Introduction
Pneumonia is a known complication of general anesthesia in horses, though the true incidence is unknown, and early diagnosis can be challenging.1–5 In 113 horses anesthetized for emergency celiotomy, 42% (48/113) developed postoperative infections, and 7% (8/113) were diagnosed with pneumonia.2 Recent anesthesia has also been identified as a risk factor for pneumonia in multiple retrospective studies1,3,5 investigating equine pneumonia. In humans and dogs, postanesthetic pneumonia can be attributed to atelectasis, trauma from endotracheal intubation, and aspiration of gastric contents during intubation.6–8 In the horse, there is a paucity of knowledge on the exact pathophysiology of postanesthetic pneumonia, though tracheal trauma from intubation, mechanical ventilation, and aspiration of gastric reflux have been suggested.1,9 Equine practitioners rely heavily on thoracic ultrasonography (TUS) for the identification of pneumonia. Changes in the pleura that support a diagnosis of pneumonia include the presence of comet tails or B-lines, consolidation, and accumulation of pleura effusion.4,10 Atelectasis and pulmonary edema, which have been more commonly reported than pneumonia following anesthesia, also often cause these changes, making differentiation difficult following anesthesia.4,11,12
The presence of fever in horses following colic surgery is a common clinical finding that can be caused by catheter site inflammation or infection, incisional infections, peritonitis, or pneumonia.2,6,7,13–15 In patients that develop fevers following general anesthesia, ruling out pneumonia as the source is critical, but can be complicated by ultrasonographic similarities between atelectasis, pulmonary edema, and pneumonia.4,16,17 To make this determination in sick horses following general anesthesia, it is first crucial to know what ultrasonographic changes may be present in healthy horses following general anesthesia for elective procedures.18
The objective of this study was to compare TUS findings in healthy horses before and after general anesthesia for elective MRI utilizing a recently developed ultrasonographic scoring system.19 The authors hypothesized that there would be a significant difference in TUS score before and after general anesthesia and that for horses positioned in lateral recumbency, the dependent side would have significantly higher TUS scores than the nondependent side.
Materials and Methods
This study was a prospective case control study utilizing horses > 3 years of age that were presented for elective MRI for orthopedic disease. Exclusion criteria included any history of respiratory or cardiac disease or presence of any of the following risk factors for respiratory disease in the 90-day period preceding the study: transport of > 6 consecutive hours, esophageal obstruction, or general anesthesia. Client consent was obtained for the use of each animal, and all protocols were approved by the IACUC. Each patient had a physical examination, rebreathing examination, and CBC performed prior to anesthesia and inclusion in the study. Physical examination was considered normal if vital parameters were within normal limits (rectal temperature, < 38.6 °C; heart rate, 28 to 48 beats/min; respiration, 10 to 20 breaths/min) and there was no nasal discharge, cough, abnormal lung sounds on auscultation, or increased respiratory effort. Patients that had abnormal physical examinations or CBCs, displayed coughing, or had abnormal lung sounds noted during or after the rebreathing examination were excluded from the study.
Scoring of radiographic findings
Following the initial examination, a standard series of right to left lateral thoracic radiographic images was taken of each patient to confirm the absence of deep pulmonary pathology. Thoracic radiographic images were evaluated by a board-certified radiologist (NCN) utilizing a previously described system.20 The cranioventral, caudodorsal, and caudoventral section of each lung was assessed for the presence of vascular, alveolar, interstitial, and bronchial radiographic patterns. Each section was given a score of 0 if the region was considered normal, a score of 1 for each pattern of which there was a moderate presence, and a score of 2 for each region where there was considered to be a “marked presence” of a specific pattern. When each region was evaluated for all 4 radiographic patterns, a total score range of 0 to 24 was determined. Radiography was not repeated following anesthesia.
Scoring of ultrasonographic findings
For all patients deemed to have normal findings on thoracic radiography and physical examinations, TUS examinations were performed within 6 hours of radiography and scored based on a novel scoring system developed by the authors.19 Ultrasonographic examinations were performed by a board-certified internal medicine specialist (KHW). Ultrasonography was performed by imaging each intercostal space (ICS) from dorsal to ventral with a 3.5-MHz curvilinear probe in B-mode with the depth adjusted to maximize the image. Since horses were client owned and many were being used in competition, hair was not clipped. Isopropyl alcohol was used as a coupling agent. Ultrasonography was performed with 1 of 2 identical machines (Sonoscape S9; Universal Imaging). Each ICS was scored as previously described.19 Briefly, the dorsal and ventral portion of each ICS was evaluated for the presence of comet tail artifacts, consolidation, and pleural effusion. The point of the shoulder was utilized as the point of reference dividing dorsal from ventral. Comet tails were defined as linear hyperechoic artifacts extending 5 mm or more perpendicularly from the pleural surface and were quantified in each ICS. Consolidation was defined as any region where the pleura was disrupted and pleural fluid was identified by the presence of anechoic or echogenic material between the pleural surface and body wall. If either consolidation or effusion was present, a score of 4 was assigned, whereas a score of 0 was assigned if these changes were absent. If no lung was visible in an ICS, then no number was assigned. The scores for the right hemithorax and left hemithorax and the total score were recorded for each horse.
Anesthesia protocol
Each patient was induced with ketamine and propofol and maintained with injectable anesthesia (either constant rate infusion of dexmedetomidine or a combination of ketamine, guaifenesin, and xylazine) at the discretion of the supervising anesthesiologist. The duration of anesthesia, recumbency of patient during anesthesia, time to recovery, and time that patient stood following anesthesia were recorded. Postanesthesia physical examination findings and ultrasonographic examinations were performed within 3 hours of the patient standing.
Results
Thirteen horses were enrolled in the study, including 6 Quarter Horses, 5 warmbloods, 1 Thoroughbred, and 1 Arabian. Ten horses were geldings and 3 were mares. Horses had a median weight of 583 kg (range, 473 to 656 kg) and a median age of 9 years (range, 6 to 19 years). Anesthesia was induced with ketamine (2.2 to 3 mg/kg, IV) and propofol (0.5 mg/kg, IV) in all horses. Nine horses were maintained with a constant rate infusion of dexmedetomidine (0.5 to 1 µg/kg/min), and a combination of guaifenesin, ketamine and xylazine (1 L 5% guaifenesin, 500 mg xylazine, 1 g ketamine administered at 1 to 3 mL/kg/h to effect). The remaining 4 horses were maintained on a constant rate infusion of dexmedetomidine (0.5 to 1 µg/kg/min). All horses were mechanically ventilated during anesthesia. Patients were anesthetized for a median of 114 minutes (range, 59 to 133 minutes) and were recumbent for a median of 166 minutes (range, 119 to 205 minutes). Anesthesia time was measured from induction until discontinuation of constant rate infusions. Time recumbent was measured from induction to the time that the horse stood in the recovery box. All horses recovered uneventfully from anesthesia and were recovered in the same laterality in which they had been anesthetized. Ten of 13 horses were positioned in right lateral recumbency, and the remaining 3 were positioned in left lateral recumbency. Median duration from the time that the horse stood to the postanesthesia examination was 106 minutes (range, 49 to 165 minutes). Median preanesthetic radiographic score was 0 (range, 0 to 2). Eight of 13 horses had radiographic scores of 0, 3 horses had radiographic scores of 1, and 2 horses had radiographic scores of 2. All findings on radiography were considered normal.
There was no significant difference in total median ultrasonography scores between pre- (median score, 20) and postanesthesia (median score, 18) examinations (P = .196). Median TUS scores on the left and right side also did not differ significantly from the preanesthetic examination (median right, 10; median left, 10) to postanesthetic examination (median right, 10 [P = .27]; median left, 13 [P = .726]). There was no significant difference in ultrasonography scores between each patient’s dependent side and nondependent side (P = .61). There was no significant correlation between the duration of time from standing to the time of the second examination with the change in TUS score on the right side (P = .40), the left side (P = .55), or the total TUS score (P = .40). There was no significant correlation between the duration of anesthesia and changes in the TUS score on the left side (P = .88), the right side (P = .56), and the total score (P = .57).
There was no significant correlation between the patient’s weight and the changes on the left side (P = .16), the right side (P = .77), and total score (P = .32). There was a significant correlation between the changes in score and the patient’s age on the right side (r = 0.65; P = .02), but not between age and the change on the left side (P = .62) and the total score (P = .63).
Discussion
In the data presented here, healthy horses were anesthetized for elective MRI, and TUS was determined before and after anesthesia. Contrary to a previous study,18 there were no significant changes noted in the TUS scores within 3 hours of the horses standing in recovery. Though Ribonnet et al18 found significant changes in numbers of specific lesions up to 6 hours after anesthesia, the only statistically significant differences between the total preanesthesia score and the postanesthesia score occurred up to the 2-hour time point after recovery. In our study, the median time from standing to the postanesthesia TUS examination was 106 minutes, with a range of 49 to 165 minutes. Forty-six percent (6/13) of the 13 horses in our study were examined at > 2 hours after standing, so it is plausible that the additional time before the second TUS examination allowed for re-expansion of the lungs and resolution of atelectasis, accounting for the lack of significant differences between total scores. However, in our data set, there was also no significant correlation between the change in total score and the duration of time that lapsed between the time the horse stood and the time the postanesthesia examination was performed. Another potential explanation for the absence of significant changes in our patients was the more rigorous exclusion criteria and preanesthetic diagnostics utilized in our study, including rebreathing examination and thoracic radiography. Any horse that had risk factors for preexisting respiratory disease, including asthma, history of esophageal obstruction, or long-distance transportation was excluded from our study; thus, it is also conceivable that some horses in the study by Ribonnet et al18 may have had subclinical pulmonary disease that was exacerbated by anesthesia.
Pathology of the upper and lower respiratory tract composes a significant portion of all complications following general anesthesia in horses.9,15,21–28 In a retrospective study21 evaluating complications following general anesthesia of 1,161 horses, the overall complication rate was 17.5% (204/1,161); 22.6% (46/204) of the complications were respiratory. In a group of 46 horses with pneumonia caused by Klebsiella spp, general anesthesia with mechanical ventilation preceded the development of pneumonia in 23.9% (11/46) of horses.1 Similarly, 9.5% (11/116) of horses diagnosed with pneumonia at North Carolina State University over an 11-year period underwent general anesthesia prior to the development of pneumonia.29 Early identification of these complications can be challenging, as pneumonia, atelectasis, and pulmonary edema lead to similar ultrasonographic changes and there are minimal data available specific to horses describing the degree of ultrasonographic change that may be present in normal, healthy horses following general anesthesia.18,30–32
Atelectasis in humans occurs within minutes of induction of anesthesia and can persist for 24 to 48 hours after recovery.33,34 It can be identified via CT, thoracic radiography, and TUS.30,35 In horses, atelectasis is known to occur during anesthesia, though identification is more troublesome due to the inability to perform CT of the equine thorax. It is also unknown how long atelectasis persists following general anesthesia in horses. Since horses stand immediately after recovery, as opposed to remaining recumbent for prolonged periods of time as in other species, it is impossible to extrapolate from these species how long atelectasis may last. In our study, 77% (10/13) of the horses were anesthetized and recovered in right lateral recumbency, and we identified a significant correlation between the change in TUS score on the right side of the thorax and age, but not between the left side or the total score in age. While this finding may be due to a larger number of horses being positioned in right lateral recumbency (n = 10) as opposed to left lateral recumbency (3), it is possible that older horses may be more prone to developing atelectasis in the dependent lung and that ultrasonographic changes in older horses may be indicative of mild atelectasis following anesthesia.
Eighty-five percent (96/113) of horses that undergo exploratory celiotomy develop mild to moderate pyrexia in the postoperative period, one cause of which can be pneumonia.2 Horses that undergo anesthesia for colic surgery and those with prolonged anesthesia times are also at a higher risk of developing respiratory complications than horses anesthetized for other procedures.21,26,36 Laurenza et al21 identified a significant association between respiratory complications and colic surgery, duration of recovery, duration of anesthesia, and lower PaO2 and FiO2. In the population of healthy horses described in our study, there was no correlation between total anesthetic time or total time recumbent and TUS score following anesthesia. Additionally, all pre- and postanesthesia TUS scores (18 and 20, respectively) were < 37, which was identified as a cutoff value for healthy horses in a previous study.19 The results of this study are consistent with previous findings that healthy horses are likely at lower risk of developing respiratory complications following general anesthesia.37,38
There were a number of limitations in this study. Like many equine studies, there was a small number of subjects, which may have contributed to the lack of significant changes noted before and after anesthesia. Only one TUS examination was performed following anesthesia in each horse, and the second examination was completed within 3 hours of standing but happened at varying times within that time frame. However, there was no association with the change in TUS score and the duration of time from standing to the second examination. Though the performance of only 1 examination may have led to changes in the immediate postrecovery period being missed, the aim was to mirror clinical practice, and more than 1 examination is typically impractical in a short period of time. Only 1 clinician performed the TUS examinations, which may have led to some bias with knowledge of specific patients. Lastly, since radiography was not performed following anesthesia, deep pulmonary lesions could not be ruled out completely. However, thoracic radiography in horses is less sensitive in identification of subtle lesions; thus, repeated radiography after anesthesia was likely of low diagnostic yield.38
The data presented here show that in healthy horses anesthetized for elective MRI, there is no significant change in the ultrasonographic appearance of the pleura within 3 hours after recovery from anesthesia. Further studies are warranted to investigate the degree of change visible on TUS following general anesthesia in sick horses, especially those anesthetized for emergency exploratory celiotomy for colic, as these animals are at higher risk for anesthetic complications. It could be advantageous to pursue preanesthetic TUS in high-risk cases to allow for more informed decision-making during the immediate postoperative period when practitioners are trying to determine the significance of ultrasonographic lesions in the thorax.
Acknowledgments
No external funding was used in this study. The authors declare that there were no conflicts of interest.
The authors would like to acknowledge James Robertson for his contribution to the statistical analysis, and the faculty, staff, and students of the North Carolina State College of Veterinary Medicine Teaching Hospital for assistance with case recruitment and data collection.
References
- 1.↑
Estell KE, Young A, Kozikowski T, et al. Pneumonia caused by Klebsiella spp. in 46 horses. J Vet Intern Med. 2016;30(1):314-321. doi:10.1111/jvim.13653
- 2.↑
Freeman KD, Southwood LL, Lane J, Lindborg S, Aceto HW. Post operative infection, pyrexia and perioperative antimicrobial drug use in surgical colic patients. Equine Vet J. 2012;44(4):476-481. doi:10.1111/j.2042-3306.2011.00515.x
- 3.↑
Raphel CF, Beech J. Pleuritis secondary to pneumonia or lung abscessation in 90 horses. J Am Vet Med Assoc. 1982;181(8):808-810.
- 4.↑
Reuss SM, Giguère S. Update on bacterial pneumonia and pleuropneumonia in the adult horse. Vet Clin North Am Equine Pract. 2015;31(1):105-120. doi:10.1016/j.cveq.2014.11.002
- 5.↑
Tomlinson JE, Reef VB, Boston RC, Johnson AL. The association of fibrinous pleural effusion with survival and complications in horses with pleuropneumonia (2002-2012): 74 cases. J Vet Intern Med. 2015;29(5):1410-1417. doi:10.1111/jvim.13591
- 6.↑
Ephgrave KS, Kleiman-Wexler R, Pfaller M, Booth B, Werkmeister L, Young S. Postoperative pneumonia: a prospective study of risk factors and morbidity. Surgery. 1993;114(4):815-819.
- 7.↑
Ovbey DH, Wilson DV, Bednarski RM, et al. Prevalence and risk factors for canine post-anesthetic aspiration pneumonia (1999-2009): a multicenter study. Vet Anaesth Analg. 2014;41(2):127-136. doi:10.1111/vaa.12110
- 8.↑
van Kaam AH, Lachmann RA, Herting E, et al. Reducing atelectasis attenuates bacterial growth and translocation in experimental pneumonia. Am J Respir Crit Care Med. 2004;169(9):1046-1053. doi:10.1164/rccm.200312-1779OC
- 9.↑
Diaz M, Hewetson M, Kaartinen J. Tracheal trauma and pneumonia secondary to endotracheal intubation in a horse undergoing general anaesthesia, computerised tomography and myelography. Equine Vet Educ. 2022;34(3):e106-e109. doi:10.1111/eve.13591
- 10.↑
Ferrucci F, Zucca E, Croci C, Di Fabio V, Martino PA, Ferro E. Bacterial pneumonia and pleuropneumonia in sport horses: 17 cases (2001-2003). Equine Vet Educ. 2008;20(10):526-531. doi:10.2746/095777308X354255
- 11.↑
Wagner AE. Complications in equine anesthesia. Vet Clin North Am Equine Pract. 2008;24(3):735-752, x. doi:10.1016/j.cveq.2008.10.002
- 12.↑
Reimer JM, Reef VB, Spencer PA. Ultrasonography as a diagnostic aid in horses with anaerobic bacterial pleuropneumonia and/or pulmonary abscessation: 27 cases (1984-1986). J Am Vet Med Assoc. 1989;194(2):278-282.
- 13.↑
Kazaure HS, Martin M, Yoon JK, Wren SM. Long-term results of a postoperative pneumonia prevention program for the inpatient surgical ward. JAMA Surg. 2014;149(9):914-918. doi:10.1001/jamasurg.2014.1216
- 14.
Grubb TL, Muir WW. Anaesthetic emergencies and complications: part 1. Equine Vet Educ. 2005;7:69-80. doi:10.1111/j.2042-3292.2005.tb01831.x
- 15.↑
Monticelli P, Adami C. Aspiration pneumonitis (Mendelson’s syndrome) as perianaesthetic complication occurring in two horses: a case report. Equine Vet Educ. 2019;31(4):183-187. doi:10.1111/eve.12781
- 16.↑
Lisciandro GR, Fosgate GT, Fulton RM. Frequency and number of ultrasound lung rockets (B-lines) using a regionally based lung ultrasound examination named vet BLUE (veterinary bedside lung ultrasound exam) in dogs with radiographically normal lung findings. Vet Radiol Ultrasound. 2014;55(3):315-322. doi:10.1111/vru.12122
- 17.↑
Ward JL, Lisciandro GR, Ware WA, Miles KG, Viall AK, DeFrancesco TC. Lung ultrasonography findings in dogs with various underlying causes of cough. J Am Vet Med Assoc. 2019;255(5):574-583. doi:10.2460/javma.255.5.574
- 18.↑
Ribonnet C, Palmers K, Saegerman C, Vanderperren K, van Galen G. Perioperative lung ultrasonography in healthy horses undergoing general anesthesia for elective surgery. J Vet Intern Med. 2022;36(3):1160-1172. doi:10.1111/jvim.16408
- 19.↑
Hepworth-Warren KL, Nelson N, Dembek KA, Young KAS. Comparison of thoracic ultrasonography and thoracic radiography between healthy adult horses and horses with bacterial pneumonia using a novel, objective ultrasonographic scoring system. Front Vet Sci. 2022;9:991634. doi:10.3389/fvets.2022.991634
- 20.↑
Mazan MR, Vin R, Hoffman AM. Radiographic scoring lacks predictive value in inflammatory airway disease. Equine Vet J. 2005;37(6):541-545. doi:10.2746/042516405775314899
- 21.↑
Laurenza C, Ansart L, Portier K. Risk factors of anesthesia-related mortality and morbidity in one equine hospital: a retrospective study on 1,161 cases undergoing elective or emergency surgeries. Front Vet Sci. 2020;6:514. doi:10.3389/fvets.2019.00514
- 22.
Kaartinen MJ, Pang DS, Cuvelliez SG. Post-anesthetic pulmonary edema in two horses. Vet Anaesth Analg. 2010;37(2):136-143. doi:10.1111/j.1467-2995.2009.00505.x
- 23.
Holbrook TC, Dechant JE, Crowson CL. Suspected air embolism associated with post-anesthetic pulmonary edema and neurologic sequelae in a horse. Vet Anaesth Analg. 2007;34(3):217-222. doi:10.1111/j.1467-2995.2006.00317.x
- 24.
Borer KE. Pulmonary oedema associated with anaesthesia for colic surgery in a horse. Vet Anaesth Analg. 2005;32(4):228-232. doi:10.1111/j.1467-2995.2005.00210.x
- 25.
Day TK, Holcombe S, Muir WW. Postanesthetic pulmonary edema in an Arab stallion. J Vet Emerg Crit Care (San Antonio). 1993;3(2):90-95. doi:10.1111/j.1476-4431.1993.tb00106.x
- 26.↑
Curto EM, Griffith EH, Posner LP, Walsh KT, Balko JA, Gilger BC. Factors associated with postoperative complications in healthy horses after general anesthesia for ophthalmic versus non-ophthalmic procedures: 556 cases (2012-2014). J Am Vet Med Assoc. 2018;252(9):1113-1119. doi:10.2460/javma.252.9.1113
- 27.
Johnston GM, Eastment JK, Wood J, Taylor PM. The confidential enquiry into perioperative equine fatalities (CEPEF): mortality results of phases 1 and 2. Vet Anaesth Analg. 2002;29(4):159-170. doi:10.1046/j.1467-2995.2002.00106.x
- 28.↑
Ronaldson HL, Monticelli P, Smith R, Adami C. Acute life-threatening laryngeal dysfunction in a draft horse recovering from general anesthesia: a case report. J Equine Vet Sci. 2020;91:103109. doi:10.1016/j.jevs.2020.103109
- 29.↑
Hallowell K, Dembek KA, Hepworth-Warren KL. An updated description of bacterial pneumonia in adult horses and factors associated with non-survival. Abstract in: Proceedings of the American College of Veterinary Internal Medicine Forum. American College of Veterinary Internal Medicine; 2022:E64.
- 30.↑
Acosta CM, Maidana GA, Jacovitti D, et al. Accuracy of transthoracic lung ultrasound for diagnosing anesthesia-induced atelectasis in children. Anesthesiology. 2014;120(6):1370-1379. doi:10.1097/ALN.0000000000000231
- 31.
Yu X, Zhai Z, Zhao Y, et al. Performance of lung ultrasound in detecting peri-operative atelectasis after general anesthesia. Ultrasound Med Biol. 2016;42(12):2775-2784. doi:10.1016/j.ultrasmedbio.2016.06.010
- 32.↑
Reef VB, Whittier M, Allam LG. Thoracic ultrasonography. Clin Tech Equine Pract. 2004;3(3):284-293. doi:10.1053/j.ctep.2005.02.006
- 33.↑
Eichenberger A, Proietti S, Wicky S, et al. Morbid obesity and postoperative pulmonary atelectasis: an underestimated problem. Anesth Analg. 2002;95(6):1788-1792. doi:10.1097/00000539-200212000-00060
- 34.↑
Strandberg A, Tokics L, Brismar B, Lundquist H, Hedenstierna G. Atelectasis during anaesthesia and in the postoperative period. Acta Anaesthesiol Scand. 1986;30(2):154-158. doi:10.1111/j.1399-6576.1986.tb02387.x
- 35.↑
Liu J, Chen SW, Liu F, Li QP, Kong XY, Feng ZC. The diagnosis of neonatal pulmonary atelectasis using lung ultrasonography. Chest. 2015;147(4):1013-1019. doi:10.1378/chest.14-1306
- 36.↑
Shnaiderman-Torban A, Steinman A, Ahmad WA, et al. Preoperative and intraoperative risk factors for post-anaesthetic pulmonary oedema in horses. Equine Vet Educ. 2021;35(1):e52-e60. doi:10.1111/eve.13646
- 37.↑
Mee AM, Cripps PJ, Jones RS. A retrospective study of mortality associated with general anaesthesia in horses: elective procedures. Vet Rec. 1998;142(11):275-276. doi:10.1136/vr.142.11.275
- 38.↑
Rodrigues NF, Giraud L, Bolen G, et al. Response to letter regarding “Comparison of lung ultrasound, chest radiographs, C-reactive protein, and clinical findings in dogs treated for aspiration pneumonia.” J Vet Intern Med. 2022;36(6):1856-1857. doi:10.1111/jvim.16558