechanically ventilated with a ventilatork initially set at a tidal volume of 8 mL/kg and a respiratory rate of 8 to 10 breaths/min, adjusted thereafter to maintain an end-tidal partial pressure of carbon dioxide between 4.6 and 6.0 kPa (35 and 45 mm Hg). Parameters were continuously monitored with a multi-parameter monitork and were as follows: HR; invasive systolic, diastolic, and mean arterial blood pressures; respiratory rate; end-tidal partial pressure of carbon dioxide; fraction of inspired oxygen; end-tidal sevoflurane concentration; and peripheral hemoglobin oxygen saturation. Arterial blood gas was analyzed every hour. For invasive blood pressure monitoring, the skin over the left or right transverse facial artery was aseptically prepared before cannulation of the artery with a 20-gauge, 32-mm, over-the-needle catheter.l The catheter was connected to a precalibrated electronic pressure transducerm by noncompliant extension lines filled with heparinized saline (0.9% NaCl) solution (10 U/mL). The pressure transducer was positioned and zeroed to atmospheric pressure at the level of the right heart. Once the arterial cannula was in place and connected, a fast-flush test was performed to confirm that 2 oscillations were seen following release of the flush valve (bag pressure at 300 mm Hg) and that a square wave had been generated. At predefined time points, the sublingual micro-circulation was evaluated with a handheld SDF video microscope.n

Anesthetic depth was continuously assessed through the presence of a palpebral reflex response and nystagmus and the position of the eyeballs. Ketamineg (0.5 mg/kg, IV) was administered when anesthetic depth was inadequate, and morphinee (0.1 mg/ kg, IV) was administered intra-operatively 2 hours after the initial dose (premedication dose). Lactated Ringer solution was administered IV at 10 mL/kg/h throughout the anesthetic period. When MAP was between 60 and 70 mm Hg, a continuous rate infusion of dobutamineo was initiated (initial rate, 2 μg/kg/min, IV; then adjusted on the basis of the hemodynamic response).

After general anesthesia was discontinued, each horse was transferred to a padded recovery stall. Xylazined (0.2 to 0.3 mg/kg, IV) was administered when deemed necessary by the anesthetist. The endotracheal tube was removed, and oxygen (15 L/ min) was insufflated through a nasal tube until anesthetic recovery.

Assessment of microcirculation

After gentle removal of saliva from the sublingual area with dry gauze, the lens of the SDF video microscopen was covered with a disposable sterile cap and applied without pressure onto a lateral side of the tongue. As recommended,19 proper application was subjectively assessed by the presence of uncompromised larger venules, ensuring blood flow. Image resolution and light intensity were adjusted on the video microscope to optimize imaging and clarity of vessels. Video sequences of 20 seconds each were recorded at each time point from at least 5 adjacent sublingual sites.

The videos were evaluated later, and the 3 best sequences were selected on the basis of the video quality as determined by agreement between 2 investigators (CM and SAJ). Acceptable videos were those with minimal to no drift, good resolution, appropriate contrast, and absence of pressure artifact. The videos were analyzed with dedicated softwarep that calculated the microcirculatory parameters PPV, PPV-S, PVD, PVD-S, and DBS as previously described.9 Parameters were determined for all interrogated microvessels and categorized by diameter (< 20 μm [PPV-S], ≥ 20 μm, and all sizes). The proportion of perfused microvessels was the percentage of microvessels with continuous RBC transit for at least 20 seconds, indicating the capability of delivering oxygen to the tissues. Representing functional microvessel density, PVD was considered as the main determinant of microvessel blood supply3,9; PVD indicated the diffusional distance and the surface area available for oxygen exchange.8 The DBS was calculated on the basis of microvasculature density and proportion of perfusion.9 Each video image was divided into 4 quadrants, and MFI was qualitatively determined for each quadrant by use of an ordinal scale, with 0 = no flow, 1 = intermittent flow, 2 = sluggish flow, and 3 = normal flow.9 Heterogeneity index was calculated as the difference between the highest and lowest MFI, divided by the mean MFI of all sites at a single time point.9 The microcirculation appears to be improved when DBS, PVD, PPV, and MFI values are increased and HI value is decreased.9

Study design

Video sequences obtained through SDF video microscopy were collected at 3 time points as follows: 30 minutes following anesthetic induction, before beginning the procedure (elective procedure or intestinal surgery); 45 minutes later, after the skin was incised; and 15 minutes before the end of anesthesia. For each time point, HR and MAP were recorded, and a MAP threshold value of 60 mm Hg was chosen to distinguish the effects of hypotension (MAP < 60 mm Hg) and normotension (MAP ≥ 60 mm Hg) on microcirculatory parameters.

Statistical analysis

Statistical analyses were performed with commercially available software.q Data were assessed for normality with the Kolmogorov-Smirnov test. Because most data were not normally distributed, non-parametric statistical tests were performed, and non-normally distributed data were expressed as median and interquartile (25th to 75th percentile) range. The Friedman test was used to detect variations in the microvascular parameters within each time point. A paired t test was performed post hoc with the Nemenyi correction to assess differences among parameters at each time point when the Friedman test indicated a significant difference. The Mann-Whitney U test was used to compare each microcirculatory parameter at each time point between groups. Values of P < 0.05 were considered significant.

Results

No significant differences in age and body weight were noted between horses of the elective group and horses of the colic group. No intra- or postanesthetic death occurred for the horses in the elective group, whereas 2 horses in the colic group were euthanized during anesthesia and 1 died 10 days after surgery.

The macro- and microcirculation parameters for both groups were summarized (Table 1). Median arterial blood pressure was lower in the colic group, compared with the elective group (70 vs 74 mm Hg; P = 0.019); however, MAP remained ≥ 60 mm Hg in both groups. Proportions of perfused microvessels, PPV-S, and DBS were significantly (P < 0.007) higher in the elective group versus the colic group.

Table 1

Median (interquartile [25th to 75th percentile] range) values for 2 macrocirculatory parameters determined with a multiparameter monitor and various microcirculatory parameters determined with SDF video microscopy of the sublingual tissue, during the perianesthetic period for horses with colic that required emergency intestinal surgery (colic group; n = 8) and for healthy horses that had elective procedures performed (elective group; 9).

Parameter Group
Elective Colic
HR (beats/min) 38 (30–40) 35 (30–42)
MAP (mm Hg)* 74 (70–79) 70 (66–75)
DBS* 9.5 (8.1–11) 9 (8.1–10)
PVD (mm/mm2) 10.4 (7.2–16.9) 9.9 (6.2–14.1)
PVD-S (mm/mm2) 8.3 (5.7–14.7) 9 (6–13.2)
PPV (%)* 71.1 (44.7–87.7) 52.7 (36.9–74.5)
PPV-S (%)* 70 (46.2–88.7) 55.7 (37–76.2)
MFI 1.7 (1.5–2) 1.7 (l.5–2)
HI 0.4 (0–0.6) 0 (0–0.5)

Significant (P < 0.05) difference for the parameter between elective and colic groups.

The microcirculatory parameters obtained during anesthesia for each group were displayed graphically (Figures 1 and 2). For the elective group, PVD (–31%) and PVD-S (–26%) were significantly (P < 0.001) decreased at the second time point 75 minutes after anesthesia induction (45 minutes after acquisition of the first data set) and at the third time point 15 minutes before the end of anesthesia (PVD, −42%; PVD-S, −39%; P < 0.001), compared with values at the first time point 30 minutes after anesthetic induction. Significant (P ≤ 0.001) but transient decreases in PPV and PPV-S were noted for the second time point (–29% for both parameters), followed by significant (P < 0.001) increases of these parameters at the third time point (59% for PPV and 49% for PPV-S). For the colic group, a significant (P = 0.04) decrease in PPV (–16%) and a significant (P = 0.04) increase in DBS (10%), compared with the first time point, were detected at the third point. No significant changes were found in MFI and HI during anesthesia for both groups.

Figure 1
Figure 1

Box-and-whisker plots of the microcirculatory parameters DBS, PVD (mm/m2), PVD-S (mm/m2), PPV (%), and PPV-S (%; A) and MFI and HI (B) obtained with SDF video microscopy of the sublingual microvasculature at 3 time points (T1, T2, and T3) for 9 healthy horses that underwent anesthesia for elective procedures (arthroscopy, n = 3; cutaneous surgery, 3; abdominal hernia surgery, 2; or castration, 1). The horizontal line within each box represents the median, boxes represent the interquartile (25th to 75th percentile) range, and whiskers indicate the maximum and minimum values. Individual data points are outliers. T1 = 30 minutes after anesthesia induction, before the elective procedure was begun. T2 = 45 minutes later, after the skin was incised. T3 = 15 minutes before the end of anesthesia. *Significant (P < 0.05) difference between time points.

Citation: American Journal of Veterinary Research 82, 7; 10.2460/ajvr.82.7.574

Figure 2
Figure 2

Box-and-whisker plots of the microcirculatory parameters DBS, PVD, PVD-S, PPV, and PPV-S (A) and MFI and HI (B) obtained at 3 time points (T1, T2, and T3) for 8 horses with colic that underwent anesthesia for emergency intestinal surgery (small intestinal volvulus, n = 3; large colon volvulus, 2; large colon displacement, 1; nephrosplenic entrapment, 1; or large colon impaction, 1). See Figure 1 for remainder of key.

Citation: American Journal of Veterinary Research 82, 7; 10.2460/ajvr.82.7.574

Before the beginning of the procedure (30 minutes after anesthetic induction), median DBS, PVD, PPV, and PPV-S were significantly (P = 0.023) higher in the elective group versus the colic group (DBS, 9.5 vs 8.7; PVD, 13.5 vs 10.1 mm/mm2; PPV, 76% vs 62%; PPV-S, 80% vs 60%; Table 2). At 15 minutes before the end of anesthesia, median PPV and PPV-S were significantly (P = 0.003) higher in the elective than in the control group (PPV, 86% vs 46%; PPV-S, 85% vs 50%).

Table 2

Median (interquartile [25th to 75th percentile] range) values of various microcirculatory parameters obtained with SDF video microscopy of the sublingual microvasculature at 3 time points for the horses of Table 1.

Time point Group DBS PVD (mm/mm2) PVD-S (mm/mm2) PPV (%) PPV-S (%) MFI HI
T1 Elective 9.5 (8.2–10.8)* l3.5 (7.5–22.8)* 9.3 (6.3-l3.5) 76 (56–93)* 80 (55–91)* 1.7 (l.5–2) 0 (0–0.5)
Colic 8.7 (7.7–9.5)* l0.1 (6.7–15.9)* ll.1 (6.2–1s9.5) 62 (44–80)* 60 (45–79)* 2 (1.7–2) 0 (0–0.5)
T2 Elective 9.5 (8.l-11.1) 9.7 (6.3–14.7) 8.3 (5.5–13.3) 54 (35–81) 57 (37–80) 1.7 (1–2) 0.4 (0–0.6)
Colic 9 (8.2–9.9) 9.3 (6.1–15.3) 9.3 (5.6–14) 52 (35–76) 57 (36–78) 1.7 (1–2) 0 (0–0.5)
T3 Elective 9.5 (7.9–11.2) 8.6 (6.8–10.6) 7.8 (6.1–9.6) 86 (43–89)* 85 (46–88)* 1.7 (l.2–1.7) 0.5 (0–0.6)
Colic 9.6 (8–10.4) 8.9 (6.1–12.2) 8.4 (6–11.2) 46 (29–65)* 50 (29–67)* 1.7 (1.5–2) 0.5 (0–0.5)

T1 = 30 minutes after anesthesia induction, before the elective procedure was begun. T2 = 45 minutes later, after the skin was incised. T3 = l5 minutes before the end of anesthesia.

During normotensive episodes, horses in the elective group had significantly higher PPV (median, 76% vs 50%; P < 0.001) and PPV-S (73% vs 51%; P = 0.001), compared with the colic group (Table 3). During hypotensive episodes, horses in the colic group had significantly (P = 0.016) higher PVD-S (11.1 mm/mm2), compared with the elective group (3.8 mm/mm2). De Backer score and PVD-S were significantly higher in the elective group during normotensive versus hypotensive episodes (DBS, 9.5 vs 8.2 [P = 0.026]; PVD-S, 8.6 vs 3.8 mm/mm2 [P = 0.011]). No differences were identified for any microcircula-tory parameter between normo- and hypotensive episodes in the colic group.

Table 3

Median (interquartile [25th to 75th percentile] range) values of various microcirculatory parameters obtained with SDF video microscopy of the sublingual microvasculature during episodes of normotension (MAP ≥ 60 mm Hg) and hypotension (MAP < 60 mm Hg) in the horses of Table 1.

MAP Group DBS PVD (mm/mm2) PVD-S (mm/mm2) PPV (%) PPV-S (%) MFI H
Normotension Elective 9.5 (8.1–11.4) 10.8 (7.4–15.7) 8.6 (6.1–13.7) 76 (40–89)* 73 (42–88)* 1.7 (1.2–2) 0.5 (0–0.6)
Colic 9.2 (8.2–10.1) 9.9 (7–15.8) 9.3 (6.8–13.5) 50 (37–62)* 51 (38–68)* 1.7 (1.7–2) 0 (0–0.5)
Hypotension Elective 8.2 (6.5–9.7) 7.3 (4.2–11.9) 3.8 (3.4–7.5)* 81 (56–92) 84 (54–89) 2 (0.9–2) 0.4 (0–1.1)
Colic 9.7 (8.6–10.2) 11.3 (6.1–16.1) 11.1 (6.1–14.1)* 61 (40–82) 62 (41–87) 1.7 (1.4–2) 0.5 (0–0.7)

Significant (P < 0.05) difference for the parameter between normotensive and hypotensive episodes within a group.

See Table 1 for remainder of key.

Discussion

The present study aimed to evaluate the influence of health status and MAP on the microcirculation in anesthetized horses. The main findings were that microcirculation parameters were better maintained throughout anesthesia in horses in the elective group, compared with those in the colic group. During hypotensive episodes, microcirculatory parameters did not differ between groups, except for PVD-S, which was higher in the colic group. Furthermore, no differences in the microcirculatory parameters were detected in the colic group between normotensive and hypotensive episodes.

The microcirculation has been increasingly studied in human medicine over the past decade concurrent with the development of SDF video microscopy. Similar to the case in people, macrocirculatory parameters are poor indicators of microcirculation dysfunction in animals, especially for patients in critical condition when macrocirculatory parameters may be preserved at the expense of the microcirculation.20 Few studies13,14,20–22,a,b in veterinary medicine include the use of SDF video microscopy. An SDF video microscope that is applied to the colonic serosa of horses with gastrointestinal disease successfully quantifies microvascular perfusion parameters, which may be useful indicators of pathological changes to the colon and its viability. Moreover, SDF video microscopy offers an objective assessment of intestinal health. However, applying the video microscope directly onto the intestinal serosa is cumbersome, whereas applying it directly to the sublingual tissue is easier. Additionally, the health of the sublingual microcirculation may reflect the health of the intestinal microcirculation.15

Overall in the present study, horses in the colic group had significantly lower microcirculatory parameters during anesthesia versus horses in the elective group. Because these horses with intestinal disease that required immediate (emergency) intervention were often hemodynamically unstable, these results were expected. Horses with colic are likely to present with microcirculation disorders because of inflammation, increased intra-abdominal pressure with associated altered splanchnic perfusion, and decreased venous return and cardiac output.23–25 Although a significant difference in MAP was found between the colic and elective groups in the present study, MAP in the colic group remained > 60 mm Hg. Thus, the microcirculatory parameters for horses in the colic group were altered despite normal hemodynamic parameters, including MAP. Nevertheless, normal hemodynamic parameters may not precisely reflect any microcirculation variations that occur during anesthesia.

Hemodynamic coherence, defined as the condition in which improvement in macrocirculatory and microcirculatory parameters is parallel, may be lost in critical conditions, and resuscitation maneuvers based on the macrocirculatory parameters may fail to maintain the microcirculation.26 Subsequent analyses of the microcirculatory parameters after the start of or during the intestinal surgery or elective procedure revealed a decrease in microcirculatory parameters. These microcirculatory disturbances in the horses in the elective group could be related to the hemodynamic effects of the anesthetic drugs, positioning of the horses in dorsal recumbency, and ventilation of the horses by mechanical means. The improvement of microcirculatory perfusion parameters in the elective group 15 minutes before the end of anesthesia may have been related to less stimulation of the sympathetic nervous system (vs during surgery) and decreased depth of anesthesia, although this supposition remains difficult to demonstrate. In contrast, horses of the colic group had significant deterioration in the microcirculatory parameters that persisted until 15 minutes before the end of anesthesia. Considering that the abdominal wall was incised and intra-abdominal pressure may have then decreased, improvement in the intestinal microcirculation may have been expected. The persistence of microcirculatory alterations was consistent with the loss of hemodynamic coherence.15 Regarding the relationship between MAP and the microcirculation, the present study showed better microcirculatory perfusion during normotensive episodes, compared with hypotensive episodes, in the elective group, whereas no difference was found in microcirculatory perfusion between normotensive and hypotensive episodes in the colic group. Results from the colic group were consistent with those of previous studies7,17 that indicate specific treatment to improve the macrocirculation, namely to maintain normal systemic blood pressure, is not able to improve the microcirculation. The selection of an MAP threshold of 60 mm Hg to differentiate normotensive and hypotensive episodes in both groups of the present study was arbitrary. Studies of horses27 and pigs28 reveal that tissue perfusion and oxygenation may be preserved during anesthesia when MAP is approximately 60 mm Hg; however, interindividual variability in microvascular responses should be considered, and MAP threshold may need to be adapted to each patient.29

Unexpectedly, PVD-S was greater during hypotensive episodes in the colic group, compared with the elective group, whereas no significant differences were found for the other microcirculatory parameters. This result might be explained by the loss of hemodynamic coherence or the IV administration of lidocaine in the colic group; lidocaine has vasodilatory properties and may influence capillary recruitment.30

The present study had several limitations. First, the inclusion of only a small number of horses and, for the colic group, of horses that had variable duration and severity of intestinal obstructions and underwent various types of surgeries may have led to an underpowered study. Second, both groups of horses were anesthetized with different anesthetic protocols, including acepromazine in the elective group and lidocaine in the colic group. The effect of acepromazine and IV administered lidocaine on the microcirculation is unknown. However, the objective of the present study was to evaluate changes in the sublingual microcirculation of horses in a clinical setting; therefore, implementing a standardized anesthetic protocol was difficult, especially considering the variable health statuses among horses. Third, monitored parameters of macrocirculation did not include those of cardiac output (eg, oxygen delivery and consumption), which may have helped to better understand the observed cardiovascular changes. Lastly, the intestinal microcirculation was not directly assessed but rather only the sublingual microcirculation was assessed. Results of some studies indicate a good correlation between the sublingual and intestinal microcirculation in people31 and horses,6 whereas other studies12 indicate that the sublingual and intestinal microcirculation are independent. However, this study was primarily observational and did not aim to compare the microcirculation of both sites.

In summary, the results of the present study indicated that the sublingual microcirculation as assessed by SDF video microscopy was better maintained in horses anesthetized for elective procedures versus horses anesthetized for intestinal surgery because of colic. Mean arterial blood pressure and microvascular changes appeared independent, which suggested that monitoring of only MAP may be insufficient to reflect the microcirculation before and after resuscitation. Results need to be confirmed with study of a larger number of horses, the type of intestinal disease and degree of hemodynamic compromise need to be considered, and whether microvasculature health could be used to help determine the prognosis of horses with colic needs to be evaluated.

Acknowledgments

Funded by the Veterinary Campus at Lyon, VetAgro Sup, University of Lyon, and Faculty of Agronomy and Veterinary Medicine, Lebanese University. Dr. Mansour has received travel grants from the Faculty of Agronomy and Veterinary Medicine, Lebanese University, for presentations related to microcirculation in horses. Funding sources did not have any involvement in the data analysis and interpretation or writing and publication of the manuscript. The authors declare that there were no other conflicts of interest.

Abbreviations

DBS

De Backer score

HI

Heterogeneity index

HR

Heart rate

MAP

Mean arterial blood pressure

MFI

Microvascular flow index

PPV

Proportion of perfused vessels

PPV-S

Proportion of perfused small vessels

PVD

Perfused vascular density

PVD-S

Perfused vascular density of small vessels

SDF

Sidestream dark field

Footnotes

a.

Londoño LA, Bowen CM, Buckley GJ. Evaluation of the endothelial glycocalyx in healthy anesthetized dogs using rapid, patient-side GlycoCheck analysis software (abstr), in Proceedings. Int Vet Emerg Crit Care Symp 2018;S7:28.

b.

Millar KK, Londoño LA, Monday JS. Evaluation of the endothelial glycocalyx in healthy anesthetized cats using rapid, patient-side Glycocheck analysis software (abstr), in Proceedings. Int Vet Emerg Crit Care Symp 2019;29:S11.

c.

Hallowell GD, Lethbridge K, Croxford A, et al. Assessment and reliability of measuring microvascular perfusion in normal adult conscious horses (abstr). J Vet Intern Med 2013;27:648–649.

d.

Rompun, Bayer GmbH, Leverkusen, Germany.

e.

Morphine chlorhydrate Aguettant, Aguettant, France.

f.

Diazepam TVM 5 mg/mL, TVM France, Lempdes, France.

g.

Imalgene 1000, Boehringer-Ingelheim Animal Health France, Lyon, France.

h.

Sevoflo, Zoetis, Lyon, France.

i.

Lurocaïne, Vetoquinol SA, Lure Cedex, France.

j.

Calmivet solution for injection, Vetoquinol, Paris, France.

k.

Tafonius, Vetronic Services Ltd, Abbotskerswell, England.

l.

Introcan Safety, B Braun Medical, Saint-Cloud, France.

m.

TruWave, Edwards Lifesciences SAS, Guyancourt, France.

n.

Microscan, Microvision Medical, Amsterdam, Netherlands.

o.

Dobutamine Aguettant, Aguettant, Lyon, France.

p.

AVA, version 4.3, Microvision Medical, Amsterdam, Netherlands.

q.

MedCalc software, version 12.1.4.0, Mariakerke, Belgium.

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Contributor Notes

Address correspondence to Dr. Mansour (christelle-mansour@hotmail.com).