Introduction
An ideal incisional closure device provides effective skin apposition, ease of application, and good cosmesis and has a low rate of complications.1–4 This concept applies to closure of equine ventral midline celiotomies, in which documented incisional complications include peri-incisional edema, incisional drainage, local incisional infection, hernia formation, and incisional dehiscence,5–10 all of which can be associated with prolonged recoveries, increased costs, and loss of performance.11–13 Historically, ventral midline incisions in horses have been closed by use of skin suture or skin staples.14–16 Absorbable suture has several advantages, including easy handling and tissue glide, minimal reactivity, and lack of the need for removal.17 However, skin sutures have been observed to cause local irritation and pain associated with closure and healing.3,18,19 A major disadvantage of percutaneous suture documented in humans is the potential for bacterial translocation into the subcutaneous tissue through skin punctures leading to incisional drainage, infection, and delayed healing.3,18–20 Multiple skin penetrations during closure causes localized trauma and focal ischemia at the wound edge from vascular compromise upon tightening of the suture line.19,20 Alternative methods of skin closure utilized in veterinary medicine include skin staples or cyanoacrylate tissue adhesive, both of which are considered acceptable methods of closure in comparison to suture.21–24 Although the use of staples for skin closure is significantly faster than suture, staples are shown to have a 3.85-fold higher risk of developing an incisional infection compared to sutured closure in horses.7,16 Complications associated with cyanoacrylate tissue adhesive include incisional infection and herniation but are not different from those of skin staples.22
Recently, newer skin closure methods have emerged in human medicine with benefits that could translate to veterinary medicine. This zip skin closure system (ZSCS) is a nontraumatic adhesive device that allows for reduced closure time, increased efficiency, and optimal tension and alignment.1–4,18,19,25–28 The device uses an adhesive hydrocolloid that attaches to intact skin adjacent to the wound.18 Microadjustable zip straps then allow for approximation of the wound edges for force-distributed low-tension closure.18 The integrated structure allows for mobility during flexion and extension of high-motion areas, making its use desirable.28 Numerous reports detail the benefits in people undergoing knee arthroplasty, with very few complications reported.1,2,4,18,19,26,27 Complications with the ZSCS in humans include skin discoloration, epidermolysis, device exfoliation, skin blistering, and mild allergic reaction.2,4,27 Limited reports investigating the ZSCS in veterinary medicine have shown significantly better holding strength than conventional sutures and effective appositional healing.3,25 Decreased infection rate was also seen in a guinea pig model comparing the ZSCS to suture.29 A clinical study in dogs using the ZSCS resulted in localized erythema and erosive dermatitis at the adhesion site in all patients with the ZSCS; histologic assessment was not performed, and a cause for the reaction was not identified.3 To date, the use of the ZSCS for skin closure has not been evaluated in horses.
The objective of this study was to assess the healing of a split-scar model of equine ventral midline celiotomy incisions by comparing the ZSCS with a simple continuous sutured skin closure, assess the closure time of each technique, and characterize any potential adverse cutaneous reactions associated with the ZSCS by use of gross and histologic assessment. We hypothesized that skin closure with the ZSCS would result in faster closure time, improved short-term visual healing scores, and superior histopathologic healing score compared to sutured skin closure.
Materials and Methods
Animals
Eight adult horses (> 1 year of age) were used in accordance with the University of Pennsylvania’s Institutional Animal Care and Use Committee guidelines (protocol No. 806545). The Institutional Animal Care and Use Committee reviewed and approved this study as part of a larger proposal in which horses would be subsequently enrolled into a separate project investigating small intestinal resection and anastomosis following final sample and data collection. Humane end points were predefined as part of the study protocol and included surgical dehiscence or uncontrollable abdominal pain. Efforts to minimize suffering and distress included the use of analgesics (flunixin meglumine) as part of the perioperative protocol. Research staff responsible for animal care and handling were all licensed veterinarians and veterinary nurses.
All horses were determined to be healthy for general anesthesia and surgery on the basis of physical examination and historical data. The skin on the ventral midline was also visually and palpably evaluated for evidence of prior surgery (scar or thickening). Horses were housed in temperature-controlled (25 °C) indoor stalls, and food was withheld 12 hours before surgery and water withheld 6 hours before surgery.
Preoperative preparation and anesthesia
A 14-gauge catheter was aseptically placed in the left jugular vein, and horses were administered flunixin meglumine (1.1 mg/kg, IV), procaine penicillin G (22,000 IU/kg, IM), and gentamicin sulfate (6.6 mg/kg, IV). Horses were premedicated with acepromazine (0.05 mg/kg, IV) and xylazine (0.8 mg/kg, IV) and induced under general anesthesia with midazolam (0.05 mg/kg, IV) and ketamine (2.2 mg/kg, IV). Anesthesia was maintained by use of desflurane and oxygen with an end-tidal inhalant concentration targeted of 8% volume. Intravenous balanced isotonic crystalloid solution was administered (5 mL/kg/h) for the duration of the procedure. All horses were instrumented for invasive blood pressure monitoring and cardiac output monitoring by thermodilution with a Swan-Ganz catheter. Pressure support was achieved with dobutamine as a continuous rate infusion as needed to maintain a mean arterial blood pressure above 70 mm Hg.
Part 1: initial celiotomy
Horses were placed in dorsal recumbency for an exploratory celiotomy. The ventral abdomen was clipped by use of a standard No. 40 clipper blade (Andis Co). Next, a specialized manufacturer clipper with disposable blade (CareFusion; Becton, Dickinson and Co) was used along the ventral midline skin to achieve an ultrafine clip to the skin surface. The abdomen was aseptically prepared with 4% chlorhexidine surgical scrub followed by 70% isopropyl alcohol. The abdomen was draped, and a sterile adhesive iodine-impregnated drape (Ioban 2 incise drape; 3M) was placed along the ventral midline.
By use of a sterilized metal ruler, a 30-cm ventral midline skin incision was made with a No. 10 scalpel blade beginning slightly cranial to the umbilicus and extending cranially. The incision was continued through the subcutaneous tissue. Mosquito hemostats were applied to subcuticular bleeding vessels until hemostasis was achieved. A second No. 10 scalpel was used to incise the linea alba the length of the incision. A routine abdominal exploratory followed, including an end-to-end handsewn jejunojejunostomy that was performed as part of a separate research study.
The linea alba was routinely closed with USP size 2 (metric size 5) on a 65-mm half-circle taper needle in a simple continuous pattern with polyglactin 910 (Vicryl; Ethicon Inc) with a tissue bite size of 15 mm and 15-mm intervals between bites.30 The subcutaneous tissue was routinely closed with USP size 2-0 (metric size 3) on a 36-mm half-circle reverse cutting needle in a simple continuous pattern with polyglactin 910 (Vicryl; Ethicon Inc).5
Skin closure
Skin closure was completed by a single nonblinded surgeon (SDH) for both closure methods. The 30-cm incision was divided into cranial and caudal halves such that each horse received both skin closure treatments. The closure method (treatment) for the cranial half was randomly assigned (ZSCS or suture) by use of a random number generator (www.random.org; Randomness and Integrity Services Ltd), with the caudal half closed with the other technique. Prior to closure, the adhesive drape was removed and the incision edges were thoroughly wiped with dry sterile gauze. To remove residual adhesive, isopropyl alcohol–soaked sterile gauze was applied to the skin, avoiding the wound edges, and then thoroughly dried (Figure 1).
Representative gross images of incision sites. A and B—At surgery, representative high-resolution images of linea alba and subcutaneous incision closure prior to zip skin closure system (ZSCS) application (A) and following ZSCS application (B). C —Both cranial and caudal portions of the incisional closure in the immediate postoperative period.
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
Representative gross images of incision sites. A and B—At surgery, representative high-resolution images of linea alba and subcutaneous incision closure prior to zip skin closure system (ZSCS) application (A) and following ZSCS application (B). C —Both cranial and caudal portions of the incisional closure in the immediate postoperative period.
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
Representative gross images of incision sites. A and B—At surgery, representative high-resolution images of linea alba and subcutaneous incision closure prior to zip skin closure system (ZSCS) application (A) and following ZSCS application (B). C —Both cranial and caudal portions of the incisional closure in the immediate postoperative period.
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
For ZSCS skin closure, a Zip-16 surgical skin closure device (Stryker) was used. Dry sterile gauze swabs were folded into thirds to cover the skin incision line before an adhesive spray (Adapt; Hollister Inc) was applied to the skin directly adjacent to the incision line along its length. The ZSCS was then applied by firmly pressing it to the region of skin coated by the adhesive and tightening the microadjustable zip straps to achieve visible apposition of the skin edges (Figure 1).
For sutured skin closure, USP size 2-0 (metric size 3) poliglecaprone 25 (Monocryl; Ethicon Inc) on a 36-mm half-circle reverse cutting needle was used in a full-thickness simple continuous pattern with sutured bites 3 to 4 mm from the wound edge and 3 to 5 mm apart (Figure 1).
After complete closure of the cutaneous incision (suture and ZSCS), a sterile bandage stent comprising a sterile nonadherent dressing (Kerlix; Covidien) backed by a sterile blue towel was applied. The stent was secured in place by use of 3 equidistant cruciate sutures by use of USP size 2 (metric size 5) polypropylene (Surgipro; Covidien) on a 75-mm, three-eighths–circle reverse cutting needle through the skin approximately 3 to 4 cm from the incision edge.
Finally, to serve as a control for histologic assessment of healing, an 8-mm-diameter full-thickness circular (ie, punch) biopsy (8-mm disposable biopsy punch; Integra Inc) was obtained from the ventral abdominal skin of each horse, 3 cm abaxial from the midpoint of the celiotomy incision, and placed in neutral-buffered 10% formalin. A single cruciate suture was placed to close the biopsy site with USP size 2-0 (metric size 3) polyglactin 910 (Vicryl; Ethicon Inc) on a 36-mm half-circle reverse cutting needle. Horses were then moved to a padded stall for recovery from anesthesia and assisted to stand with head and tail ropes. Recovery was subjectively judged by a board-certified anesthesiologist (KH) as good (1 or 2 attempts to stand), fair (> 2 coordinated attempts to stand), or poor (multiple attempts to stand with uncoordinated or frantic activity).
The time taken to close each half of the incision was recorded. For sutured closure, the time recorded was time of first passage of the needle to cutting of the final knot suture ends. For the ZSCS, the time taken was from removal of the plastic backing from the device to tightening of the last cable.
Postoperative care
Postoperatively, horses were treated with postoperative antimicrobials (procaine penicillin G, 22,000 IU/kg, IM, q 12 h; gentamicin sulfate, 6.6 mg/kg, IV, q 24 h for 3 days; and flunixin meglumine, 1.1 mg/kg, IV, q 12 h for 3 days) and were gradually refed over 3 to 5 days. Animal health and behavior were monitored in the intensive care unit on the basis of recommendations by the attending licensed veterinarian. Complete physical examinations (heart rate, respiratory rate, temperature, borborygmi, mucous membrane color, capillary refill time, manure output, and subjective assessment of pain) were performed every 6 hours for the first 3 days postoperatively, then every 12 hours thereafter. The bandage stent was removed 24 hours postoperation, and a reusable abdominal support wrap (Sta-Put; Equus Therapeutics Inc) with a sterile nonadherent padding (SteriRoll 14 X 48 inch; Franklin-Williams Co) was placed directly on the incision. This bandage was changed daily for 4 days. On day 5 postoperatively, the abdominal bandage was removed and the incision was left exposed to the ambient stall environment (indoor, covered, 12 X 12 feet, and containing straw bedding). The incision was evaluated daily by the attending licensed veterinarian for evidence of complications (pain on palpation, peri-incisional swelling, incisional drainage, incisional infection, or skin dehiscence) through visual inspection and palpation.
Part 2: repeat celiotomy
Horses were anesthetized in a manner similar to that described above and placed into dorsal recumbency. After removing the ZSCS manually, the incision was aseptically prepared with 4% chlorhexidine gluconate scrub and 70% isopropyl alcohol. The incision was dried with sterile gauze, and photograph images were obtained of the complete incision, as well as each sutured and ZSCS sections individually.
Incisional assessment at 14 days
The incisions were then inspected by the surgeon (SDH) for evidence of gapping by attempting to digitally distract the wound edges from one another the entire length. Incisional scars were palpated for pliability and assigned a score of 0 (normal), 1 (barely palpable), 2 (firm but yielding), or 3 (hard) by 2 observers (SDH and CEK). Height of the incisional scar was assessed and scored as flat, slightly raised (1 to 3 mm), or raised (≥ 4 mm). Incisional or peri-incisional edema for both skin closure regions was subjectively scored as absent (score 0), mild (score 1), moderate (score 2), or severe (score 3). Finally, an 8-mm full-thickness skin biopsy was taken at the midpoint of both the sutured and ZSCS segments of the incision and placed in neutral-buffered 10% formalin. Horses were then enrolled into part 2 of a separate intestinal anastomosis study.
Based on previous human scar scoring criteria,31–37 an equine celiotomy incision score (ECIS) was created (Table 1). The factors evaluated were assessed by both palpation of the incision line at 14 days and visual inspection of high-resolution photography (iPhone X; Apple Inc). The factors included pigmentation (darkening discoloration of the skin compared to the surrounding tissue), pliability (suppleness of the scar), height, distortion (alteration of the original shape), and surface finish (matte or shiny). Two reviewers, who were blinded to each other’s scores at the time of evaluation, independently assigned each incision a cranial score and caudal score to represent the 2 closure methods.
Equine celiotomy incision score.
| Numerical score/category | 0 | 1 | 2 | 3 |
|---|---|---|---|---|
| Pigmentation | Normal | Hypopigmentation | Hyperpigmentation | N/A |
| Pliability | Normal | Barely palpable | Firm but yielding | Hard |
| Height | Flat | Slightly raised (1–3 mm) | Raised (≥ 4 mm) | N/A |
| Distortion | None | Mild | Moderate | Severe |
| Surface finish | Matte/normal | N/A | Shiny | N/A |
Histopathology
After fixation, the 3 skin biopsies from each horse (normal, ZSCS, and suture treatments) were hemisectioned and embedded in a plane oriented orthogonal to the incision line so that the epidermis and deep dermis flanking both sides of the incision line were incorporated into each hemisection. Tissues were routinely processed, sectioned, histochemically stained, and evaluated by use of brightfield microscopy by a board-certified pathologist (JBE) who was blinded to the samples. Based on histologic features identified in this equine model that were not wholly incorporated by previous reports of human29 and animal37,38 studies of wound healing, a novel semiquantitative histopathologic scoring system (Supplementary Table S1) was created. Hematoxylin and eosin stains evaluated overall tissue architecture, including bridging of the incision site by granulation tissue and presence and type of cellular inflammation; phosphotungstic acid hematoxylin stains evaluated ongoing fibrin deposition; pirosirius red stains evaluated collagen deposition and organization; and Gram stains characterized bacteria. Each biopsy of normal skin was used as an internal control of each horse to compare normal architecture and dermal collagen density (Figure 2) with biopsies from each treatment site and to rule out the presence of underlying subclinical dermatitis or dermatosis. Neovascularization within healing granulation tissue beds was assessed with polyclonal factor VIII (von Willebrand factor) immunohistochemical antibody (Dako; Agilent Technologies Inc) at a 1:1,000 dilution with a heat-induced enzyme retrieval pretreatment at a pH of 6.0 and an intelliPATH autostainer (Biocare Medical LLC) to calculate the number of endothelial-lined channels (ie, blood vessels) per unit area of dermis in normal skin to compare partially healed incisions closed with the ZSCS versus suture closure methods (Supplementary Table S2). For each representative treatment site, factor VIII–positive blood vessels were manually counted and normalized to a unit area of scar tissue present within a 10X magnification field centered on the superficial to mid dermis measured from images obtained with a DP27 digital camera (Olympus Corp) mounted on a BX46 microscope (Olympus Corp) with imaging software (cellSens version 3.1; Olympus Corp). A comparable unit area of normal skin normalized for each horse was found by calculating the average unit areas of incisional scar tissue measured from the ZSCS and suture treatment sites at 10X magnification fields as described above. Factor VIII–positive dermal blood vessels present within the comparable unit area of normal superficial and mid-dermis (Supplementary Table S2) were used as a baseline value for statistical comparisons between each treatment group.
Histology of normal skin biopsy site. H&E- (A and B) and polarized pirosirius red (PSR)–stained (C) photomicrographs of normal skin adjacent to the ventral abdominal surgical incision (horse 7). A—Low-magnification (2X) image shows an intact epidermis and dermal adnexae with fine collagen fibers in the superficial dermis that transition to coarse collagen fibers within the mid to deep dermis. B and C—High-magnification (10X) images of framed area (A) shows an epidermis (e) composed of few (4 to 6) layers of stratified epithelium 20 to 40 μm thick and adnexae extending from the superficial (sd) to mid (md) dermis comprising hair follicles (asterisks) with adjacent sebaceous glands, erector pili muscles, and apocrine glands; the PSR stain highlights the densely packed, organized arrangement and stratification of bright yellow, refractile collagen fibers. Scale bars = 500 μm (A) and 100 μm (B and C).
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
Histology of normal skin biopsy site. H&E- (A and B) and polarized pirosirius red (PSR)–stained (C) photomicrographs of normal skin adjacent to the ventral abdominal surgical incision (horse 7). A—Low-magnification (2X) image shows an intact epidermis and dermal adnexae with fine collagen fibers in the superficial dermis that transition to coarse collagen fibers within the mid to deep dermis. B and C—High-magnification (10X) images of framed area (A) shows an epidermis (e) composed of few (4 to 6) layers of stratified epithelium 20 to 40 μm thick and adnexae extending from the superficial (sd) to mid (md) dermis comprising hair follicles (asterisks) with adjacent sebaceous glands, erector pili muscles, and apocrine glands; the PSR stain highlights the densely packed, organized arrangement and stratification of bright yellow, refractile collagen fibers. Scale bars = 500 μm (A) and 100 μm (B and C).
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
Histology of normal skin biopsy site. H&E- (A and B) and polarized pirosirius red (PSR)–stained (C) photomicrographs of normal skin adjacent to the ventral abdominal surgical incision (horse 7). A—Low-magnification (2X) image shows an intact epidermis and dermal adnexae with fine collagen fibers in the superficial dermis that transition to coarse collagen fibers within the mid to deep dermis. B and C—High-magnification (10X) images of framed area (A) shows an epidermis (e) composed of few (4 to 6) layers of stratified epithelium 20 to 40 μm thick and adnexae extending from the superficial (sd) to mid (md) dermis comprising hair follicles (asterisks) with adjacent sebaceous glands, erector pili muscles, and apocrine glands; the PSR stain highlights the densely packed, organized arrangement and stratification of bright yellow, refractile collagen fibers. Scale bars = 500 μm (A) and 100 μm (B and C).
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
Statistical analysis
Data analysis was performed with commercial software (Excel; Microsoft Corp; Prism version 8; GraphPad Software). Continuous data were assessed for normality with a Shapiro-Wilk test. Parametric data are expressed as mean ± SD and nonparametric as median (range). Differences in skin closure time between methods overall (ZSCS vs suture) and between cranial and caudal halves were evaluated with a Student t test or Mann-Whitney U test. Differences in closure time within horse was evaluated with a paired t test. Differences in mean ECIS and edema score between closure methods were evaluated with a Student t test.
Interobserver ECIS agreement (overall and for each skin closure method) was assessed with weighted kappa (κ) statistics and intraclass coefficient (ICC) with 95% CI. Differences in histopathologic scores were compared with a Student t test or Mann-Whitney U test (ZSCS vs suture) and Kruskal-Wallis test with Dunn testing for comparison between both skin closure methods and control samples. A value of P < 0.05 was significant.
Results
Animals
There were 3 geldings and 5 mares. All 8 horses were Thoroughbreds. Median age was 14 years (range, 5 to 21 years). Median weight was 511 kg (range, 486 to 568 kg). All horses completed the study protocol and were judged to have good equine recovery scores from general anesthesia.
Skin closure
In 4 horses, the ZSCS was applied on the cranial half of the incision, with the ZSCS being applied to the caudal half of the incision in the remaining 4 horses. Skin closure was significantly faster when the ZSCS was used (44 ± 13 seconds), compared to conventional suture (173 ± 18 seconds; P < 0.001). When assessed within horse, the ZSCS was significantly faster to close the skin than suture (P < 0.001). In 2 horses, cyanoacrylate glue was required to improve adhesion of the ZSCS hydrocolloid to intact skin due to persistent skin bleeding that hindered adhesion focally. The time required to apply the cyanoacrylate glue was not recorded.
Gross appearance and scoring
No major incisional complications were observed with the ZSCS. Median peri-incisional edema scores were 1 (range, 1 to 2) and 2 (range, 1 to 3) for ZSCS and sutured skin, respectively (P = 0.88). Complications associated with sutured closure included 1 horse that had suppuration associated with the sutured portion at the cranial aspect of the incision first noted at 11 days postoperatively and 1 horse with partial skin suture dehiscence at the cranial edge of the sutured incision observed at 4 days postoperatively.
The mean ECIS was significantly lower for ZSCS (4.1 ± 2.4) compared to sutured skin (7.5 ± 1.6; P = 0.005). Mean scores were not different between cranial (5.7 ± 2.9) and caudal (6.1 ± 2.3) for each skin closure method (P = 0.79). When height was excluded as a parameter due to the nature of suturing raising the skin edges, the mean ECISs were lower for ZSCS (2.5 ± 2.1) compared to sutured skin (5.9 ± 1.2; P = 0.005) and mean scores were not different between cranial (3.4 ± 2.5) and caudal (4.4 ± 2.0) when height was not included in ECIS scoring (P = 0.65).
There was good to excellent agreement in ECIS between 2 observers (interobserver κ = 0.85, agreement of 87.5%, and ICC = 0.99 [0.97 to 0.99]) for overall scores (cranial and caudal combined). For all ZSCS scores, the agreement was κ = 0.87 and ICC (average) of 0.98 (0.98 to 0.99), and for sutured scores, the agreement was κ = 0.76 and ICC (average) of 0.99 (0.95 to 0.998).
Histopathology
Mean total histopathologic healing scores between ZSCS (4.1 ± 2.6) and suture closure (5.6 ± 3.4) techniques were not different (P = 0.34), correlating with gross healing assessments (Figure 3).
Correlation between gross and histologic healing for ZSCS (A through D) and suture (E through F) closure techniques. A—Gross appearance of healing within the caudal portion of the surgical incision closed with ZSCS (below the arrowhead) in horse 3 correlates with histologic healing from the same site. B—Low-magnification (2X) photomicrograph shows the incisional edges are completely spanned by well-organized granulation tissue (double-headed arrows) extending through all dermal layers without inflammatory or necrotic foci. C and D—H&E- (C) and polarized PSR–stained (D), high-magnification photomicrographs of the incisional scar in panel B show an intact, moderately acanthotic epidermis (e) overlying a collagen-rich scar (double-headed arrows) flanked by normal dermal collagen (dc) and adnexal units (asterisks). E—Gross appearance of healing within the caudal portion of the surgical incision closed with suture (below the arrowhead) in horse 5 correlates with histologic healing from the same site. F—Low-magnification photomicrograph shows complete spanning of the incision by slightly wider seam of well-organized granulation tissue (double-headed arrows) adjacent to a depressed surface (large arrowheads) with mildly inflamed intradermal clefts (small arrowheads) associated with cutaneous sutures. G and H—H&E (G) and polarized PSR–stained (H), high-magnification photomicrographs of the incisional scar in panel F also show similar healing as the ZSCS with an intact, moderately acanthotic epidermis (e) overlying a collagen-rich scar flanked by normal dermal collagen (dc) and adnexal units (asterisks). Scale bars = 500 μm (B and F) and 100 μm (C, D, G, and H).
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
Correlation between gross and histologic healing for ZSCS (A through D) and suture (E through F) closure techniques. A—Gross appearance of healing within the caudal portion of the surgical incision closed with ZSCS (below the arrowhead) in horse 3 correlates with histologic healing from the same site. B—Low-magnification (2X) photomicrograph shows the incisional edges are completely spanned by well-organized granulation tissue (double-headed arrows) extending through all dermal layers without inflammatory or necrotic foci. C and D—H&E- (C) and polarized PSR–stained (D), high-magnification photomicrographs of the incisional scar in panel B show an intact, moderately acanthotic epidermis (e) overlying a collagen-rich scar (double-headed arrows) flanked by normal dermal collagen (dc) and adnexal units (asterisks). E—Gross appearance of healing within the caudal portion of the surgical incision closed with suture (below the arrowhead) in horse 5 correlates with histologic healing from the same site. F—Low-magnification photomicrograph shows complete spanning of the incision by slightly wider seam of well-organized granulation tissue (double-headed arrows) adjacent to a depressed surface (large arrowheads) with mildly inflamed intradermal clefts (small arrowheads) associated with cutaneous sutures. G and H—H&E (G) and polarized PSR–stained (H), high-magnification photomicrographs of the incisional scar in panel F also show similar healing as the ZSCS with an intact, moderately acanthotic epidermis (e) overlying a collagen-rich scar flanked by normal dermal collagen (dc) and adnexal units (asterisks). Scale bars = 500 μm (B and F) and 100 μm (C, D, G, and H).
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
Correlation between gross and histologic healing for ZSCS (A through D) and suture (E through F) closure techniques. A—Gross appearance of healing within the caudal portion of the surgical incision closed with ZSCS (below the arrowhead) in horse 3 correlates with histologic healing from the same site. B—Low-magnification (2X) photomicrograph shows the incisional edges are completely spanned by well-organized granulation tissue (double-headed arrows) extending through all dermal layers without inflammatory or necrotic foci. C and D—H&E- (C) and polarized PSR–stained (D), high-magnification photomicrographs of the incisional scar in panel B show an intact, moderately acanthotic epidermis (e) overlying a collagen-rich scar (double-headed arrows) flanked by normal dermal collagen (dc) and adnexal units (asterisks). E—Gross appearance of healing within the caudal portion of the surgical incision closed with suture (below the arrowhead) in horse 5 correlates with histologic healing from the same site. F—Low-magnification photomicrograph shows complete spanning of the incision by slightly wider seam of well-organized granulation tissue (double-headed arrows) adjacent to a depressed surface (large arrowheads) with mildly inflamed intradermal clefts (small arrowheads) associated with cutaneous sutures. G and H—H&E (G) and polarized PSR–stained (H), high-magnification photomicrographs of the incisional scar in panel F also show similar healing as the ZSCS with an intact, moderately acanthotic epidermis (e) overlying a collagen-rich scar flanked by normal dermal collagen (dc) and adnexal units (asterisks). Scale bars = 500 μm (B and F) and 100 μm (C, D, G, and H).
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
Healing scores did not significantly differ between cranial and caudal locations (5 ± 2.6 vs 4.8 ± 3.6; P = 0.87). One horse (horse 3), with gross evidence of suppuration involving the site closed with suture, showed inadequate bridging of the incision that extended from the superficial through the subadnexal dermis and had an adjacent focus of epidermal necrosis (Figure 4); however, at the location of the incision, the overlying epidermis was intact without evidence of inflammation or infection, and Gram stains did not reveal bacteria. Eight incision sites (evenly distributed between ZSCS and suture closure sites) had regional dermal necrosis and granulomatous to pyogranulomatous inflammatory foci < 3 mm in diameter associated with subcuticular suture tracts (both ZSCS and suture closure sites) and cutaneous closure (suture closure site only). The regions of dermal necrosis demonstrated a polarity that extended in a hemicircumferential pattern from the suture material (Figure 4). The median percentage area of dermal necrosis associated with suture tracts was not different between ZSCS (0.2; range, 0% to 16%) and sutured methods (0.15; range, 0% to 13%; P > 0.99). Dermal granulomas comprised discrete, concentrated aggregates of epithelioid macrophages and multinucleate giant cells admixed with lymphocytes and plasma cells that occasionally surrounded a core of neutrophils with few eosinophils (ie, pyogranulomas; Figure 4). Gram stains did not reveal bacteria; small fragments of individualized to aggregated bundles of refractile material (ie, partially hydrolyzed suture material) were present within them. The median number of dermal suture granulomas for the ZSCS (1.0; range, 0 to 2) was not different from that of sutured skin (0.5; range, 0 to 2; P > 0.99), as all horses had subcutaneous suture, which caused granuloma formation. When comparing cranial and caudal incision sites, no differences were identified for the median numbers of granulomas (cranial, 0.5 [range, 0 to 2]; caudal, 1.5 [range, 0 to 2]; P = 0.4) or median percentage of dermal necrosis (cranial, 0.2 [range 0% to 6.0%]; caudal, 0.15 [range 0% to 16%]; P = 0.86). Cutaneous suture closures from 2 horses had small (< 500-μm-diameter) displaced epidermal islands and keratinaceous debris displaced into the dermis adjacent to the incision site that were associated with suppurative inflammation (Figure 4). Gram stains revealed few gram-positive cocci and gram-negative filamentous bacilli associated with the keratin debris in horse 5, but the inflammation was localized to the keratin focus and there was complete incisional bridging noted by well-organized, collagen-rich granulation tissue.
H&E-stained histology of wound healing complications identified in suture closure (A and B) and ZSCS (C and D) groups. A—A serosuppurative epidermal crust (arrowhead) overlies a persistent superficial dermal cleft (double-headed arrow; high-magnification inset) extending to a hemorrhagic cavity (asterisks); an adjacent focus of necrotic, ulcerated epidermis (arrow) corresponds to gross suppuration of a suture site. B—Serosuppurative epidermal crusts (asterisks) flank an epidermal cleft overlying inflamed suture tracts (arrowheads) associated with a region of dermal necrosis (black outline); high-magnification inset of framed area shows smudged pale eosinophilic collagen fibers with fibroblast karyolysis and pyknosis (arrows). C—An incision bridged by an intact epidermis and well-organized granulation tissue overlies deep dermal pyogranulomatous foci (arrows); Gram stains (not shown) did not identify microorganisms. D—Small (< 500-μm-diameter) displaced dermal islands of epidermis (e) and suppurative inflammation surrounding keratinized debris (arrows) containing few gram-positive and gram-negative bacteria (not shown). Scale bars = 500 μm (A through C), 100 μm (D and A inset), and 20 μm (B inset).
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
H&E-stained histology of wound healing complications identified in suture closure (A and B) and ZSCS (C and D) groups. A—A serosuppurative epidermal crust (arrowhead) overlies a persistent superficial dermal cleft (double-headed arrow; high-magnification inset) extending to a hemorrhagic cavity (asterisks); an adjacent focus of necrotic, ulcerated epidermis (arrow) corresponds to gross suppuration of a suture site. B—Serosuppurative epidermal crusts (asterisks) flank an epidermal cleft overlying inflamed suture tracts (arrowheads) associated with a region of dermal necrosis (black outline); high-magnification inset of framed area shows smudged pale eosinophilic collagen fibers with fibroblast karyolysis and pyknosis (arrows). C—An incision bridged by an intact epidermis and well-organized granulation tissue overlies deep dermal pyogranulomatous foci (arrows); Gram stains (not shown) did not identify microorganisms. D—Small (< 500-μm-diameter) displaced dermal islands of epidermis (e) and suppurative inflammation surrounding keratinized debris (arrows) containing few gram-positive and gram-negative bacteria (not shown). Scale bars = 500 μm (A through C), 100 μm (D and A inset), and 20 μm (B inset).
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
H&E-stained histology of wound healing complications identified in suture closure (A and B) and ZSCS (C and D) groups. A—A serosuppurative epidermal crust (arrowhead) overlies a persistent superficial dermal cleft (double-headed arrow; high-magnification inset) extending to a hemorrhagic cavity (asterisks); an adjacent focus of necrotic, ulcerated epidermis (arrow) corresponds to gross suppuration of a suture site. B—Serosuppurative epidermal crusts (asterisks) flank an epidermal cleft overlying inflamed suture tracts (arrowheads) associated with a region of dermal necrosis (black outline); high-magnification inset of framed area shows smudged pale eosinophilic collagen fibers with fibroblast karyolysis and pyknosis (arrows). C—An incision bridged by an intact epidermis and well-organized granulation tissue overlies deep dermal pyogranulomatous foci (arrows); Gram stains (not shown) did not identify microorganisms. D—Small (< 500-μm-diameter) displaced dermal islands of epidermis (e) and suppurative inflammation surrounding keratinized debris (arrows) containing few gram-positive and gram-negative bacteria (not shown). Scale bars = 500 μm (A through C), 100 μm (D and A inset), and 20 μm (B inset).
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
For angiogenesis, compared to normal skin biopsies, there was a significant increase in the median number of factor VIII–staining vessels at 14 days of healing for both ZSCS (P = 0.048) and sutured (P < 0.01) incisions compared to control skin biopsies (48/mm2; range, 23 to 71/mm2; Figure 5). The median number of factor VIII–staining blood vessels per unit area between ZSCS incisions (77/mm2; range, 58 to 166/mm2) and sutured incisions (125/mm2; range, 58 to 241/mm2) was not statistically significant (P = 0.065). There was no difference in the median number of blood vessels between cranial and caudal incisions (P > 0.99).
Factor VIII–positive vascular profiles within biopsies of control skin compared to ZSCS and suture incisional closure sites. Few factor VIII–positive vascular profiles (A; arrows) per unit area are interspersed among adnexae including follicles (asterisk) and sebaceous glands (s) of the superficial to mid-dermis compared to healing incisional scar tissue from ZSCS (B) and suture closure (C) sites, where adnexae are effaced by organizing granulation tissue. A trend for fewer vascular profiles per unit area in ZSCS sites compared to suture closure sites did not reach statistical significance. e = Epidermis. Scale bars = 50 μm.
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
Factor VIII–positive vascular profiles within biopsies of control skin compared to ZSCS and suture incisional closure sites. Few factor VIII–positive vascular profiles (A; arrows) per unit area are interspersed among adnexae including follicles (asterisk) and sebaceous glands (s) of the superficial to mid-dermis compared to healing incisional scar tissue from ZSCS (B) and suture closure (C) sites, where adnexae are effaced by organizing granulation tissue. A trend for fewer vascular profiles per unit area in ZSCS sites compared to suture closure sites did not reach statistical significance. e = Epidermis. Scale bars = 50 μm.
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
Factor VIII–positive vascular profiles within biopsies of control skin compared to ZSCS and suture incisional closure sites. Few factor VIII–positive vascular profiles (A; arrows) per unit area are interspersed among adnexae including follicles (asterisk) and sebaceous glands (s) of the superficial to mid-dermis compared to healing incisional scar tissue from ZSCS (B) and suture closure (C) sites, where adnexae are effaced by organizing granulation tissue. A trend for fewer vascular profiles per unit area in ZSCS sites compared to suture closure sites did not reach statistical significance. e = Epidermis. Scale bars = 50 μm.
Citation: American Journal of Veterinary Research 83, 5; 10.2460/ajvr.21.08.0135
Discussion
We found that using the ZSCS in a ventral midline split-scar model resulted in acceptable skin closure and that the postoperative cosmetic and histopathologic healing at 2 weeks was similar or superior to that of sutured closure. Further, we found that there was a significant time reduction using ZSCS compared to suture.
Incisional morbidities in horses undergoing ventral midline celiotomy are common postoperatively and may contribute to prolonged recovery, increased costs, and potential loss of performance.5–12 A closure technique that would reduce the risk of complications is ideal, prompting this study’s investigation into the use of the ZSCS for celiotomy closures. In comparison to suture and staples, the ZSCS offers the advantage of not penetrating the skin, therefore minimizing local trauma and reducing potential bacterial translocation.1–4,18,19,25–28 The flexible nature of the ZSCS allows for dynamic compression during axial incisional extension, as documented in nonequid species translocation.1–4,18,19,25–28 The patented force distribution structure acts as a scaffold to distribute tension and offload external distraction forces, resulting in a lower-tension closure with improved perfusion to the wound edges.18,28 Although suture-associated dermal granulomas and pyogranulomas were identified in both sutured and ZSCS sites, no bacteria were identified within these inflammatory foci on Gram stain. One exception was a sutured closure site of 1 horse with excellent incisional healing, where small, displaced islands of epidermis and keratinized debris associated with suppurative inflammation of the deep dermis contained few mixed bacteria. We speculated that using ZSCS could potentially mitigate regional dermal necrosis, as seen with suture-associated tension and ischemia. This may further have protective benefits to reduce infection. A blinded, randomized, prospective study investigating incisional infection in horses is needed to determine whether using ZSCS significantly reduces the risk of incisional infection.
In addition to being fast and simple to apply, we found that the ZSCS was well tolerated by the horses postoperatively and removal was simple. A significant disadvantage of the ZSCS was the need for the skin to be dry to achieve adequate ZSCS adhesion. The hydrocolloid must be adhered to the skin to essentially anchor and bring the edges together by use of the zip straps. Failure of hydrocolloid adhesion results in an inability to appose the skin edges. In our study, we found that drying the skin thoroughly with sterile dry gauze swabs followed by a light application of an isopropyl alcohol–moistened gauze swab and allowing to air dry was an effective method of drying the skin. Further, application of a skin adhesive spray while protecting the incision with a dry gauze swab allowed for good adhesion of the ZSCS to the skin. Excessive hemorrhage or oozing represents a significant challenge to the application of the ZSCS and should be recognized that its use is limited for incisions unable to be kept dry. Hair length affects the adhesion of the ZSCS and is a notable consideration in animals. A commonly used clipper blade (Andis Co) in veterinary medicine (No. 40) cuts the hair to 0.25 mm. The recommended clipper and disposable blade for the ZSCS system cuts the hair to 0.22 mm. The impact of this small reduction in hair length is unknown in terms of maximizing ZSCS adhesion. We recognize that these additional skin preparation steps add to the total time to skin closure with the ZSCS. As a result, we acknowledge that the faster skin closure time compared to sutured closure is likely overemphasized and that excluding the required preparation time for the application of the ZSCS in the overall application time was a major limitation of the current study.
In human medicine, multiple scoring systems, such as the Burn Scar Index (Vancouver Scar Scale), have been used to evaluate linear scars.31–37 Although there are many different scoring systems used in human medicine and in a recent study38 evaluating scars in a porcine model, there is a lack of a validated scar evaluation system for horses, including ventral midline incisions. The proposed ECIS used for this study was created based on a combination of human scar scoring criteria that specifically applied to characteristics that could be used to evaluate equine scars, including palpation and visual inspection. Due to inherent differences in closure techniques, we also evaluated the ECIS excluding height as a variable to account for these differences. When height was excluded, there was a significant difference in ECIS between closure methods, suggesting that ZSCS was cosmetically superior. This ECIS is a proposed incisional scoring system created specifically for this study, although its application could be considered in future studies using a larger number of horses. More rigorous inter- and intraobserver agreement assessment (greater than 2 in the current study) is needed before it could be adopted in routine clinical practice.
Semiquantitative histologic grading schemes from previously published human and animal wound healing studies were modified to incorporate features identified within skin biopsies of this equine study.29,37,38 Histologic assessments were enhanced with quantitative analyses to further assess granulomatous inflammatory foci and regional dermal necrosis associated with suture tracts, as well as neovascularization within incisional healing sites compared to normal skin. When comparing the ZSCS and suture mean histopathologic scores, the post hoc power calculation was 21% (0.21). The post hoc power calculation comparing cranial and caudal histopathologic scores was 4% (0.04). Both calculations indicate lack of statistical power, and therefore interpretation of lack of significance should be lessened.
Although statistical differences between ZSCS and suture closure techniques were not identified in this study, several limitations were evident. Subjects enrolled in this study were healthy animals. Factors associated with perioperative morbidity have shown that shock status, cardiopulmonary performance under general anesthesia, lesion type, and nutritional plane may all influence the development of incisional morbidity.6–9,39–41 Due to the small number of animals in this study, the number of incisional morbidities encountered was also low, limiting any ability to compare rates between methods. Although granulomas and regional dermal necrosis with associated suture tracts were identified in both treatment groups, it is possible that more pronounced differences between ZSCS and traditional skin closure methods might be seen in animals at higher risk for postoperative incisional infections. We propose that the combination of semiquantitative and quantitative assessments could be implemented in future comparative studies that include a randomized prospective study comparing the ZSCS with not only sutured closure but staple and cyanoacrylate skin closure in a cohort of emergency celiotomy patients.
Cosmetic grading was performed by only 2 investigators. Although objective assessment of incisional edema with ultrasound would better characterize incisional swelling,14 accurately assessing edema remains challenging due to the gravitational migration of fluid toward the cranial portion of the incision. Furthermore, post hoc power calculation for edema scores was 23% (0.23), indicating lack of statistical power, and as such, interpretation of lack of significance should be tempered. Although the cosmetic result for a ventral midline incision is unlikely to be of owner concern compared to an incision on the face or body, ventral midline incisions are commonly performed and could serve as a model for evaluating skin healing by a variety of experimental methods, and having a validated scoring system is useful to make direct comparisons of healing between skin closure methods.
The nonblinded nature of this study served as a limitation. Although the closure method for the cranial and caudal halves of the incision was randomly assigned, the surgeon performing the closure was unable to be blinded to the treatment methods. Additionally, although the boarded pathologist was blinded to the samples submitted for histopathologic evaluation, observing suture material in the samples allowed for subsequent unblinding due to understanding of the initial study design. Ideally, the surgeon and the pathologist would both be blinded to eliminate any potential bias when evaluating the incisional healing and histopathologic grades.
An additional limitation of the study design included evaluation of the incision at 14 days postoperatively. In the proliferative phase of wound healing, peak collagen production occurs within 1 to 3 weeks, with reepithelialization and contraction occurring simultaneously and the remodeling and maturation phase beginning during the second week of repair.42 As such, although the majority of wound healing is completed within the first 2 weeks, evaluation at 14 days may not be fully representative of tissue healing in all incisions.43 A longer follow-up period would be required to determine the true cosmesis and healing of the incisions, as incisional morbidities, including infection and herniation, have been documented as occurring weeks to months after surgery.44
The use of the sutured abdominal stent applied for the recovery period was a further limitation in the present study. Advantages of an abdominal stent include applying direct pressure to the incision and possibly reducing tension on the primary incision line.45 It is possible that the abdominal stent could have served as additional protection to the ZSCS during recovery. Without the stent, it is likely that the incision and the ZSCS would have been under more strain. Comparing ZSCS with and without a stent placed would be interesting to assess the impact of anesthetic recovery on ZSCS utility and its ability to maintain wound closure.
Finally, use of the ZSCS is more expensive than sutured closure. A packet of Monocryl suture is approximately $20, compared to a Zip-16 ZSCS at approximately $100. Having additional supplies to support hydrocolloid adhesion further adds cost. Until there is a proven incisional morbidity risk reduction using the ZSCS, its higher overall expense compared to suture is not clinically justified at this time.
In conclusion, closure with the ZSCS resulted in faster skin closure times, superior cosmetic appearance scores, and similar histopathologic healing scores compared to sutured closure of the ventral midline skin in horses. While limitations to the utility of the ZSCS are recognized, the potential benefits of expedient closure, good cosmetic outcome, and satisfactory healing make this method a viable alternative for closure of linear wounds and incisions. Future studies investigating whether a reduction in incisional morbidities is observed in horses undergoing colic surgery is warranted to determine the clinical impact of the ZSCS in horses.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org
Acknowledgments
This study was approved by the University of Pennsylvania Institutional Animal Care and Use Committee (approval No. 806545).
The authors (SDH and KH) received funding from the USDA National Institute of Food and Agriculture (NIFA) Formula Fund #1021791. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Stryker (previously ZipLine Medical) donated the Zip-16 surgical skin closure device.
The authors would like to thank Darko Stefanovski for his statistical advice and Karie Durynski for her histochemical and immunohistochemical expertise.
References
- 1. ↑
Gorsulowsky DC, Talmor G. A novel noninvasive wound closure device as the final layer in skin closure. Dermatol Surg. 2015;41(8):987–989. doi:10.1097/DSS.0000000000000399
- 2. ↑
Tanaka Y, Miyamoto T, Naito Y, Yoshitake S, Sasahara A, Miyaji K. Randomized study of a new noninvasive skin closure device for use after congenital heart operations. Ann Thorac Surg. 2016;102(4):1368–1374. doi:10.1016/j.athoracsur.2016.03.072
- 3. ↑
Corrie C, Shmalberg J, Senneca C, Conner B. Use of a non-invasive surgical skin closure device in dogs following dorsolateral hemilaminectomy. Can Vet J. 2017;58(6):604–606.
- 4. ↑
Ko JH, Yang IH, Ko MS, Kamolhuja E, Park KK. Do zip-type skin-closing devices show better wound status compared to conventional staple devices in total knee arthroplasty? Int Wound J. 2017;14(1):250–254. doi:10.1111/iwj.12596
- 5. ↑
Freeman DE, Rötting AK, Inoue OJ. Abdominal closure and complications. Clin Tech Equine Pract. 2002;1(3):174–187. doi:10.1053/ctep.2002.35575
- 6. ↑
Isgren CM, Salem SE, Townsend NB, Timofte D, Maddox TW, Archer DC. Sequential bacterial sampling of the midline incision in horses undergoing exploratory laparotomy. Equine Vet J. 2019;51(1):38–44. doi:10.1111/evj.12958
- 7. ↑
Shearer TR, Holcombe SJ, Valberg SJ. Incisional infections associated with ventral midline celiotomy in horses. J Vet Emerg Crit Care (San Antonio). 2020;30(2):136–148. doi:10.1111/vec.12936
- 8.
Klohnen A. New perspectives in postoperative complications after abdominal surgery. Vet Clin North Am Equine Pract. 2009;25(2):341–350. doi:10.1016/j.cveq.2009.05.003
- 9. ↑
Honnas CM, Cohen ND. Risk factors for wound infection following celiotomy in horses. J Am Vet Med Assoc. 1997;210(1):78–81.
- 10. ↑
Wilson DA, Baker GJ, Boero MJ. Complications of celiotomy incisions in horses. Vet Surg. 1995;24(6):506–514. doi:10.1111/j.1532-950x.1995.tb01362.x
- 11. ↑
Davis W, Fogle CA, Gerard MP, Levine JF, Blikslager AT. Return to use and performance following exploratory celiotomy for colic in horses: 195 cases (2003–2010). Equine Vet J. 2013;45(2):224–228. doi:10.1111/j.2042-3306.2012.00615.x
- 12. ↑
Christophersen MT, Tnibar A, Pihl TH, Andersen PH, Ekstrøm CT. Sporting activity following colic surgery in horses: a retrospective study. Equine Vet J Suppl. 2011;43(suppl 40):3–6. doi:10.1111/j.2042-3306.2011.00490.x
- 13. ↑
Colbath AC, Patipa L, Berghaus RD, Parks AH. The influence of suture pattern on the incidence of incisional drainage following exploratory celiotomy. Equine Vet J. 2014;46(2):156–160. doi:10.1111/evj.12091
- 14. ↑
Scharner D, Gittek C, Winter K, et al. Comparison of incisional complications between skin closures using a simple continuous or intradermal pattern: a pilot study in horses undergoing ventral median celiotomy. PeerJ. 2018;6:e5772. doi:10.7717/peerj.5772
- 15.
Biedrzycki AH, Brounts SH. Case series evaluating the use of absorbable staples compared with metallic staples in equine ventral midline incisions. Equine Vet Educ. 2016;28(2):83–88. doi:10.1111/eve.12523
- 16. ↑
Torfs S, Levet T, Delesalle C, et al. Risk factors for incisional complications after exploratory celiotomy in horses: do skin staples increase the risk? Vet Surg. 2010;39(5):616–620. doi:10.1111/j.1532-950X.2009.00636.x
- 17. ↑
Al-Mubarak L, Al-Haddab M. Cutaneous wound closure materials: an overview and update. J Cutan Aesthet Surg. 2013;6(4):178–188. doi:10.4103/0974-2077.123395
- 18. ↑
Lalani GG, Schricker AA, Salcedo J, et al. Cardiac device implant skin closure with a novel adjustable, coaptive tape-based device. Pacing Clin Electrophysiol. 2016;39(10):1077–1082. doi:10.1111/pace.12926
- 19. ↑
De Maria E. New skin closure system facilitates wound healing after cardiovascular implantable electronic device surgery. World J Clin Cases. 2015;3(8):675–677. doi:10.12998/wjcc.v3.i8.675
- 20. ↑
Attia MW, Durani Y, Weihmiller SN. Minor trauma. In: Shaw KN, Bachur RG, eds. Fleisher and Ludwig’s Textbook of Pediatric Emergency Medicine. 7th ed. Wolters Kluwer; 2016:2142–2170.
- 21. ↑
Waldron DR. Skin and fascia staple closure. Vet Clin North Am Small Anim Pract. 1994;24(2):413–423. doi:10.1016/s0195-5616(94)50160-8
- 22. ↑
Martinez-Lopez J, Brown JA, Werre SR. Incisional complications after skin closure with n-butyl cyanoacrylate or stainless-steel skin staples in horses undergoing colic surgery. Vet Surg. 2021;50(1):186–195. doi:10.1111/vsu.13534
- 23.
Sabol F, Vasilenko T, Novotný M, et al. Intradermal running suture versus 3M™ Vetbond™ tissue adhesive for wound closure in rodents: a biomechanical and histological study. Eur Surg Res. 2010;45(3-4):321–326. doi:10.1159/000320837
- 24. ↑
Pope JFA, Knowles T. The efficacy of n-butyl-cyanoacrylate tissue adhesive for closure of canine laparoscopic ovariectomy port site incisions. J Small Anim Pract. 2013;54(4):190–194. doi:10.1111/jsap.12047
- 25. ↑
Levi K, Ichiryu K, Kefel P, et al. Mechanics of wound closure: emerging tape-based wound closure technology vs. traditional methods. Cureus. 2016;8(10):e827. doi:10.7759/cureus.827
- 26. ↑
Mitwalli H, Dolan C, Bacigalupi R, Khorasani H. A randomized, controlled, prospective clinical study comparing a novel skin closure device to conventional suturing. J Am Acad Dermatol. 2016;74(1):173–174. doi:10.1016/j.jaad.2015.08.004
- 27. ↑
Carli AV, Spiro S, Barlow BT, Haas SB. Using a non-invasive secure skin closure following total knee arthroplasty leads to fewer wound complications and no patient home care visits compared to surgical staples. Knee. 2017;24(5):1221–1226. doi:10.1016/j.knee.2017.07.007
- 28. ↑
Zip skin closure. Stryker. Accessed July 31, 2021. https://www.stryker.com/us/en/orthopaedic-instruments/products/zip-skin-closure.html
- 29. ↑
Safa B, Belson A, Meschter C, et al. In vivo efficacy study showing comparative advantage of bacterial infection prevention with zip-type skin closure device vs. subcuticular sutures. Cureus. 2018;10(8):e3102. doi:10.7759/cureus.3102
- 30. ↑
Kümmerle JM, Fogle C. Suture materials and patterns. In: Auer JA, Stick JA, Kümmerle JM, Prange T, eds. Equine Surgery. 5th ed. Elsevier; 2019:255–280.
- 31. ↑
Sullivan T, Smith J, Kermode J, Mclver E, Courtemanche DJ. Rating the burn scar. J Burn Care Rehabil. 1990;11(3):256–260. doi:10.1097/00004630-199005000-00014
- 32.
Baryza MJ, Baryza GA. The Vancouver Scar Scale: an administration tool and its interrater reliability. J Burn Care Rehabil. 1995;16(5):535–538. doi:10.1097/00004630-199509000-00013
- 33.
Truong PT, Lee JC, Soer B, Gaul CA, Olivotto IA. Reliability and validity testing of the Patient and Observer Scar Assessment Scale in evaluating linear scars after breast cancer surgery. Plast Reconstr Surg. 2007;119(2):487–494. doi:10.1097/01.prs.0000252949.77525.bc
- 34.
Draaijers LJ, Tempelman FR, Botman YA, et al. The Patient and Observer Scar Assessment Scale: a reliable and feasible tool for scar evaluation. Plast Reconstr Surg. 2004;113(7):1960–1965. doi:10.1097/01.prs.0000122207.28773.56
- 35.
Cromi A, Ghezzi F, Gottardi A, Cherubino M, Uccella S, Valdatta L. Cosmetic outcomes of various skin closure methods following cesarean delivery: a randomized trial. Am J Obstet Gynecol. 2010;203(1):36.e1–36.e8. doi:10.1016/j.ajog.2010.02.001
- 36.
van de Kar AL, Corion LU, Smeulders MJ, Draaijers LJ, van der Horst CM, van Zuijlen PP. Reliable and feasible evaluation of linear scars by the Patient and Observer Scar Assessment Scale. Plast Reconstr Surg. 2005;116(2):514–522. doi:10.1097/01.prs.0000172982.43599.d6
- 37. ↑
Beausang E, Floyd H, Dunn KW, Orton CI, Ferguson MW. A new quantitative scale for clinical scar assessment. Plast Reconstr Surg. 1998;102(6):1954–1961. doi:10.1097/00006534-199811000-00022
- 38. ↑
Theunissen D, Seymour B, Forder M, Cox SG, Rode H. Measurements in wound healing with observations on the effects of topical agents on full thickness dermal incised wounds. Burns. 2016;42(3):556–563. doi:10.1016/j.burns.2015.09.014
- 39. ↑
Phillips TJ, Walmsley JP. Retrospective analysis of the results of 151 exploratory laparotomies in horses with gastrointestinal disease. Equine Vet J. 1993;25(5):427–431. doi:10.1111/j.2042-3306.1993.tb02985.x
- 40.
Mair TS, Smith LJ. Survival and complication rates in 300 horses undergoing surgical treatment of colic. Part 2: short-term complications. Equine Vet J. 2005;37(4):303–309. doi:10.2746/0425164054529364
- 41. ↑
Costa-Farré C, Prades M, Ribera T, Valero O, Taurà P. Does intraoperative low arterial partial pressure of oxygen increase the risk of surgical site infection following emergency exploratory laparotomy in horses? Vet J. 2014;200(1):175–180. doi:10.1016/j.tvjl.2014.01.029
- 42. ↑
Provost PJ. Wound healing. In: Auer JA, Stick JA, Kümmerle JM, Prange T, eds. Equine Surgery. 5th ed. Elsevier; 2019:53–69.
- 43. ↑
Theoret C. Physiology of wound healing. In: Theoret C, Schumacher J, eds. Equine Wound Management. 3rd ed. John Wiley and Sons Inc; 2017:1–13.
- 44. ↑
Gibson KT, Curtis CR, Turner AS, McIlwraith CW, Aanes WA, Stashak TS. Incisional hernias in the horse. Incidence and predisposing factors. Vet Surg. 1989;18(5):360–366. doi:10.1111/j.1532-950x.1989.tb01100.x
- 45. ↑
Tnibar A, Grubbe Lin K, Thurøe Nielsen K, et al. Effect of a stent bandage on the likelihood of incisional infection following exploratory coeliotomy for colic in horses: a comparative retrospective study. Equine Vet J. 2013;45(5):564–569. doi:10.1111/evj.12026
