Veterinary Ophthalmology (Modified Lateral Enucleation Technique) - PDF - AQA - 2024

Received: 7 March 2024 | Revised: 13 August 2024 | Accepted: 4 October 2024 DOI: 10.1111/vop.13293 ORIGINAL REPORT Modified lateral enucleation technique—Surgery without ligation or clamping of the optic nerve: Technique description, complication rate and risk factors, and intraoperative blood loss estimation in companion animals Ingrid Allgoewer | Petr Soukup Animal Eye Practice, Berlin, Germany Abstract Correspondence Purpose: The purpose of this study is to describe modification of the lateral enu- Ingrid Allgoewer, Animal Eye Practice, cleation technique without ligation or clamping of the optic nerve, document the Lindenthaler Allee 9, Berlin 14163, Germany. incidence of complications, estimate intraoperative blood loss and identify pos- Email: [email protected] sible risk factors for the developments of complications. Methods: Medical records of dogs, cats, and rabbits undergoing lateral enu- cleation without clamping of the optic nerve were identified and retrospectively reviewed for post-operative complications (2000–2022). The significance of possi- ble risk factors for the development of complications, including species, sex, age, eye, surgeon, presumed ocular surface infection, cultures, follow-up, antibiotics, NSAIDs, complications and diabetes mellitus was examined in a subset of these patients (2019–2022). As a prospective study, intraoperative blood loss was esti- mated by gravimetric analysis in an additional subset. Results: Records of 1296 enucleations were retrospectively reviewed and de- tailed evaluation regarding potential risk factors was performed in 446 enuclea- tions. The overall complication rate and surgical site infection rate was 2.31% and 2.08% respectively. Only Pseudomonas spp. bacterial culture was associated with development of complications. Estimated relative intraoperative blood loss was 2.2% and 4.1% in 43 dogs and 29 cats respectively. Conclusions: The modified lateral enucleation technique is a safe and fast proce- dure with minimal risk of postoperative complications in dogs, cats, and rabbits. Based on the anatomy of the orbital vasculature ligation or clamping of the optic nerve and surrounding tissue is contraindicated. KEYWORDS bacterial culture, companion animals, globe surgery, orbital vasculature, pseudomonas spp, surgical site infection © 2024 American College of Veterinary Ophthalmologists. Veterinary Ophthalmology. 2024;00:1–13. wileyonlinelibrary.com/journal/vop | 1 2 | ALLGOEWER and SOUKUP 1 | I N T RO DU CT ION musculares for the eye muscles; (2) the lacrimal artery, which runs laterally along the eye muscle cone to the lac- Enucleation is a commonly performed surgical proce- rimal gland; (3) the supraorbital artery, which is absent dure in veterinary medicine for numerous conditions in the dog and emerges from the orbit rostrodorsally; (4) requiring removal of the globe. However, reports about the external ethmoidal artery, which runs through the surgical techniques for enucleation1–3 or their compli- ethmoid foramen to the nasal cavity; (5) the supraorbital cations4–6 are sparse. In the literature, two widely used artery, which exits the orbit rostrodorsally; and (6) the surgical approaches are most commonly described, viz. anastomotic branch with the internal ophthalmic artery, the transpalpebral and the transconjunctival technique. which is often referred to as the “ramus bulbi” because The transconjunctival approach3,7 involves an incision most of the arteries for the eyeball branch off from this in the upper and lower palpebral conjunctiva with sub- branch. The internal ophthalmic artery is only responsible sequent dissection of the eyelids, while the transpal- for the vascular supply of the eye cup during fetal devel- pebral approach1 starts with a sharp transection of the opment and postnatally it becomes rudimentary. It arises lid skin and subcutaneous dissection. In 1972, Bellhorn intracranially from the rostral cerebral artery and only described a lateral approach which allows for a better supplies the optic nerve, with which it enters the orbit orientation during dissection of the orbital tissues.2 through the optic canal.12 The corresponding ophthalmic This technique was then included in Gelatt's textbook artery is the main artery for the eye in humans.13 (1991).8 The venous blood of the eyeball and its accessory or- However, most current textbooks mention only the gans collects within the orbit in an ophthalmic plexus transconjunctival and transpalpebral techniques and which is surrounded by the periorbita and is formed by indicate the necessity of clamping of the optic nerve, in the external dorsal and ventral ophthalmic veins, the analogy to enucleation procedures described in human internal ophthalmic vein which is often duplicated and ophthalmology.9,10 Allgoewer (2006) introduced a modi- the numerous connections between these three major fication of Bellhorn's lateral enucleation technique. The veins. unique feature of the modification was the omission of The ophthalmic plexus (in dogs and cats) or ophthal- the ligation or clamping of the optic nerve and surround- mic sinus (in rabbits) has several connections with the ing tissues.11 intracranial cavernous sinus as well as with the facial The purpose of this study is to review the modified and maxillary veins. The ophthalmic venous plexus or lateral enucleation technique in detail, to evaluate the sinus drains all the venous blood from the eyeball as associated blood loss, to present a retrospective review of well as venous branches from the eye muscles, the lac- the complications and to evaluate possible risk factors for rimal vein from the lacrimal gland and the conjunctival complications after enucleation with the modified lateral veins, which drain blood from the conjunctiva in a vari- approach. able manner. On the other hand, blood from the eyelids The anatomical background of the orbital vasculature is drained through the palpebral veins to the facial vein is described as an introduction for the surgical technique. (Figures 1 and 2).12 1.1 | The orbital vasculature 1.2 | Surgical procedure The arterial blood supply to the eyeball and its acces- The surgery is performed under general anesthesia. The sory organs is provided by various arteries which in animal is placed in lateral recumbency with the head po- the cat arise from the rete mirabile arteriae maxillaris, sitioned on a vacuum cushion pointing towards the end whereas in the dogs and rabbits they arise from the ex- of the table. The surgical area is clipped and disinfected ternal ophthalmic artery. The latter runs through the by a repeated application of a 2% povidone-iodine solu- orbit to the dorsal side of the optic nerve, where it rami- tion. For the modified lateral enucleation, a lateral can- fies into several branches and connects with the weak thotomy is performed in preparation for blunt cleavage of internal ophthalmic artery. Additional branches from the outer layer of the eyelids from the inner. The temporal the malar artery, which originates from the maxillary canthus is clamped with a hemostat (Figure 3A) and then artery and runs ventromedially in the orbit, contribute cut with Metzenbaum scissors (Figure 3B). Blunt cleaving to the supply of the eyelids, the conjunctiva and nictitat- of both eyelids is performed by introducing and advanc- ing membrane.12 ing Metzenbaum scissors from the temporal to the nasal Within the orbit, the external ophthalmic artery gives canthus (Figure 3C,E). The tips of the scissors are intro- off its branches in the following ways: (1) various rami duced into the plane of cleavage between the orbicularis ALLGOEWER and SOUKUP | 3 F I G U R E 1 Corrosion casts of the orbital arteries (red) and veins in cat (A, B) and dog (C, D). (A) Lateral view of the left ocular and retrobulbar vessels of a cat (drawing). (B) Lateral view of the major arteries in the left feline orbit (the infraorbital and lingual arteries are indicated by black and white arrows, respectively). (C) Lateral view of the left ocular and retrobulbar vessels of a dog (drawing). (D) Dorsal view of the right orbital vasculature in a dog, consisting of vessels of smaller diameter only. 1. A. carotis externa; 2. A. maxillaris; 3. Rete mirabile a. maxillaris; 4. A. ophthalmica externa; 5. Ramus bulbi (Ramus anastomoticus cum a. ophthalmica interna); 6. A. ophthalmica interna; 7. Plexus ophthalmicus; 8. V. ophthalmica externa; 9. V. ophthalmica interna; 10. V. angularis oculi; 11. V. profunda faciei. F I G U R E 2 Corrosion casts of the orbital and ocular vasculature (P. Simoens 2006). (A) Left eye of a dog, medial view. (B) Left eye of a cat, medial view. (C) Left eye of a cat, ventral view. (D) Posterior aspect of the left eye of a cat, dorsal view. 1. Ramus bulbi (Ramus anastomoticus cum a. ophthalmica interna); 2. A. ophthalmica interna; 3. A. ciliaris posterior longa; 4. Aa. ciliares posteriores breves; 5. Aa. and Vv. cilioretinales; 6. Plexus vasculosus n. optici; 7. V. vorticosa; 8. Plexus venosus sclerae; 9. V. ciliaris anterior; 10. V. ophthalmica externa; 11. Plexus ophthalmicus; 12. V. angularis oculi. muscle and the tarsal plate. With blunt dissection, this exposed for further dissection of the periocular tissues.2 plane of separation is carried from the temporal to the (Video 1). medial canthus for both the upper and the lower eyelids. The eyelids are clamped together with a hemostat just (Figure 3D,F). Metzenbaum scissors are utilized to cut the proximal to the lid margin (Figure 4A). The nasal can- skin parallel and close to the lid margin. This incision is so thus is then circumcised with the scissors. The globe is extended nasally until the region of the medial canthus is gently rotated inwards (nasally) to improve access to the reached. Thus, the subconjunctival tissues have now been lateral canthal ligament which is transected with scissors 4 | ALLGOEWER and SOUKUP F I G U R E 3 Enucleation of the right eyeball with lateral approach as described by Bellhorn (1972): (A) Lateral canthotomy starting with clamping hemostat on the temporal canthus. (B) Temporal canthotomy performed with scissors. (C) Blunt subcutaneous separation of the upper lid tissues between a skin and orbicularis muscle layer anteriorly and a tarsal plate and conjunctival layer posteriorly with a Metzenbaum scissors. (D) Incision of the anterior skin and orbicularis muscle layer of the lower lid with scissors. (E, F) Repetition of steps C and D for the upper lid: Blunt separation of the lid tissues and incision of the skin and orbicularis muscle layer. facilitating further inward rotation. The subconjuncti- packing with gauzes. Then the peripheral remnants of the val tissues are then dissected down through the Tenon's Tenon's capsule and orbital septum are drawn together in capsule to the sclera just behind the limbus starting tem- a cruciate pattern with a 3-0 resorbable suture starting na- porally (Figure 4B). This dissection close to the sclera ex- sally. The cruciate pattern allows for good adaptation as tends all around the globe except for the region adjacent to well as a quick closure. the medial canthus.2 (Video 1). Care is taken to accurately adapt the remaining perio- The remnant of the lateral canthal ligament, where cular tissues in a watertight fashion. Before completing it inserts into the Tenon's capsule is grasped by a for- the deep suture temporally, the gauzes are retrieved. The ceps and the globe can now be rotated further inwards, more superficial layers are closed with single interrupted superiorly, or inferiorly as needed to expose the various sutures. For all sutures resorbable suture material is used muscular and tendinous tissues where they attach to (i.e. Vicryl® 3-0 and 4-0, Ethicon, Johnson & Johnson the sclera. There is no need to identify individual extra- Surgical Technologies). Hemorrhage is usually minor un- ocular muscles while dissecting down into the orbit.2 less eyes with long-standing disease process have caused (Video 1). many smaller orbital vessels to enlarge.2 Finally, the in- By leaving the medial attachments in place, further cised edges of the eyelids are sutured together over the rotation outward of the posterior segment of the globe is fascial sheath with single interrupted sutures. The eye- readily accomplished. This exposes the temporal portions lids may be trimmed as necessary to approximate the cut of the retractor bulbi.2 The remaining retractor bulbi and edges. Locoregional anesthesia may be optionally applied. the optic nerve with surrounding tissues is transected with The surgery is performed as an ambulatory proce- curved scissors without prior clamping or ligation. The dure. A non- steroidal anti- inflammatory (NSAID) (i.e. posterior pole of the globe is then easily rotated outward. Carprofen, Rimadyl®; Zoetis) and a broad-spectrum an- At this time the medial canthal ligament is transected and tibiotic (i.e. amoxicillin clavulanic acid, Synulox®, Zoetis) the medial periocular tissues are readily dissected. The re- are administered at the time of anesthesia induction and maining subconjunctival tissue and the nictitating mem- continued orally for 5–7 days after surgery. After the sur- brane are excised and the globe lifted free.2 (Video 1). gery, the wound is not covered. An Elizabethan collar is Inspection of the exterior surfaces of the globe and ex- not used. The patients are typically discharged within 2 h amination the exposed orbital tissues is followed by orbital after recovery from anesthesia. ALLGOEWER and SOUKUP | 5 V I D E O 1 A lateral canthotomy is performed in preparation for blunt cleavage of the outer layer of the eyelids from the inner. Therefore, the temporal canthus is clamped with a hemostat and then cut with Metzenbaum scissors. Blunt cleaving of both eyelids is performed by introducing and advancing Metzenbaum scissors from the temporal to the nasal canthus. The tips of the scissors are introduced into the plane of cleavage between the orbicularis muscle and the tarsal plate. With blunt dissection, this plane of separation is carried from the temporal to the medial canthus for both the upper and the lower eyelids. Metzenbaum scissors are utilized to cut the skin parallel and close to the lid margin. This incision is so extended nasally until the region of the medial canthus is reached. Thus, the subconjunctival tissues have now been exposed for further dissection. The eyelids are clamped together with a hemostat just proximal to the lid margin. The nasal canthus is then circumcised with the scissors. The globe is gently rotated inwards. This makes the lateral canthal ligament accessible. It is then severed with the scissors so as to allow further inward rotation. The subconjunctival tissues are then dissected down through the Tenon's capsule to the sclera just behind the limbus. This dissection close to the sclera extends all around the globe except for the region adjacent to the medial canthus. The remnant of the lateral canthal ligament where 2 | M AT E R IALS AN D M ET H OD S it inserts into the Tenon's capsule is grasped by a forceps and the globe can now be rotated further inwards, superiorly, or inferiorly 2.1 | Retrospective evaluation of as needed to expose the various muscular and tendinous tissues where they attach to the sclera. There is no need to identify the complications and evaluation of potential extraocular muscles while dissecting down into the orbit. By leaving risk factors the medial attachments in place, further rotation outward of the posterior segment of the globe is readily accomplished. This exposes A retrospective evaluation of cases that underwent the the temporal portions of the retractor bulbi. The remaining retractor surgical procedure described above was performed. bulbi and the optic nerve with surrounding tissues is transected with Cases with a minimum follow- up of 7 days were curved scissors without prior clamping or ligation. The posterior included. pole of the globe is then easily rotated outward. At this time the This evaluation was completed in two parts. First, the medial canthal ligament is transected and the medial periocular overall complication rate was evaluated in dogs, cats, tissues are readily dissected. The remaining subconjunctival tissue and rabbits for the period of 2000–2022. In this evalua- and the nictitating membrane are excised and the globe lifted free. tion, the complications were graded as: minor (seroma Inspection of the exterior surfaces of the globe and examination the exposed orbital tissues is followed by orbital packing with gauzes. formation, focal suture dehiscence, subcutaneous or- The peripheral remnants of the Tenon's capsule and orbital septum bital emphysema, skin necrosis, wound dehiscence after are drawn together in a cruciate pattern with a 3-0 resorbable stitch removal), moderate (superficial wound infection, suture starting nasally. The cruciate pattern allows for good deep focal suture reaction), severe (orbital infection, adaptation as well as a quick closure. orbital infection requiring orbital revision) and self- trauma to the wound. Cases treated by the same pro- cedure but without follow-up were excluded from this retrospective evaluation. luxation, proptosis bulbi, neoplasia, other), presumed Second, a detailed review of cases in dogs, cats, and ocular surface infection (“non-clean” eye), bacterial cul- rabbits for the four-year period 2019–2022 was performed. ture results, follow-up length, NSAID treatment length, In this evaluation, a possible influence of risk factors antibiotic treatment length, antibiotic used (amoxicillin- on the development of complications was researched. clavulanate, enrofloxacin, cefovecin, marbofloxacin, The following variables were noted: species, breed, sex, azithromycin, doxycycline, trimethoprim- sulfonamide, spay or neuter status, age, left and right eye, enucleation none), diabetes mellitus status. Complication grading of both eyes at the same time, enucleation of both eyes and recording of specific complications were the same consecutively, operating surgeon, reason for enucleation as stated above for the overall complications. Moreover, (with a maximum of two equivalent reasons being noted; days until development of the complication and days until glaucoma, ocular infection/perforation, retinal detach- resolution were noted. Exclusion criteria were identical to ment and uveitis, phthisis bulbi or microphthalmos, lens the above stated. The retrospective study was performed 6 | ALLGOEWER and SOUKUP F I G U R E 4 Enucleation with lateral approach continued: (A) Clamping of palpebral fissure with a hemostat. (B) Careful dissection close to the globe starting laterally and continuing into the sub-Tenon's space. Blunt and sharp dissection of the orbital tissues and sharp transection of the extraocular muscles. according to GERVO guidelines and was approved by the 2.3 | Estimation of blood loss during responsible authority (Landesamt für Gesundheit und modified lateral enucleation procedure Soziales, Berlin, Germany) under the registration number StNo 009-2023. Absolute and relative blood loss were estimated in a pro- spective study according to a previously published study design by Lenihan et al.17 on cases operated by the modi- 2.2 | Statistical analysis fied lateral enucleation technique between January and August 2023. Briefly, blood loss was estimated by gravi- The detailed review (2019–2022) was statistically evalu- metric method.18 Prior to the surgery, the dry weight ated. Any association was determined between the pres- of swabs and draping was weighed using a dedicated ence of postoperative complications and species, sex, calibrated digital accuracy weighing scale (AMIR Brifit, age (in years), the surgeon effect, left versus right eye, Hongkong Feytin Technology Co Ltd) with a precision enucleation of both eyes at the same time, enucleation of 0.01 g. The same was performed directly after surgery of both eyes consecutively (animals that occurred twice and the difference was noted as absolute blood loss (ABL). in the data were considered in the statistical analysis The assumption of 1 g of blood equaling 1 mL of blood was by cluster robust standard errors instead of indepen- used.19 No additional fluids were used during the surgery dently and identically distributed errors), reason for to flush the surgical site. The relative blood loss (RBL) enucleation, presumed ocular surface infection, antibi- was calculated as percentage of blood loss from the total otics used, length of antibiotic use and length of anti- estimated circulating blood volume. For dogs and rab- inflammatory medications. Metric data is reported as bits, 85 mL/kg of body weight was used in the equation17 the mean ± standard deviation, since no outliers were whereas for cats, 65 mL/kg was used.20 In the observation detected. Categorical variables are represented as per- period, all client-owned dogs, cats, and rabbits present- centages. Presence of postoperative complications ver- ing for enucleation as a treatment of their ocular disease sus variables was investigated by logistic regression with were included in the study. The following criteria were cluster robust standard errors and the coefficients were subsequently used to exclude cases: orbital surgery differ- tested by Wald-test. In the case of presence of quasi- ing from the regular procedure (e.g. exenteration), cases complete separation, Fisher's exact test was used. This with clinical or histopathologic evidence of scleral rupture condition occurred for the following variables: enuclea- and/or orbital bleeding, and cases with incomplete weigh- tion of both eyes consecutively, lens luxation, phthisis ing data. The prospective part of the study was approved bulbi/microphthalmos, proptosis. by the responsible authority (Landesamt für Gesundheit Additionally, the association of the presence of postop- und Soziales, Berlin, Germany) under the registration erative complications after enucleation with cultured bac- number StNo 009-2023. teria strains was investigated on a subset of original data (cases with bacterial culture). The investigation was made by logistic regression with homoscedastic standard errors 3 | RESULTS and the coefficients were tested by Wald-test. The case of quasi-complete separation did not occur. Statistical signif- 3.1 | Overall complication rate icance for all tests was set at 0.05. R version 4.2.3 was used for analysis.14–16 A medical history search of the clinical database for enu- Statistical analysis was performed by Novustat GmbH cleation procedures from 2000 to 2022 was performed. (Wollerau, Switzerland). 1296 eyes that were removed by lateral enucleation and ALLGOEWER and SOUKUP | 7 had a minimum follow up of 7 days were included in the 3.94% in dogs (11/279), and 1.89% in cats (3/159). Since study (762 dog, 502 cat and 32 rabbit procedures). An there were only eight operations on rabbits and no compli- overall complication rate of 2.31% was noted (30/1296). cations were observed, these were excluded in the logistic Ten cases were minor complications (seroma formation regression model with species as covariable. Seven sur- in three dogs and one cat, focal suture dehiscence in two geons performed the surgeries. Surgeon A had a complica- dogs and one cat, subcutaneous orbital emphysema in 1 tion rate of 3.70% (6/161), surgeon B 5.26% (5/95), surgeon dog, skin necrosis in 1 dog, wound dehiscence after stitch C 1.20% (1/83), surgeon D 2.22% (1/45), surgeon E 3.33% removal in 1 cat). Thirteen cases were moderate complica- (1/30). Surgeons F and G did not have any complications tions (superficial wound infection n = 10 dogs, deep focal (0/20 and 0/12) and both were excluded for the considera- suture reaction, n = 3 cats). Seven complications were se- tion of a surgeon effect due to non-representative num- vere (orbital infection n = 4 dogs, orbital infection requir- ber of operations. Reasons for enucleation are detailed in ing orbital revision, n = 3 dogs). The overall complication Figure 5. Presumed ocular infection prior to surgery was rate was 3.15% (24/762) for dogs and 1.20% (6/502) for present in 86 cases and four of those developed complica- cats, whereas for rabbits no surgery related complications tions (4.65%), whereas non-infection was present in 360 were reported. The incidence of surgical site infection was cases and ten of those developed complications (2.78%). 2.08% (27/1296). Self-trauma to the wound, as a separate Standard peri-and postoperative therapy with amoxicillin- category, was observed in 2.39% of cases (31/1296), that is, clavulanate was used in 369 cases, 13 with complications in 0.92% of dogs (7/762) and in 4.78% of cats (24/502). This (3.52%). Cefovecin was used in 51 indicated cases, none phenomenon, especially in cats, did not happen directly of which developed complications. Enrofloxacin was after the surgery, but appeared between day 4 and 12 post- used in indicated cases according to pre-operative, peri- operatively. In one case, it disappeared only 2 months after operative or post-operative bacterial testing or due to con- surgery, when the primary wound had already healed for current systemic indication in 30 dogs, out of which seven 45 days. had complications (23.33%). Enrofloxacin was the most commonly used secondary antibiotic after surgical site infection developing under the therapy with primary an- 3.2 | Evaluation of risk factors on the tibiotic. Other antibiotics (marbofloxacin, azithromycin, development of complications doxycycline, trimethoprim-sulfonamide) or no antibiotics were used sporadically. The average duration of antibiotic A detailed review of enucleation cases for the years 2019– therapy was 7.2 ± 3.49 days. The average systemic anti- 2022 was performed. In these 4 years, altogether 484 enu- inflammatory therapy length was 9.1 ± 2.35 days. None of cleation procedures were performed. Thirty-eight cases the patients that developed complications were diabetic. did not meet the inclusion criteria and were excluded. The Pre-, peri-or post- operative bacterial cultures were final dataset contained 446 enucleation procedures, pro- available for 48 out of 446 cases. Thirteen cultures did not cedures, which were performed in 279 dogs, 159 cats and show any bacterial growth. The most commonly isolated 8 rabbits. Two hundred and twenty five right eyes and two bacteria were Pseudomonas spp. 7 cases (P. aeruginosa hundred and twenty one left eyes were removed and com- n = 5, P. monteillii n = 1, P. orizyhabitans n = 1) patho- plications occurred in 7 instances on each side. Bilateral genic Staphylococcus spp. 12 cases (S. pseudintermedius enucleation was performed in 17 patients. In seven cases, n = 9, S. aureus n = 1, S. felis n = 1, S. haemolyticus n = 1), both eyes were removed in two separate procedures. In beta hemolytic Streptococcus spp. 6 cases, E. coli 3 cases, dogs, the median age was 10.04 years (0.2–16.5 years), Pasteurella spp. 3 cases (P. multocida n = 2, P. canis n = 1). 60 eyes were removed from intact males, 66 from intact Other bacterial isolates were cultured only once, specific females, 64 from castrated males und 89 from spayed information can be found in Table S1. Bacterial groups females. In our dataset, the most common breeds were being cultured three times and less were removed from French Bulldogs (n = 30), Jack Russell Terriers (n = 20) statistical analysis. and Shih-Tzus (n = 16). In cats, median age was 9.55 years Average follow-up was 128.7 days with a median of (0.3–21.5 years), 9 eyes were removed from intact males, 12.0 days (7–1245 days). Postoperative complications de- 12 from intact females, 79 from castrated males und 59 veloped as following: Minor complications developed from spayed females. The most common breeds in our in seven cases (seroma formation n = 1 dog, focal suture dataset were domestic shorthair (n = 117), British short- dehiscence n = 2 dogs and 1 cat, subcutaneous orbital hair (n = 18) and Persian cats (n = 7). In rabbits, median emphysema n = 1 dog, skin necrosis n = 1 dog, wound age was 3.45 years (1.2–9.7), 2 eyes were removed from dehiscence after suture removal n = 1 cat). Five cases intact males, 4 from intact females and 2 from castrated were moderate complications (superficial wound infec- males. Complications were seen after 14 enucleations: tion n = 4 dogs, deep focal suture reaction n = 1 cat). Two 8 | ALLGOEWER and SOUKUP F I G U R E 5 Indications for enucleation. Hatched area for glaucoma. were severe complications (orbital infection n = 2 dogs). of estimated circulating blood volume (median 4.1%). In Postoperative complications developed after a median the rabbit case, ABL and RBL was 11.72 mL and 6.6%, re- time lapse of 12 days after surgery (4–75 days). Resolution spectively. In the canine case of bilateral enucleation, RBL of the complication was achieved after median time lapse totaled 4% whereas in the feline case, RBL totaled 2.3%. of 10 days after diagnosis (4–30 days). All cases received a standard surgery rate crystalloid infu- Detailed logistic regression statistical evaluation results sion of 5–10 mL/kg bodyweight. No postoperative compli- are listed in Table 1 and full R code is included in Data S1. cations were noted. For further details of the individual The majority of the potential risk factors did not reach cases see Table S2. statistical significance. The following three variables were statistically significantly associated with cases that devel- oped complications: positive Pseudomonas spp. bacterial 4 | DISC USSION culture (p <.05), treatment with enrofloxacin (p <.001) and duration of antibiotic therapy (p <.001). Neither the The enucleation techniques mostly mentioned in the lit- surgeon nor presumed ocular infection were associated erature are the transconjunctival approach as well as the with higher complication rates. transpalpebral approach. The transconjunctival approach has advantages of being simple, fast and associated with reduced bleeding, while the disadvantages mentioned are 3.3 | Estimation of blood loss during less exposure of orbital tissues,21 possible increased trac- modified lateral enucleation tion on the optic nerve22,23 as well as possible contami- nation from the ocular surface.21 Another disadvantage Altogether 84 animals were enrolled within the study is the risk of inadvertently leaving conjunctival tissue period (January 2023–August 2023). From those, 11 ani- in orbit which may then induce formation of cystic tis- mals had to be excluded from the final dataset, the most sue.24,25 Advantages of the transpalpebral approach are common exclusion criterion being scleral rupture. The a limited risk for contamination from the ocular surface final dataset contained 43 dogs, 29 cats, and one rabbit. and an increased exposure of orbital tissues and the optic One dog and one cat have undergone bilateral enuclea- nerve, while the disadvantages are increased bleeding and tion; thus, the final number of enucleated eyes was 75. In the procedure being slower than the transconjunctival dogs, absolute blood loss (ABL) range was 1.92–100.64 mL approach.21 The lateral transpalpebral enucleation tech- (median 19.1 mL), while relative blood loss (RBL) range nique was first described in 1972 by Bellhorn2 and listed as was from 0.19% to 7.74% of estimated circulating blood an alternative technique in Gelatt.8 The lateral approach (median 2.2%). In cats, ABL ranged from 1.54 to 38.48 mL was later included in Gelatt's ophthalmic surgery book (median 11.42 mL), and RBL ranged from 0.51 to 11.80% and is well illustrated in the current edition of Veterinary ALLGOEWER and SOUKUP | 9 T A B L E 1 Logistic regression statistical analysis: Evaluation of potential risk factors for development of postoperative complications. Calculation of odds ratio (OR), confidence intervals (CI), and statistical significance (p <.05). No complications Complications No. of Categorial variables operations n % n % OR (95% CI) p-value Species (dogs vs. cats 446 268/156/8 62.0/36.1/1.9 11/3/0 78.6/21.4/0.0 0.47 (0.10–1.53).2507 vs. rabbits)a Sex (female vs. female 446 79/145/68/140 18.3/33.6/15.7/32.4 3/3/3/5 21.4/21.4/21.4/35.7 0.54 (0.10–3.00).4649 spayed vs. male vs. 1.16 (0.21–6.46).8566 male neutered)b 0.94 (0.22–4.68).9345 Comparison of 5 414 155/90/82/44/29 38.8/22.5/20.5/11.0/7.3 6/5/1/1/1 42.9/35.7/7.1/7.1/7.1 1.43 (0.40–4.90).5603 surgeonsc 0.32 (0.02–1.89).2892 0.59 (0.03–3.56).6267 0.89 (0.05–5.49).9163 Eye (OS vs. OD) 446 214/218 49.5/50.5 7/7 50.0/50.0 1.02 (0.34–3.02).9728 Bilateral enucleation 446 399/33 92.4/7.6 13/1 92.9/7.1 0.93 (0.05–4.90).9444 (no vs. yes) Consecutive 446 418/14 96.8/3.2 14/0 100.0/0.0 1.0000 enucleation (no vs. yes) Retinal detachment 446 375/57 86.8/13.2 13/1 92.9/7.1 0.51 (0.03–2.62) 5163 and uveitis (no vs. yes) Glaucoma (no vs. yes) 446 203/229 47.0/53.0 7/7 50.0/50.0 0.89 (0.30–2.63).8244 Ocular infection/ 446 351/81 81.3/18.8 10/4 71.4/28.6 1.73 (0.47–5.33).3630 perforation (no vs. yes) Lens luxation (no 446 403/29 93.3/6.7 14/0 100.0/0.0.6136 vs. yes) Phthisis bulbi or 446 407/25 94.2/5.8 13/1 92.9/7.1 1.25 (0.07–6.69).8325 microphthalmos (no vs. yes) Proptosis bulbi (no 446 427/5 98.8/1.2 14/0 100.0/0.0 1.0000 vs. yes) Neoplasia (no vs. yes) 446 332/100 76.9/23.1 12/2 86.7/14.3 0.55 (0.09–2.07).4440 Other cause for 446 415/17 96.1/3.9 13/1 92.9/7.1 1.88.5552 enucleation (no vs. (0.10–10.31) yes) Presumed infected 446 350/82 81.0/19.0 10/4 71.4/28.6 1.71 (0.46–5.25).8845 (no vs. yes) Amoxicillin- 446 76/356 17.6/82.4 1/13 7.1/92.9 2.78.3294 clavulanate (no vs. (0.54–50.80) yes) Enrofloxacin (no vs. 446 409/23 94.7/5.3 7/7 50.0/50.0 17.78.0000006 yes) (5.66–56.27) Cefovecin (no vs. yes) 446 381/51 88.2/11.8 14/0 100.0/0.0.3856 Pseudomonas spp.(no 48 36/5 87.8/12.2 3/4 42.9/57.1 9.60 (1.68–63.1).0120 vs. yes) Staphylococcus (no 48 30/6 83.3/16.7 9/3 75.0/25.0 1.67 (0.30–7.79).5246 vs. yes) No complications Complications No. of p- Metric variables operations n Mean n Mean OR (95% CI) value Age (years) 443 432 9.20 14 8.77 0.97 (0.87–1.11).6708 Antibiotic therapy length (days) 446 432 7.03 14 10.86 1.21 (1.09–1.36).0002 (Continues) 10 | ALLGOEWER and SOUKUP TABLE 1 (Continued) No complications Complications No. of p- Metric variables operations n Mean n Mean OR (95% CI) value Anti-inflammatory therapy length 446 432 9.01 14 10.21 1.15 (0.97–1.34).1551 (days) Abbreviations: CI, confidence interval, OD, right eye, OR, odds ratio; OS, left eye. a CI and p-value were computed without the rabbits. b OR is in comparison to female. c Surgeons with few operations and no complications excluded. Ophthalmic Surgery (2021).26 An advantage of this ap- nerve nor did we employ electrocautery. Moreover, au- proach is a better overview of the orbital tissues during thors reported a difference in RBL between a retrobulbar dissection. Nonetheless, these texts still suggested clamp- block and a splash block (1.0% ± 0.8% and 1.9% ± 1.5% re- ing of the optic nerve. The lateral approach was mentioned spectively).17 In our study, no additional locoregional an- again when a modified lateral technique was presented.11 esthesia was applied. To the best of our knowledge, our The ophthalmic artery is the main artery for the eye in study is the first one to report ABL and RBL after enu- humans.13 In companion animals, the corresponding in- cleation in cats as 1.54–38.48 mL (median 11.42 mL) and ternal ophthalmic artery becomes rudimentary after birth 0.51%–11.80% (median 4.1%). The numbers are higher for and is supplemented by a larger external ophthalmic ar- cats than for dogs, partly because the reported circulating tery. The blood supply of the eyeball and its accessory or- blood volume per kg is lower than in dogs.17,20 Despite gans is provided by several smaller arteries that branch this numerical difference, no increased postoperative or within the orbit (Figures 1, 2). Therefore, a mass ligation post anesthesia complications were noted in comparison or clamping of the orbital vasculature and the optic nerve to dogs. will be relatively ineffective. Based on this, the authors of Complications of enucleation surgery described in the this paper believe that attempts to clamp the vasculature literature include surgical site infection (SSI)4 or likewise associated with the optic nerve are not necessary. The mentioned orbital cellulitis,5 cystic tissue formation,24,25 modified lateral technique described in the present paper orbital emphysema,27,28 blindness and optic neuropathy is Bellhorn's lateral approach omitting clamping and/or in the contralateral eye22,23 as well as implant migration ligation of the optic nerve and surrounding tissues. This and extrusion in orbits with silicone prosthesis.5 A lim- is described here for the first time in the literature after it itation of our study could be the mean follow-up time of was previously presented in 2006.11 128.7 days with median of 12 days (7–1245 days). Long- As mentioned earlier, according to the literature, one of term complications might be missed. However, owners the differences between the subconjunctival and transpal- were instructed to report back if any long-term complica- pebral enucleation technique is the blood loss during the tions would occur. procedure21 with the blood loss being higher in the trans- Generally, in soft tissue surgery, the incidence of SSI palpebral technique. However, only recently a first peer in dogs was reported to be up to 8.7%.29 For enucleations reviewed publication estimating blood loss during enucle- in dogs, Dacanay reported an SSI of 5% (14/280),4 Palmer ation in dogs has been published.17 The authors reported noted an SSI rate of 6.5% (14/215),5 whereas our data re- a median RBL of 1.3% (0.1%–6.7%) with a mean RBL of vealed a much lower incidence of SSI of 2.08% with ap- 1.3 ± 1.2% (n = 112) for the subconjunctival approach and proximately five times more cases (27/1296). Reported a mean RBL of 2.2 ± 1.6% (n = 18) for the transpalpebral median follow-up was 14 days4 which is similar to our approach. In that study, hemostasis with electrocautery median of 12 days, whereas Palmer reported a median fol- was routinely used by 3 out of 8 surgeons, whereas 3/8 low-up of 147 days.5 It is noteworthy that 50% of dogs de- surgeons routinely placed mosquito forceps around the veloping complications had concurrent diabetes mellitus apical vasculature and optic nerve before transection. (27.5% complication incidence in diabetes mellitus cases)5 Ligation was not performed by any of the surgeons. In whereas none of the dogs in our risk factors evaluation our canine data, we achieved a similar RBL (median 2.2%, that developed complications had a known diabetic sta- 0.19%–7.74%) when compared to the transpalpebral enu- tus. We had a very low incidence of orbital emphysema cleation technique, which is not surprising as the lateral in 0.08% cases (1/1296). No cases of cystic tissue forma- enucleation technique was developed as a modification tion were observed after the modified approach25 while of the transpalpebral approach.2 However, in our study, a recent retrospective evaluation of 201 enucleations re- neither did we use clamping of the vasculature and optic vealed five cases of orbital cysts (2.5%), all of them after ALLGOEWER and SOUKUP | 11 transconjunctival approach.24 We assume that due to the Pseudomonas spp. are a known cause of surgical site and inherent nature of these techniques, the modified lateral nosocomial infections in both humans and animals,30–32 approach as well as the transpalpebral approach are not so this finding is not surprising. To compare the risk prone to leaving conjunctival tissue behind and thus do factor evaluation, Dacanay et al. concluded that no risk not cause cyst development. Also, we did not experience a factors have been identified to guide clinical decision- single case of blindness or optic neuropathy in the contra- making for prevention of surgical site infections.4 Apart lateral eye after enucleation. As described, the lateral ap- from a Pseudomonas bacterial culture, we conclude that proach was developed to increase exposure of the orbital no other risk factors had influence on the development structures, especially the optic nerve.2 The modification of complications in our study. of the lateral technique by abandoning ligation or clamp- One potential risk factor that did not reach statisti- ing of the optic nerve adds safety to the procedure as the cal significance but should receive special attention is risk of damage of the optic nerve and chiasm is reduced. presumed ocular surface infection (or as mentioned by Strictly speaking, ligation or clamping of the optic nerve Dacanay et al.4 as “non-clean enucleation”). An important and surrounding tissues during enucleation is contrain- consideration when deciding to use transconjunctival ver- dicated as it may result in rostral traction with chiasmal sus transpalpebral enucleation technique is the presumed injury leading to blindness in the contralateral eye. This ocular surface infection. Transpalpebral approach is gen- has been described in the cat.22 erally believed to be cleaner than transconjunctival ap- In our detailed review of enucleation cases, we strove proach.9,21 Dacanay et al. found no statistical significance to identify risk factors for the development of postsur- between these two approaches and SSI. Nevertheless, gical complications. Most of the potential risk factors they evaluated the dataset in univariable fashion and did not influence the development of complications relationship between surgical approach in “clean” and (Table 1). Three variables were statistically significantly “non-clean” eyes was not shown.4 Our data did not find associated with cases that developed complications: du- any statistical significance between presumed ocular in- ration of antibiotic therapy (p <.001), animals treated fection and incidence of SSI. Moreover, given the fact that with enrofloxacin (p <.001), and positive Pseudomonas SSI incidence in our study was much lower than SSI rate spp. bacterial culture (p <.05). Understandably, the reported in other studies utilizing both transpalpebral and length of the antibiotic therapy was directly correlated subconjunctival approach,4,5 we believe that even though to complications, as most of the complication cases were the surgical field in the lateral approach must be consid- surgical site infections that required prolonged antibiotic ered contaminated, it does not increase risk for develop- therapy. This variable is also connected to the second one ment of SSI even in presumed ocular surface infection. We that is, animals treated with enrofloxacin. Enrofloxacin, believe that the choice of the surgical approach does not a fluoroquinolone antibiotic with indication restriction, play such an important role as previously stated.9,21 was used in 10.45% of the cases (30/287, no cats having A special category that was included in the present been treated with enrofloxacin). In 23 cases, enrofloxacin study was postoperative self-trauma to the wound/pruri- was the first postoperative antibiotic based on preopera- tus with local erythema and alopecia. We wanted to de- tive bacterial culture or concurrent systemic disorder. In fine what percentage of animals scratch their wound or seven cases, it was used as a second line treatment after surgical area after enucleation, as no E-collar was used developing complications after the first line antibiotics. in our clinical setting. Dogs were scratching their wound Therefore, it is clear that the statistical significance of en- in 0.92% of cases (7/762) whereas cats had a higher in- rofloxacin results is more of a consequence than a cause cidence of 4.78% (24/502). This phenomenon, especially of complications as it was used in cases that were already in cats, did not happen directly after the surgery, but it prone to the development of complications. We believe appeared between days 4 and 12 postoperatively. In one that this finding is similar to the previously published case, it disappeared as late as 2 months after surgery, when statistical significance of postoperative use of cepha- the primary wound had already healed for 45 days. In lit- lexin.4 The latter antibiotic was only used in 6.8% of cases erature, post-enucleation pruritus was described in 28.6% in the present study (13/191) and three of those devel- (4/14) of cats, presumably due to the resorptive phase of oped complications. The third statistically significant the suture.33 In a recent retrospective enucleation evalu- variable was positive Pseudomonas spp. bacterial cul- ation presented by Bott et al., 2.5% of cases (5/201) also ture (which summarized both pre-and perioperative for developed “severe pruritus” postoperatively without any those “presumed infected” cases or postoperative when further specification.24 Cats seem to be overrepresented SSI develop). Pseudomonas spp. was cultivated from for that phenomenon and periocular Herpesvirus FHV-1 44.4% (4/9) of cases with complications as compared to infection may play a role in the etiopathogenesis of the 7.69% (3/39) of cases without complications. Different pruritus.34 12 | ALLGOEWER and SOUKUP 3. Kuhns E. Enucleation of the eye by subconjunctival ablation. In summary, this comprehensive study confirms that Vet Med Small Anim Clin. 1976;71:1433-1440. modified lateral enucleation without clamping of the optic 4. Dacanay SJ, Barber RM, Diehl KA, Myrna KE. Incidence nerve head and its surrounding tissues is a safe procedure and risk factors for surgical site infection following enucle- with minimal complications and blood loss comparable ation in dogs. Front Vet Sci. 2023;9:1086956. doi:10.3389/ to a routine transpalpebral technique. Based on anatom- fvets.2022.1086956 ical considerations, ligation or clamping is not necessary 5. Palmer SV, Ramos RV, Woodoff- Leith ED, Galarza RMR. when an enucleation is performed in small animals. Causes, outcomes, and owner satisfaction of dogs undergoing enucleation with orbital implant placement. Vet Ophthalmol. 2021;24(4):346-353. doi:10.1111/vop.12892 AUTHOR CONTRIBUTIONS 6. Hamzianpour N, Smith K, Dawson C, Rhodes M. Bilateral enu- Ingrid Allgoewer: Conceptualization; data curation; cleation in dogs: a review of owner perceptions and satisfaction. formal analysis; funding acquisition; investigation; meth- Vet Ophthalmol. 2019;22(5):566-576. doi:10.1111/vop.12623 odology; resources; supervision; validation; visualization; 7. Slatter DH, Basher T. Orbit. In: Slatter DH, ed. Textbook of writing – original draft; writing – review and editing. Petr Small Animal Surgery. 3rd ed. W.B. Saunders; 2003:1430-1454. Soukup: Conceptualization; data curation; formal analy- 8. Kern TJ. The canine orbit. In: Gelatt KN, ed. Veterinary Ophthalmology. 2nd ed. Lea & Febiger; 1991:239-255. sis; investigation; methodology; validation; visualization; 9. Pot SA, Voelter K, Kircher PR. Diseases and surgery of the ca- writing – original draft; writing – review and editing. nine orbit. In: Gelatt KN, ed. Veterinary Ophthalmology. Vol 2. 6th ed. Wiley-Blackwell; 2021:879-922. ACKNOWLEDGMENTS 10. Maggs DJ, Miller PE, Ofri R. Slatter's Fundamentals of We thank Claudia Schlueter for the preparation of the Veterinary Ophthalmology. 6th ed. Elsevier Saunders; 2018. casts of Figure 1B,D. We would like to express our special 11. Allgoewer I, Noeller C, Reese S. Enucleation: is ligation nec- thanks to Paul Simoens for supplying the photos of the essary? In: Abstracts: 37th Annual Meeting of the American casts of the orbital vasculature (Figure 2), elaborating the College of Veterinary Ophthalmologists, San Antonio, TX, USA. November 1–4, 2006. Vet Ophthalmol. 2006;9:414-425. drawings of Figure 1A,C as well as critically reviewing doi:10.1111/j.1463-5224.2006.00520.x the manuscript—specifically the anatomy of the orbital 12. Simoens P. Ocular vascularization. In: Salomon U, Geyer H, vasculature—providing most valuable comments and Gille H, eds. Anatomie Für Die Tiermedizin. Enke Verlag; 2005. improving the manuscript. We are honored and grate- doi:10.1055/b-002-35730 ful that Roy Bellhorn previewed our manuscript. The 13. Bird B, Stawicki SP. Anatomy, Head and Neck, Ophthalmic described technique is based on Roy Bellhorn's original Arteries. StatPearls Publishing LLC; 2024. concept. 14. R-Core-Team. R: a language and environment for statistical com- puting. R foundation for statistical. Vienna, Austria: Computing. 2023; https://www.R-project.org/ CONFLICT OF INTEREST STATEMENT 15. Zeileis A, Köll S, Graham N. Various versatile variances: an The authors declare no conflicts of interest. object-oriented implementation of clustered covariances in R. J Stat Softw. 2020;95(1):1-36. doi:10.18637/jss.v095.i01 DATA AVAILABILITY STATEMENT 16. Zeileis A, Hothorn T. Diagnostic checking in regression rela- Data available in article supplementary material. tionships. R News. 2002;3(2):7-10. https://api.semanticscholar. org/CorpusID:13220158 ETHICS STATEMENT 17. Lenihan E, Baines SJ, Linn-Pearl RN, et al. Estimation of the intraoperative blood loss in dogs undergoing enucleation. Vet The study was performed according to GERVO guidelines Ophthalmol. 2023;26(1):19-30. doi:10.1111/vop.13035 and was approved by the responsible authority (Landesamt 18. Schorn MN. Measurement of blood loss: review of the literature. für Gesundheit und Soziales, Berlin, Germany) under the J Midwifery Womens Health. 2010;55(1):20-27. doi:10.1016/j. registration number StNo 009-2023. jmwh.2009.02.014 19. Vitello DJ, Ripper RM, Fettiplace MR, Weinberg GL, Vitello JM. ORCID Blood density is nearly equal to water density: a validation study Ingrid Allgoewer https://orcid. of the gravimetric method of measuring intraoperative blood org/0000-0002-2939-4213 loss. J Vet Med. 2015;2015:152730. doi:10.1155/2015/152730 20. Mott JC. The effect of haemorrhage on haemoglobin con- Petr Soukup https://orcid.org/0000-0001-6125-8580 centration, blood volume and arterial pressure in kittens and cats. J Physiol. 1968;194(3):659-667. doi:10.1113/jphysiol.1968. REFERENCES sp008431 1. Wolf E. Enucleation of the globe. In: Bojrab MJ, ed. Current 21. Gelatt KN, Gelatt JP, Plummer CE. Surgical instrumentation. Techniques in Small Animal Surgery. 3rd ed. Lea & Febiger; Veterinary Ophthalmic Surgery. 2st ed. Saunders Ltd.; 2021. 1990:119-123. 22. Donaldson D, Riera MM, Holloway A, Beltran E, Barnett KC. 2. Bellhorn R. Enucleation technique: a lateral approach. J Am Contralateral optic neuropathy and retinopathy associated Anim Hosp Assoc. 1972;8:59-60. with visual and afferent pupillomotor dysfunction following ALLGOEWER and SOUKUP | 13 enucleation in six cats. Vet Ophthalmol. 2014;17(5):373-384. aureus. Expert Rev Anti-Infect Ther. 2015;13(5):605-613. doi:10 doi:10.1111/vop.12104.1586/14787210.2015.1023291 23. Stiles J, Buyukmihci NC, Hacker DV, Canton DD. Blindness from 32. Lyczak JB, Cannon CL, Pier GB. Establishment of damage to optic chiasm. J Am Vet Med Assoc. 1993;202(8):1192. Pseudomonas aeruginosa infection: lessons from a versatile 24. Bott M, Heitz E, Jondeau C, Chahory S. Orbital cysts post- opportunist. Microbes Infect. 2000;2(9):1051-1060. doi:10.1016/ enucleation in dogs and cats: a retrospective study (2017-2022). s1286-4579(00)01259-4 Abstracts: Annual Scientific Meeting of the European College 33. Thienel F. Wundheilung Und Kosmetische Aspekte Nach of Veterinary Ophthalmologists. 2023. Vet Ophthalmol. 2024; Enukleation Unter Berücksichtigung Verschiedener 27:e1-39. doi:10.1111/vop.13245 Operationsverfahren Bei Hund Und Katze. Free University of 25. Ward AA, Neaderland MH. Complications from residual Berlin; 2018. adnexal structures following enucleation in three dogs. J 34. Gould D. Feline Herpesvirus- 1. J Feline Med Surg. Am Vet Med Assoc. 2011;239(12):1580-1583. doi:10.2460/ 2011;13(5):333-346. doi:10.1016/j.jfms.2011.03.010 javma.239.12.1580 26. Gelatt KN, Gelatt JP. Handbook of small animal ophthalmic surgery. Volume 1. Extraocular Procedures. 1st ed. Butterworth- SUPPORTING INFORMATION Heinemann Ltd; 1994. Additional supporting information can be found online 27. Bedford PGC. Orbital pneumatosis as an unusual compli- in the Supporting Information section at the end of this cation to enucleation. J Small Anim Pr. 1979;20(9):551-555. article. doi:10.1111/j.1748-5827.1979.tb06765.x 28. Gornik KR, Pirie CG, Alario AF. Orbital and subcutaneous emphysema following enucleation and respiratory distress in a Japanese Chin. J Am Anim Hosp Assoc. 2015;51(6):413-418. How to cite this article: Allgoewer I, Soukup P. doi:10.5326/jaaha-ms-6279 29. Espinel- Rupérez J, Martín- Ríos MD, Salazar V, Baquero- Modified lateral enucleation technique—Surgery Artigao MR, Ortiz-Díez G. Incidence of surgical site infection without ligation or clamping of the optic nerve: in dogs undergoing soft tissue surgery: risk factors and eco- Technique description, complication rate and risk nomic impact. Vet Rec Open. 2019;6(1):e000233. doi:10.1136/ factors, and intraoperative blood loss estimation in vetreco-2017-000233 companion animals. Vet Ophthalmol. 2024;00:1-13. 30. Padhy A, Mishra R, Behera SS, Sahu AR, Sahoo S. Microbial doi:10.1111/vop.13293 profile of canine persistent wound infections. Vet World. 2014;7(4):244-247. doi:10.14202/vetworld.2014.244-247 31. Serra R, Grande R, Butrico L, et al. Chronic wound infections: the role of Pseudomonas aeruginosa and Staphylococcus

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