Potential Pathogens Recovered from the Upper Respiratory Tract of Psittacine Birds

Sandra O. Jesus and J.H. Duarte Correia

Department of Morphology and Clinics, Faculty of Veterinary Medicine, Rua Gomes Freire, 1199 Lisboa codex, Portugal

Abstract. This study was done to clarify the hypothesis that the resident flora of the upper respiratory tract of psittacine birds can behave as opportunistic pathogens. Swabs were taken from the choanal slit of nineteen healthy psittacines and four birds with upper respiratory disease (three with sinusitis and one with unspecified upper respiratory pathology). The isolation and identification of bacteria and fungi were accomplished by standard microbiological methods and the use of commercial identification systems. A total of 44 isolates were recovered from the choanae of the 23 psittacines sampled. Twenty six percent of the isolates recovered from the choanal slits of healthy birds were gram-positive bacteria, 62% gram-negative bacteria, and 12% were fungi. From sick birds, 60% of the isolates were bacterial and 40% were fungal. Fifty eight percent of the swabs from healthy birds yielded more than one isolate, whereas 75% of the swabs from sick birds had more than one isolate. Among other organisms, Streptococcus sp., Staphylococcus sp., Alcaligenes sp., Klebsiella pneumoniae pneumoniae, K. oxytoca, Pasteurella sp., Pseudomonas alcaligenes, P. stutzeri, and Xanthomonas maltophila, all considered to be potential pathogens of the respiratory tract, were isolated from the choanal slits of healthy birds. These findings suggest that the upper respiratory tract of healthy animals can harbour microorganisms which can behave as opportunistic pathogens. From the choanal slits of sick birds, the following potentially pathogenic organisms were isolated: Streptococcus sp., Staphylococcus sp., Escherichia coli, Klebsiella pneumoniae pneumoniae, K. oxytoca, Proteus mirabilis, Candida albicans, and Aspergillus flavus. All of these organisms have been reported to be associated with upper respiratory disease under certain circumstances.

Key Words: Avian, Psittacine birds, Upper respiratory tract, Normal flora, Pathogenic bacteria

Introduction

Pathogenic bacteria and fungi have been isolated both from birds with upper respiratory tract disease and from healthy birds, suggesting that saprophytic flora can behave as opportunistic pathogens. Fudge, Reavill and Rosskopf consider opportunistic bacterial infections to be one of the most frequent causes of veterinary clinic visits for pet birds. ⁴ To try to clarify the hypothesis that saprophytic flora can behave as opportunistic pathogens, swabs were taken from the choanal slit of nineteen healthy psittacines and four birds with upper respiratory disease (three with sinusitis and one with unspecified upper respiratory pathology). The isolation and identification of bacteria and fungi in this project was accomplished by simple microbiological methods and commercial kits. These techniques and kits are available to and can easily be used by the average veterinary clinician with access to an in-house laboratory.

Materials and Methods

Sample collection: Swabs were taken from the choanal slit of nineteen healthy psittacine birds, as well as from four birds with upper respiratory tract disease. The sample population of birds is presented in Table 1.

TABLE 1. Various species of psittacine birds sampled by microbiological culture.

Data are expressed as number of choanal slits sampled

Microorganism identification: Bacterial identification, ideally to the species level, was pursued by means of biochemical reactions using API identification systems. Yeasts were identified, when possible, to the genus level. Otherwise, they were reported only as yeasts. Moulds also were identified to the genus level when possible. Alternatively, they were identified only as moulds based upon their colony and cellular morphology.

Results

A total of 44 isolates were recovered from the choanae of the 23 psittacines sampled. Thirty six (82%) of the isolates were bacterial and eight (18%) were fungal in origin. Of the 34 isolates from healthy birds, 30 (88%) were bacterial and four (12%) were fungal. As far as the isolates from birds with upper respiratory disease are concerned, 10 isolates were recovered; six (60%) being bacterial and four (40%) being fungal.

A comprehensive list of the isolates recovered from the choanal slits of healthy psittacines is given in Table 2.

TABLE 2. Choanal flora identified from healthy psittacine birds.

Data are expressed as number of choanal slits (% of the choanal slits).

The isolates recovered from the choanal slits of psittacines with upper respiratory disease are listed in Table 3.

TABLE 3. Isolates from psittacine birds with upper respiratory disease.

Data are expressed as number of choanal slits (% of choanal slits).

Discussion

Twenty six percent of the isolates recovered from the choanal slits of healthy psittacines were gram-positive bacteria, 62% were gram-negative bacteria, and 12% were fungi. These findings reflect the bacterial types and fungi that may be part of the resident flora of the upper respiratory tract of these birds. These results differ from those of Tully;⁸ Tully and Harrison;⁹ Harris;⁶ Bounous, Schaeffer, and Roy;¹ and Drewes and Flammer² which state that the normal flora of the upper respiratory tract of healthy psittacines contains predominantly gram-positive organisms. Gerlach⁵ and Spenser⁷ consider gram-negative growth from the choanae to be abnormal and potentially pathogenic. On the other hand, one must be cautious when interpreting these results. According to Harris,⁶ although gram-negative bacteria isolated from the choanae can be potentially pathogenic, a bird should not be considered ill simply because these organisms are present in the absence of pathology. Tully adds that bacteria identified by culture or Gram’s stain from samples taken from a bird without clinical abnormalities have questionable significance; if clinical signs are present, then isolation of potentially pathogenic organisms may be significant. ⁸ In fact, the high proportion of gram-negative bacteria recovered in this survey may be due to contamination of the swab with oral flora,⁷ caudal choanal flora,² or with the bird’s last meal. ⁶

Three unidentified yeasts and one isolate of Cryptococcus neoformans were recovered from healthy birds. These findings are not surprising for Candida sp. which are normal inhabitants of the oropharyngeal cavity and may spread from the choana to the infraorbital sinus where they can act as opportunistic pathogens and cause disease. ⁸ As for Cryptococcus neoformans, birds are believed to be a major source of the organism and the respiratory system is considered its portal of entry. ³

In this survey, many potential pathogens were recovered from the choanal slits of healthy psittacines. These potential pathogens included: Streptococcus sp. (16%), Staphylococcus sp. (11%), Alcaligenes sp. (5%), Klebsiella pneumoniae pneumoniae (11%), Klebsiella oxytoca (26%), Pasteurella sp. (11%), Pseudomonas alcaligenes (5%), Pseudomonas stutzeri (21%), and Xanthomonas maltophila (5%). The findings of our study suggest that healthy psittacine birds may harbour potentially pathogenic bacteria in their upper respiratory tract. In times of stress, these organisms may cause respiratory infection. This hypothesis is supported by Tully,⁸ who states that companion birds commonly are exposed to infectious bacterial and fungal organisms through the environment, handfeeding techniques, foods, and contact with other birds. Furthermore, he adds that immunocompromised birds (e.g., neonatal or handfed birds, young birds, or birds with nutritional deficiencies or concurrent infections) may become susceptible to these ubiquitous infectious organisms.

One must remember that the isolation of some respiratory pathogens (e.g., Mycoplasma, Haemophilus, and Chlamydia sp. ) was not within the scope of this study. Therefore, one cannot draw any conclusions whether or not these specific organisms are part of the normal flora of the upper respiratory tract of psittacine birds.

All bacteria (Streptococcus sp., Staphylococcus xylosus, Escherichia coli, Klebsiella pneumoniae pneumoniae, Klebsiella oxytoca, and Proteus mirabilis) isolated from birds with upper respiratory tract disease are considered to be pathogenic and associated with upper respiratory system infections. ^8,9 Two recognised fungal pathogens, Candida albicans and Aspergillus flavus, were recovered from psittacines with sinusitis.

Comparing the isolates recovered from healthy birds with those from birds with upper respiratory tract infections, it is interesting to note that Klebsiella pneumoniae pneumoniae, Klebsiella oxytoca, a - haemolytic Streptococcus sp., and Staphylococcus sp. were isolated from both groups of birds. According to Tully,⁹ the genera Staphylococcus and Streptococcus are most likely part of the normal flora. However, Klebsiella pneumoniae and K. oxytoca frequently have been recovered from birds in which they can function as primary pathogens or can be involved as opportunists in immunosuppressed or stressed patients. ⁵ Gerlach also states that local infections involving the sinuses also may occur, particularly in Psittaciformes. ⁵ In summary, these statements also support the hypothesis that saprophytic flora can behave as opportunistic pathogens in stressful situations. Although attempts to isolate some specific respiratory pathogens were excluded from this study, our findings still suggest that the resident flora of the upper respiratory tract of healthy psittacine birds can behave as opportunistic pathogens.

References

1. Bounous DI, Schaeffer DO, Roy A: Coagulase-negative Staphylococcus sp. septicaemia in a lovebird. J Am Vet Med Assoc 195:1120-1122, 1989.

2. Drewes LA, Flammer K: Clinical microbiology. In: Clinical Avian Medicine and Surgery. Harrison GL, Harrison LR (eds). W.B. Saunders Co., Philadelphia, 1986, pp. 157-171.

3. Fenwick B, Takeshita K, Wong A: A moluccan cockatoo with disseminated cryptococcosis. J Am Vet Med Assoc 187:1218-1219, 1985.

4. Fudge AM, Reavill DR, Rosskopf WJ: Clinical aspects of avian Pseudomonas infections: a retrospective study. In: Proc Assoc Avian Vet Ann Conf, New Orleans, LA, 1992, pp. 141-150.

5. Gerlach H: Bacteria. In: Avian Medicine: Principles and Application. Ritchie BW, Harrison GJ, Harrison LR (eds). Wingers Publishing Inc., Lake Worth, Florida, 1994, pp. 949-983.

6. Harris DJ: Laboratory testing in pet avian medicine. Vet Clin N Am / Small Animal Pract 21:1147-1156, 1991.

7. Spenser EL: Common infectious diseases of psittacine birds seen in practice. Vet Clin N Am / Small Animal Pract 21:1213-1230, 1991.

8. Tully TN: Avian respiratory diseases: clinical overview. J Avian Med Surg 9:162-174, 1995.

9. Tully TN, Harrison GJ: Pneumology. In: Avian Medicine: Principles and Application. Ritchie BW, Harrison GJ, Harrison LR (eds). Wingers Publishing Inc., Lake Worth, Florida, 1994, pp. 574-575.

This Page Last Updated May 15, 1998

^  Top of page