A plethora of medical conditions that affect the respiratory system of camelids and that potentially alter respiratory function have been identified,1–4 yet functional analysis has rarely been performed in this species. Therefore, there is a lack of understanding of physiologic pulmonary function and the effect various diseases would have on respiratory mechanical function in camelids.
Diagnostic modalities that provide information regarding the function of the respiratory system can improve the identification of respiratory diseases that are not detected by conventional imaging techniques as well as aid in the characterization, localization, and objective assessment of response to treatment of many respiratory ailments.5 For example, measurement of FRC is helpful in identifying trapped gas within the alveoli, and values have been established for clinically normal animals of several domestic species, including llamas,6 cattle,7 sheep,1,8,9 horses,7,10,11 and dogs.12–14 Respiratory inductive plethysmography has been used to describe the breathing patterns of horses at rest15 and during exercise,16 foals with evoked obstructions of the proximal and distal portions of the airways,17 healthy llamas,6 and a llama with diaphragmatic paralysis.1 This test is also used to diagnose inflammatory airway disease and recurrent airway obstruction in horses.5,15,18 Both RRS and XRS, measured by FOT, are frequently used to characterize the degree of airway obstruction in horses.19–21 In a study6 in llamas, investigators found that RL measured via esophageal balloon pneumotachography (criterion-referenced standard) was positively correlated with RL measured via FOT, with the latter having the advantage of being less invasive and time-consuming.
Analysis of BALF can replace the need to obtain lung biopsy specimens in many patients and is frequently used to diagnose diffuse pulmonary disease such as inflammatory airway disease in horses.19,20,22,23 Analysis of results for cytologic examination and bacteriologic culture of BALF improves the sensitivity of the diagnosis of fungal pneumonia and tuberculosis in humans24 and may also be useful in the antemortem diagnosis of several conditions that affect alpacas, such as tuberculosis,25–29 nocardiosis,30 viral pneumonia,31,32 pulmonary neoplasia,33 fungal pneumonia,2,4,34 and Rhodococcus equi–associated pneumonia.35 Reference values for BALF cytologic examination have been established for several domestic species, including horses23 and dogs.36 Although BAL has been performed in a llama with histoplasmosis,34 no technique for the procedure or reference values for cytologic analysis of the BALF have been reported in camelids to our knowledge. Therefore, the purpose of the study reported here was to provide values for respiratory mechanical function and results of BALF cytologic examination in healthy adult alpacas, which would allow for the use of these diagnostic tools in clinical patients.
Bronchoalveolar lavage fluid
Forced oscillatory technique
Functional residual capacity
Peak expiratory flow
Peak inspiratory flow
Respiratory inductive plethysmography
Respiratory system resistance
Respiratory system reactance
Hans Rudolph, Kansas City, Mo.
Mila International Inc, Erlanger, Ky.
SPSS, version 12, SPSS Inc, Chicago, Ill.
Bedenice D, Mazan MR, Kuehn H, et al. Diaphragmatic paralysis due to phrenic nerve degeneration in a llama. J Vet Intern Med 2002; 16:603–606.
Smith JA. Noninfectious diseases, metabolic diseases, toxicities, and neoplastic diseases of South American camelids. Vet Clin North Am Food Anim Pract 1989; 5:101–143.
Hoffman AM. Clinical application of pulmonary function testing in horses. In: Lekeux P, ed. Equine respiratory diseases. Ithaca, NY: International Veterinary Information Services, 2002. Available at: www.ivis.org. Accessed Nov 01, 2008.
Lascola KM, Hoffman AM, Mazan MR, et al. Respiratory mechanics in sedated and nonsedated adult llamas. Am J Vet Res 2007; 68:676–684.
Mundie TG, Dodd KT, Lagutchik M. Relationship of functional residual capacity to various body measurements in normal sheep. Lab Anim Sci 1992; 42:589–592.
Aguilera-Tejero E, Pascoe JR, Smith BL, et al. Evaluation of a technique for detection of pulmonary hemorrhage in horses, using carbon monoxide uptake. Am J Vet Res 1994; 55:1032–1036.
Hoffman AM, Swanson LG, Bruns SJ, et al. Effects of tension of the girth strap on respiratory system mechanics in horses at rest and during hyperpnea induced by administration of lobeline hydrochloride. Am J Vet Res 2005; 66:1167–1174.
Amis TC, Jones HA. Measurement of functional residual capacity and pulmonary carbon monoxide uptake in conscious Greyhounds. Am J Vet Res 1984; 45:1447–1450.
Bedenice D, Rozanski E, Bach J, et al. Canine awake head-out plethysmography (HOP): characterization of external resistive loading and spontaneous laryngeal paralysis. Respir Physiol Neurobiol 2006; 151:61–73.
Hoffman A, Kuehn H, Riedelberger K, et al. Flowmetric comparison of respiratory inductance plethysmography and pneumotachography in horses. J Appl Physiol 2001; 91:2767–2775.
Marlin DJ, Schrotert RC, Cashman PM, et al. Movements of thoracic and abdominal compartments during ventilation at rest and during exercise. Equine Vet J Suppl 2002;(34):384–390.
Miller C, Hoffman AM, Hunter J. Thoracoabdominal asynchrony failed to grade airway obstructions in foals. J Appl Physiol 2000; 88:2081–2087.
Nolen-Walston RD, Kuehn H, Boston RC, et al. Reproducibility of airway responsiveness in horses using flowmetric plethysmography and histamine bronchoprovocation. J Vet Intern Med 2009; 23:631–635.
Derksen FJ, Brown CM, Sonea I, et al. Comparison of transtracheal aspirate and bronchoalveolar lavage cytology in 50 horses with chronic lung disease. Equine Vet J 1989; 21:23–26.
Hoffman AM, Mazan MR, Ellenberg S. Association between bronchoalveolar lavage cytologic features and airway reactivity in horses with a history of exercise intolerance. Am J Vet Res 1998; 59:176–181.
Derksen FJ, Robinson NE, Armstrong PJ, et al. Airway reactivity in ponies with recurrent airway obstruction (heaves). J Appl Physiol 1985; 58:598–604.
Hoffman AM. Bronchoalveolar lavage: sampling technique and guidelines for cytologic preparation and interpretation. Vet Clin North Am Equine Pract 2008; 24:423–435.
Baughman RP, Dohn MN, Loudon RG, et al. Bronchoscopy with bronchoalveolar lavage in tuberculosis and fungal infections. Chest 1991; 99:92–97.
Oevermann A, Pfyffer GE, Zanolari P, et al. Generalized tuberculosis in llamas (Lama glama) due to Mycobacterium microti. J Clin Microbiol 2004; 42:1818–1821.
Frank W, Reisinger EC, Brandt-Hamerla W, et al. Mycobacterium microti-pulmonary tuberculosis in an immunocompetent patient. Wien Klin Wochenschr 2009; 121:282–286.
Zanolari P, Robert N, Lyashchenko KP, et al. Tuberculosis caused by Mycobacterium microti in South American Camelids. J Vet Intern Med 2009; 23:1266–1272.
Galbreath EJ, Holland RE, Trapp AL, et al. Adenovirus-associated pneumonia and hepatitis in four llamas. J Am Vet Med Assoc 1994; 204:424–426.
Williams JR, Evermann JF, Beede RF, et al. Association of bovine herpesvirus type 1 in a llama with bronchopneumonia. J Vet Diagn Invest 1991; 3:258–260.
Creevy KE. Airway evaluation and flexible endoscopic procedures in dogs and cats: laryngoscopy, transtracheal wash, tracheobronchoscopy, and bronchoalveolar lavage. Vet Clin North Am Small Anim Pract 2009; 39:869–880.
Van Saun RJ. Nutritional requirements and assessing nutritional status in camelids. Vet Clin North Am Food Anim Pract 2009; 25:265–279.
Young SS, Tesarowski D, Viel L. Frequency dependence of forced oscillatory respiratory mechanics in horses with heaves. J Appl Physiol 1997; 82:983–987.
Young SS, Tesarowski D. Respiratory mechanics of horses measured by conventional and forced oscillation techniques. J Appl Physiol 1994; 76:2467–2472.
Leclere M, Desnoyers M, Beauchamp G, et al. Comparison of four staining methods for detection of mast cells in equine bronchoalveolar lavage fluid. J Vet Intern Med 2006; 20:377–381.
Fowler ME. General biology and evolution. In: Medicine and surgery of South American camelids. 2nd ed. Ames, Iowa: Iowa State University Press, 1998;1–11.
Fowler ME. Hemic and lymphatic systems. In: Medicine and surgery of South American camelids. 2nd ed. Ames, Iowa: Iowa State University Press, 1998;364–376.
Bedenice D, Bar-Yishay E, Ingenito EP, et al. Evaluation of head-out constant volume body plethysmography for measurement of specific airway resistance in conscious, sedated sheep. Am J Vet Res 2004; 65:1259–1264.
Verschakelen JA, Demedts MG. Normal thoracoabdominal motions. Influence of sex, age, posture, and breath size. Am J Respir Crit Care Med 1995; 151:399–405.
Koterba AM, Kosch PC, Beech J, et al. Breathing strategy of the adult horse (Equus caballus) at rest. J Appl Physiol 1988; 64:337–346.
Hoffman AM, Oura TJ, Riedelberger KJ, et al. Plethysmographic comparison of breathing pattern in heaves (recurrent airway obstruction) versus experimental bronchoconstriction or hyperpnea in horses. J Vet Intern Med 2007; 21:184–192.
Gallivan GJ, McDonell WN, Forrest JB. Comparative ventilation and gas exchange in the horse and the cow. Res Vet Sci 1989; 46:331–336.
Mazan MR, Deveney EF, DeWitt S, et al. Energetic cost of breathing, body composition, and pulmonary function in horses with recurrent airway obstruction. J Appl Physiol 2004; 97:91–97.
Rabello E, Batista VF, Lago PM, et al. Bronchoalveolar lavage analysis in victims of severe facial burns. J Bras Pneumol 2009; 35:343–350.