Immunopathological Changes of Streptococcus pneumoniae Causing Respiratory Infection in Lambs
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Abstract
Streptococcus pneumoniae are common bacterial pathogens that can cause a range of diseases in humans and animals. This study attempts to clarify the course and consequences of pneumonia caused by this bacterial infection. A total of 6 male un-weaned lambs aged between 1 to 2 months and weighing 5 to 7 kg were subjected to S. pneumoniae strain ATCC 6303 serotype 3 at 2×106 CFU/mL by inhalation to induce pneumonia. Pneumonic clinical signs were monitored daily throughout the study period. The blood samples were collected from all animal groups at day zero before pneumoniae induction and 3, 6, and 14 days post infection for total and differential white blood cell count (WBCs) and tumor necrosis factor-alpha (TNF-α) assessments. Additionally, on days 6 and 14 post-exposure, trachea and lung tissue samples were harvested for macroscopic and microscopic pathological changes evaluation. The results showed that there was a significant increase (P<0.001) in total WBC counts from day 3 post-exposure and maintaining elevated levels on days 6 and 14 compared to day zero. Differential WBC counts showed an early, significant rise in neutrophils, with sustained elevation in lymphocytes and monocytes. TNF-α levels significantly elevated on day 3 and gradually declined by day 14 post-exposure (P<0.001). On day 6 post-exposure, the gross pathological changes in the lung showed pulmonary edema, and emphysema, with mild to moderate lung congestion and emphysematous changes observed on day 14 post-exposure. Histopathologically, severe erosion and necrosis in the trachea and bronchus epithelium, along with inflammation in adjacent mucosa and submucosa, accompanied by focal inflammatory infiltration and emphysema in the lung by day 6 post-exposure, were observed. By day 14, these changes progressed to marked epithelial vacuolation and necrosis in the trachea, with lung sections revealing perivascular cuffing, peri bronchiolitis, mild bronchiectasis, atelectasis, and alveolar collapse. This study is attempt for a better understanding of S. pneumoniae infection in lamb and contributing to the development of preventive and management strategies in Iraq.
Received: 15 March 2024
Revised: 12 April 2024
Accepted: 30 June 2024
Published: 28 December 2024
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Brogden KA, Lehmkuhl HD, Cutlip RC. Pasteurella haemolytica complicated respiratory infections in sheep and goats. Vet Res. 1998;29(3-4):233-254.
Kumar A, Verma AK, Rahal A. Mycoplasma bovis, a multi disease-producing pathogen: An overview. Asian J Anim Vet Adv. 2011;6(6):537-546 10.3923/ajava.2011.537.546
Kumar A, Verma AK, Gangwar NK, Rahal A. Isolation, characterization, and antibiogram of Mycoplasma bovis in sheep pneumonia. Asian J Anim Vet Adv. 2012;7(2):149-157. 10.3923/ajava.2012.149.157
Kumar A, Verma AK, Sharma AK, Rahal A. Isolation and antibiotic sensitivity of Streptococcus pneumoniae infections with involvement of multiple organs in lambs. Pak. J Biol. Sci. 2013;16(24):2021–2025. 10.3923/pjbs.2013.2021.2025
Jones GE, Field AC, Gilmour JS, Rae AG, Nettleton PF, McLauchlan M. Effects of experimental chronic pneumonia on bodyweight, feed intake and carcase composition of lambs. Vet Rec. 1982;110(8):168–173. 10.1136/vr.110.8.168
Goodwin KA, Jackson R, Brown C, Davies PR, Morris RS, Perkins NR. Pneumonic lesions in lambs in New Zealand: patterns of prevalence and effects on production. N Z Vet J. 2004;52(4):175–179. 10.1080/00480169.2004.36425
Zivich PN, Grabenstein JD, Becker-Dreps SI, Weber DJ. Streptococcus pneumoniae outbreaks and implications for transmission and control: a systematic review. Pneumonia (Nathan). 2018;(10):11. 10.1186/s41479-018-0055-4
Proctor M, Manning PJ. Production of immunoglobulin A protease by Streptococcus pneumoniae from animals. Infect Immun. 1990;58(9):2733–2737. 10.1128/iai.58.9.2733-2737.1990
Alnajjar S, Sitthicharoenchai P, Gallup J, Ackermann M, Verhoeven D. Streptococcus pneumoniae serotype 22F infection in respiratory syncytial virus infected neonatal lambs enhances morbidity. PLoS One. 2021;16(3):0235026. 10.1371/journal.pone.0235026
Borsa N, Di Pasquale M, Restrepo MI. Animal models of Pneumococcal pneumonia. Int J Mol Sci. 2019;20(17):4220. 10.3390/ijms20174220
Sharma L, Feng J, Dela Cruz CS. Mechanisms of epithelial immunity evasion by respiratory bacterial pathogens. Front Immunol. 2020;11:511421. 10.3389/fimmu.2020.00091
Mahdi ZS, Hashim MS, Karim AJ, Mahmood TA. Pathological study of the main pulmonary infections isolated from sheep in Holy Kerbala province. J. Genet. Environ. Resour. Conserv. 2022,10(2):163-170.
Korkmaz FT, Traber KE. Innate immune responses in pneumonia. Pneumonia. 2023;15:4. 10.1186/s41479-023-00106-8
Lee M, Lee SY, Bae YS. Emerging roles of neutrophils in immune homeostasis. BMB Rep. 2022;55(10):473. 10.5483/BMBRep.2022.55.10.115
He SWJ, van de Garde MDB, Pieren DKJ, Poelen MCM, Voß F, Abdullah MR, et al. Diminished pneumococcal-specific CD4+ T-cell response is associated with increased regulatory T cells at older age. Front Aging. 2021;2:746295. 10.3389/fragi.2021.746295
Anandachar MS, Roy S, Sinha S, Boadi A, Katkar GD, Ghosh P. Diverse gut pathogens exploit the host engulfment pathway via a conserved mechanism. J of Bio Chem .2023;299(12):105390. 10.1016/j.jbc.2023.105390
Silva LB, dos Santos Neto AP, Maia SMAS, dos Santos Guimarães C, Quidute IL, Carvalho A de AT, et al. The role of TNF-α as a proinflammatory cytokine in pathological processes.The Open Dent J. 2019;13(1):332-338. 10.2174/1874210601913010332
D'Amato RF, Swenson JM, McKinley GA, Hochstein L, Wallman AA, Cleri DJ, et al. Quantitative antimicrobial susceptibility test for Streptococcus pneumoniae using inoculum supplemented with whole defibrinated sheep blood. J Clin Microbiol. 1987;25(9):1753-1756. 10.1128/jcm.25.9.1753-1756.1987
McDevitt E, Khan F, Scasny A, Thompson CD, Eichenbaum Z, McDaniel LS, Vidal JE. Hydrogen Peroxide production by Streptococcus pneumoniae results in alpha-hemolysis by oxidation of oxy-hemoglobin to met-hemoglobin. Msphere. 2020;5(6):10-1128. 10.1128/mSphere.01117-20
Wu SC, Trask LM, Phee RE. Comparison of media and culture techniques for detection of Streptococcus pneumoniae in respiratory secretions. J Clin Microbiol. 1980;12(6):772-775. 10.1128/jcm.12.6.772-775.1980
Quinn PJ, Markey BK, Leonard FC, Hartigan P, Fanning S, Fitzpatrick E. Veterinary microbiology and microbial disease.2nd edition. John Wiley & Sons; 2011.928 p.
Alnajjar SSA, Sitthicharoenchai P, Gallup J, Ackermann M, Verhoeven D. Streptococcus pneumoniae infection in respiratory syncytial virus infected neonatal lambs. FASEB J. 2018;32:594–594. 10.1096/fasebj.2018.32.1
Bancroft JD, Gamble M. Theory and Practice of Histological Techniques. 6th ed. Philadelphia: Churchill Livingstone Elsevier; 2008. 744p.
Luna LG. Manual of histologic staining methods of the Armed Forces Institute of Pathology. 3rd ed. New York: McGraw-Hill; 1968. (pp. xii-258).
Ismail Ibrahim Z. Pathological Findings of respiratory diseases in one hump camel (Camelus dromedaries) in Wasit governate. Al-Qadisiyah J Vet Med Sci. 2022;21(2):56–61.
Viitanen SJ, Lappalainen A, Rajamäki MM. Co‐infections with respiratory viruses in dogs with bacterial pneumonia. J Vet Intern Med. 2015;29(2):544-551. 10.1111/jvim.12553
Beck JM, Young VB, Huffnagle GB. The microbiome of the lung. Trans Res. 2012;160(4):258–266. 10.1016/j.trsl.2012.02.005
Zhang T, Zhang M, Yang L, Gao L and Sun W. Potential targeted therapy based on deep insight into the relationship between the pulmonary microbiota and immune regulation in lung fibrosis. Front. Immunol. 2023;14:1032355. 10.3389/fimmu.2023.1032355
Jakic D, Ranisavljevic M. Streptococcosis in swine, its diagnosis, control and prevention. Veterinarski glasnik (Yugoslavia). 1989;43(7).
Houldsworth S, Andrew PW, Mitchell TJ. Pneumolysin stimulates production of tumor necrosis factor alpha and interleukin-1 beta by human mononuclear phagocytes. Infect Immun. 1994;62(4):1501–1513. 10.1128/iai.62.4.1501-1503.1994
Glimåker M, Kragsbjerg P, Forsgren M, Olcen P. Tumor necrosis factor-α (TNFα) in cerebrospinal fluid from patients with meningitis of different etiologies: high levels of TNFα indicate bacterial meningitis. J Inf Dis. 1993;167(4):882–889. 10.1093/infdis/167.4.882
Nohynek H, Teppo AM, Laine E, Leinonen M, Eskola J. Serum tumor necrosis factor-α concentrations in children hospitalized for acute lower respiratory tract infection. J Inf Dis. 1991;163(5):1029-1032. 10.1093/infdis/163.5.1029
Saukkonen K, Sande S, Cioffe C, Wolpe S, Sherry B, Cerami A, et al. The role of cytokines in the generation of inflammation and tissue damage in experimental gram-positive meningitis. J Exp Med. 1990;171(2):439-448. 10.1084/jem.171.2.439
Takashima K, Tateda K, Matsumoto T, Ito T, Iizawa Y, Nakao M, et al. Establishment of a model of penicillin-resistant Streptococcus pneumoniae pneumonia in healthy CBA/J mice. J Med Microbiol. 1996;45(5):319322. 10.1099/00222615-45-5-319
Meutia N, Lubis LD, Megawati ER. Moderate dose of lipopolysaccharide induces tumor necrosis factor-alpha and interleukin-6 production by human monocyte-derived macrophages. OAMJMS. 2021;9(A):468-72. 10.3889/OAMJMS.2021.6453
Pageaut H, Lacouture S, Lehoux M, Marois-Créhan C, Segura M, Gottschalk M. Interactions of Mycoplasma hyopneumoniae and/or Mycoplasma hyorhinis with Streptococcus suis serotype 2 using in vitro co-infection models with swine cells. Pathogens. 2023;12(7):866. 10.3390/pathogens12070866
Obradovic MR, Segura M, Segalés J, Gottschalk M. Review of the speculative role of co-infections in Streptococcus suis-associated diseases in pigs. Vet Res. 2021;52(1):49. 10.1186/s13567-021-00918-w