Skip to main content
Download PDF

Respiratory virus infections of the lower respiratory tract elevate bronchoalveolar lavage eosinophil fraction: a clinical retrospective study and case review

BMC Pulmonary Medicine volume 23, Article number: 111 (2023) Cite this article

Abstract

Background

Eosinophilic airway inflammation caused by respiratory virus infection has been demonstrated in basic research; however, clinical investigations are lacking. To clarify the extent to which respiratory virus infection induces airway eosinophilic inflammation, we reviewed the results of bronchoalveolar lavage (BAL) and respiratory virus testing performed at our hospital.

Methods

Among the BAL procedures performed at the University of the Ryukyu Hospital from August 2012 to September 2016, we collected cases of acute respiratory disease in which multiplex polymerase chain reaction (PCR) was used to search for respiratory viruses. The effect of respiratory virus detection on BAL eosinophil fraction was analyzed using statistical analysis. A case study was conducted on respiratory virus detection, which showed an elevated BAL eosinophil fraction.

Results

A total of 95 cases were included in this study, of which 17 were PCR-positive. The most common respiratory virus detected was parainfluenza virus (eight cases). The PCR-positive group showed a higher BAL eosinophil fraction than the PCR-negative group (p = 0.030), and more cases had a BAL eosinophil fraction > 3% (p = 0.017). Multivariate analysis revealed that being PCR-positive was significantly associated with BAL eosinophil fraction > 1% and > 3%. There were nine PCR-positive cases with a BAL eosinophil fraction > 1%, of which two cases with parainfluenza virus infection had a marked elevation of BAL eosinophil fraction and were diagnosed with eosinophilic pneumonia.

Conclusions

Cases of viral infection of the lower respiratory tract showed an elevated BAL eosinophil fraction. The increase in eosinophil fraction due to respiratory virus infection was generally mild, whereas some cases showed marked elevation and were diagnosed with eosinophilic pneumonia. Respiratory virus infection is not a rare cause of elevated BAL eosinophil fraction and should be listed as a differential disease in the practice of eosinophilic pneumonia.

Peer Review reports

Background

Respiratory viruses are often implicated in the exacerbation of respiratory diseases, including asthma exacerbations, which is a well-known fact [1]. This is thought to be due to the eosinophilic inflammation in the lower respiratory tract caused by respiratory virus infection. Basic medical studies have shown that respiratory viruses induce eosinophilic inflammation in the airways [2]. However, clinical studies are scarce and insufficient to determine the extent of eosinophilic inflammation of the lower respiratory tract caused by viral respiratory infections. To confirm this, clinical specimens of the lower respiratory tract of infected patients are required.

In our institution, when bronchoalveolar lavage (BAL) fluid is collected in clinical practice, multiplex polymerase chain reaction (PCR) testing for respiratory viruses is performed as a routine test to differentiate between infectious. Therefore, PCR results and BAL cell fraction can be collected from past data. We retrospectively summarized this data in patients with acute lung disease and investigate whether the detection of respiratory viruses in BAL fluid is associated with increased BAL eosinophil fraction. Additionally, we reviewed cases of respiratory virus infection and elevated BAL eosinophil fraction.

Methods

We reviewed data from BAL testing and respiratory virus search multiplex PCR testing of BAL fluid at the University of the Ryukyus Hospital from August 2012 to September 2016. To collect cases of acute respiratory virus infections, cases without respiratory symptoms or new lung lesions within two weeks prior to BAL testing were excluded. Multiplex PCR was performed using commercially available kits (Seeplex RV15 OneStep ACE Detection, Seegene, Korea), which can detect multiple community-acquired respiratory viruses, such as adenovirus; coronavirus 229E/NL63; OC43; parainfluenza virus 1, 2, 3, 4, rhinovirus A/B/C; respiratory syncytial viruses A and B; metapneumovirus; enterovirus; influenza viruses A and B; and bocavirus 1/2/3/4. We defined elevated BAL eosinophil fraction as a value greater than 1% [3].

Factors that increased BAL eosinophil fraction were statistically analyzed. Statistical analysis was performed using IBM SPSS Statistics for Windows, version 22.0 (Armonk, NY, USA). Differences among patients’ backgrounds and laboratory test results were compared between the PCR-positive group and the PCR-negative group using the chi-square and Mann–Whitney U tests. Because the PCR-positive group included cases with marked elevation of BAL eosinophil fraction, cutoff values for eosinophil fraction (> 1%, > 3%, and > 5%) were set and analyzed with binary variables as well. Stepwise logistic regression analysis (increasing variables method) was performed to explore factors involved in increased BAL eosinophil fraction. The independent variables were PCR-positive in BAL, user of systemic corticosteroid, user of inhaled corticosteroid, bronchial asthma, history of allergies or allergic reactions, and eosinophils in blood > 500/µL. Independent variables were selected based on the results of the univariate analysis and the clinical importance of airway eosinophilic inflammation.

This study was approved by the Clinical Research Ethics Committee of the University of the Ryukyus.

Results

Ninety-five cases were included in this study, of which 17 were PCR-positive (Fig. 1). The 17 PCR-positive cases were classified by virus detection: eight parainfluenza virus, three rhinovirus, two enterovirus, two influenza A virus, one respiratory syncytial virus, and one human metapneumovirus. Table 1 shows the patient background. The PCR-positive group tended to be younger and had a higher prevalence of bronchial asthma. The administration of systemic steroids did not differ between the two groups. Table 2 summarizes the final diagnoses of the respiratory diseases in the included cases. They can be broadly divided into respiratory infection and interstitial lung disease; among the PCR-positive cases. Viral pneumonia was diagnosed in two cases, while respiratory virus infections were considered a comorbidity in the other cases. Except for patients with influenza virus infection, none of the patients were treated with antiviral therapy.

Fig. 1
figure 1

Flow diagram of this study

A total of 130 patients with respiratory disease underwent bronchoalveolar lavage and multiplex polymerase chain reaction. Cases without respiratory symptoms or new lung lesions within two weeks prior to bronchoalveolar lavage testing were excluded, and 95 patients were included

Full size image
Table 1 Demographic data of study subjects
Full size table
Table 2 Final diagnoses of pulmonary diseases
Full size table

Table 3 shows the results of BAL cell fraction and peripheral blood eosinophils categorized into the PCR-positive and the PCR-negative groups. BAL eosinophil fraction was higher in the PCR-positive group than in the PCR-negative group; however, only when mildly elevated (> 1% and > 3%). There was no difference in eosinophils in the peripheral blood. The results of the multivariate analysis of the factors involved in increased BAL eosinophil fraction are shown in Table 4. The results showed that PCR positivity of BAL and elevated peripheral blood eosinophils were associated with an eosinophil fraction > 1% and > 3% of BAL. On the other hand, for BAL eosinophil fraction > 5%, only elevated peripheral blood eosinophils were shown to be associated factors. Systemic steroid use decreased the likelihood of BAL eosinophil fraction > 1%.

Table 3 Comparison of eosinophils in bronchoalveolar lavage fluid and blood between the PCR-positive group and the PCR-negative group
Full size table

Differences among laboratory test results were compared between polymerase chain reaction-positive and -negative cases using the chi-square and Mann–Whitney U tests.

Table 4 The factor for elevation of eosinophil fraction in bronchoalveolar lavage
Full size table

The stepwise logistic regression analysis (with variable increase method) was conducted. The independent variables were PCR-positive in BAL, user of systemic corticosteroid, user of inhaled corticosteroid, bronchial asthma, history of allergies or allergic reactions, and eosinophils in blood > 500/µL.

Of these, nine cases with elevated BAL eosinophil fraction are shown (Table 5). Parainfluenza virus infection was the most common, and two patients diagnosed with eosinophilic pneumonia had parainfluenza infections. Also, two cases of viral pneumonia were included: respiratory syncytial virus and rhinovirus.

Table 5 PCR-positive cases with elevated BAL eosinophil fraction
Full size table

Elevated BAL eosinophil fraction was defined as > 1%. None of the patients were treated with antiviral therapy.

Discussion

Several studies have been conducted on eosinophilic airway inflammation caused by respiratory virus infections. In basic research, respiratory syncytial virus infection is often reported to be involved in eosinophilic airway inflammation [4,5,6]. Clinical studies have demonstrated eosinophilic inflammation due to respiratory virus infections using upper respiratory tract specimens, such as nasal secretions [7, 8]; however, clinical studies using lower respiratory tract specimens, such as BAL, are rare. There have been small studies on rhinovirus and respiratory syncytial virus, showing a slight elevation of BAL eosinophil fraction due to infection [9, 10]. Recent studies have shown that BAL eosinophil fraction is elevated in coronavirus disease 2019 (COVID-19) [11]. Table 6 shows these and other studies showing bronchoalveolar lavage cell analysis in respiratory virus infection subjects [9,10,11,12,13,14,15,16,17,18,19]. Although some studies have shown that respiratory virus infection increases BAL eosinophil fraction, they have been conducted in patients with allergic diseases such as bronchial asthma, and the increase in the eosinophil fraction was slight, as in the present study. On the other hand, two studies in the clinical setting, like the present study, were conducted in patients with underlying pulmonary diseases; however, they did not find an increased BAL eosinophil fraction due to viral infection. Unlike the present study, none of these studies had as their main objective the analysis of BAL eosinophil fraction.

Table 6 Articles showing bronchoalveolar lavage cell analysis in subjects infected with respiratory viruses
Full size table

Eosinophilic airway inflammation caused by respiratory virus infections is considered a protective response to respiratory viruses, and basic medical and clinical studies have shown that eosinophilic inflammation is protective against respiratory viral infections [20,21,22,23]. Eosinophils produce and contain molecules with antiviral activity, such as RNase and active nitrogen species [22]. In addition, eosinophils can capture and inactivate viruses [23]. Therefore, increased BAL eosinophil fraction due to respiratory virus infection is a rational response to protect against respiratory viruses.

In the present study, two patients with positive results for parainfluenza virus had a marked elevation of BAL eosinophil fraction and were diagnosed with eosinophilic pneumonia (Case 2 and 3). They had a history of bronchial asthma and had uncontrolled asthma symptoms prior to the examination. Chest imaging revealed a non-regional subpleural infiltrate in the right lower lobe in Case 2, and a typical finding of chronic eosinophilic pneumonia, a photographic negative of pulmonary edema, in Case 3. After bronchoscopy, the patient was diagnosed with eosinophilic pneumonia and started on systemic steroid therapy. Clinical and imaging findings improved quickly, and tapering was completed in about 2 months. Their clinical course was consistent with the usual course of chronic eosinophilic pneumonia. In these two patients, eosinophilic pneumonia was probably caused by parainfluenza infection since there was no other obvious cause. Although there have been reports of cases of eosinophilic pneumonia with a marked elevation of BAL eosinophil fraction in influenza virus infection and COVID-19 [24,25,26], there are no reports of eosinophilic pneumonia caused by parainfluenza virus. There has been a case report of parainfluenza virus pneumonia; however, the increase of BAL eosinophils was mild and not eosinophilic pneumonia [27]. It is likely that there are many more cases of eosinophilic pneumonia caused by respiratory viral infections in clinical practice. Highly sensitive multiplex testing will further clarify the relationship between respiratory viral infections and allergic respiratory diseases.

There were some limitations to this study. First, this was a retrospective single-center study. PCR testing was performed as a routine test on BAL specimens during the study period. However, it was not mandatory and may not have been performed on cases deemed unnecessary by the attending physician. The number of such cases is unknown. It is possible that there was a bias in the backgrounds of the cases included in this study or in the respiratory viruses prevalent in our region. Second, the number of positive cases was too small to properly perform a multivariate analysis of all possible confounders. The statistical analysis on BAL eosinophil fraction should have been performed with the eosinophil fraction measured as a continuous variable; however, we had to replace it with a binary variable to reduce the effect of outliers due to the small population. Third, the degree of eosinophilic airway inflammation is different for different respiratory viruses. A previous report showed that respiratory syncytial virus infection caused higher eosinophil counts than metapneumovirus infection in peripheral blood [28]. When comparing rhinovirus and influenza virus, infection of the former was higher in peripheral blood [29]. Additionally, some respiratory viruses, adenovirus, and bocavirus, probably do not cause eosinophilic inflammation [30, 31]. Further studies on each respiratory virus species are necessary. Finally, patient bias and factors other than respiratory virus infection may influence an increase in BAL eosinophil fraction. A history of bronchial asthma tended to be more common in the PCR-positive group. Even though multivariate analysis showed no association with elevated BAL eosinophil fraction, it may have influenced the results. Alternatively, this background bias may have been inevitable, as respiratory virus infections are reported to be more likely to occur in patients with bronchial asthma [32]. There were more cases of drug-induced lung injury and pneumocystis pneumonia not related to human immunodeficiency virus infection in the PCR-negative group. Since both diseases elevate BAL lymphocyte fraction, it is likely that BAL fraction of the PCR-negative group tended to be higher [3, 33]. As a result, BAL eosinophil fraction of the PCR-negative group may have been relatively lower.

Conclusion

In this study, we found that BAL eosinophil fraction was increased in patients infected with respiratory viruses in the lower respiratory tract. The degree of eosinophilic inflammation caused by respiratory virus infections is mild; however, it can occasionally cause eosinophilic pneumonia. Clinicians should also consider respiratory virus infection as a differential cause of elevated BAL eosinophils.

Data Availability

The datasets generated and/or analysed during the current study are not publicly available due privacy and ethical restrictions but are available from the corresponding author on reasonable request.

Abbreviations

BAL:

Bronchoalveolar lavage

PCR:

polymerase chain reaction

References

  1. Hewitt R, Farne H, Ritchie A, Luke E, Johnston SL, Mallia P. The role of viral infections in exacerbations of chronic obstructive pulmonary disease and asthma. Ther Adv Respir Dis. 2016;10(2):158–74.

    Article  PubMed  Google Scholar 

  2. Cottin V. Eosinophilic Lung Diseases. Clin Chest Med. 2016;37(3):535–56.

    Article  PubMed  Google Scholar 

  3. Meyer KC, Raghu G, Baughman RP, Brown KK, Costabel U, du Bois RM, Drent M, Haslam PL, Kim DS, Nagai S, et al. An official american thoracic society clinical practice guideline: the clinical utility of bronchoalveolar lavage cellular analysis in interstitial lung disease. Am J Respir Crit Care Med. 2012;185(9):1004–14.

    Article  PubMed  Google Scholar 

  4. Wu YH, Lai AC, Chi PY, Thio CL, Chen WY, Tsai CH, Lee YL, Lukacs NW, Chang YJ. Pulmonary IL-33 orchestrates innate immune cells to mediate RSV-evoked airway hyperreactivity and eosinophilia. Allergy 2019.

  5. Schwarze J, Cieslewicz G, Hamelmann E, Joetham A, Shultz LD, Lamers MC, Gelfand EW. IL-5 and eosinophils are essential for the development of airway hyperresponsiveness following acute respiratory syncytial virus infection. J Immunol. 1999;162(5):2997–3004.

    Article  CAS  PubMed  Google Scholar 

  6. Olszewska-Pazdrak B, Casola A, Saito T, Alam R, Crowe SE, Mei F, Ogra PL, Garofalo RP. Cell-specific expression of RANTES, MCP-1, and MIP-1alpha by lower airway epithelial cells and eosinophils infected with respiratory syncytial virus. J Virol. 1998;72(6):4756–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Okamoto N, Ikeda M, Okuda M, Sakamoto T, Takasugi M, Takahashi N, Araki T, Morishima T, Yasui K. Increased eosinophilic cationic protein in nasal fluid in hospitalized wheezy infants with RSV infection. Allergol Int. 2011;60(4):467–72.

    Article  CAS  PubMed  Google Scholar 

  8. Sigurs N, Bjarnason R, Sigurbergsson F. Eosinophil cationic protein in nasal secretion and in serum and myeloperoxidase in serum in respiratory syncytial virus bronchiolitis: relation to asthma and atopy. Acta Paediatr. 1994;83(11):1151–5.

    Article  CAS  PubMed  Google Scholar 

  9. Calhoun WJ, Dick EC, Schwartz LB, Busse WW. A common cold virus, rhinovirus 16, potentiates airway inflammation after segmental antigen bronchoprovocation in allergic subjects. J Clin Invest. 1994;94(6):2200–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Kim CK, Kim SW, Park CS, Kim BI, Kang H, Koh YY. Bronchoalveolar lavage cytokine profiles in acute asthma and acute bronchiolitis. J Allergy Clin Immunol. 2003;112(1):64–71.

    Article  CAS  PubMed  Google Scholar 

  11. Zaid Y, Doré É, Dubuc I, Archambault AS, Flamand O, Laviolette M, Flamand N, Boilard É, Flamand L. Chemokines and eicosanoids fuel the hyperinflammation within the lungs of patients with severe COVID-19. J Allergy Clin Immunol. 2021;148(2):368–380e363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kim CK, Kim SW, Kim YK, Kang H, Yu J, Yoo Y, Koh YY. Bronchoalveolar lavage eosinophil cationic protein and interleukin-8 levels in acute asthma and acute bronchiolitis. Clin Exp Allergy. 2005;35(5):591–7.

    Article  CAS  PubMed  Google Scholar 

  13. Kim CK, Chung CY, Choi SJ, Kim DK, Park Y, Koh YY. Bronchoalveolar lavage cellular composition in acute asthma and acute bronchiolitis. J Pediatr. 2000;137(4):517–22.

    Article  CAS  PubMed  Google Scholar 

  14. Cameron A, Dhariwal J, Upton N, Ranz Jimenez I, Paulsen M, Wong E, Trujillo-Torralbo MB, Del Rosario A, Jackson DJ, Edwards MR, et al. Type I conventional dendritic cells relate to disease severity in virus-induced asthma exacerbations. Clin Exp Allergy. 2022;52(4):550–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Message SD, Laza-Stanca V, Mallia P, Parker HL, Zhu J, Kebadze T, Contoli M, Sanderson G, Kon OM, Papi A, et al. Rhinovirus-induced lower respiratory illness is increased in asthma and related to virus load and Th1/2 cytokine and IL-10 production. Proc Natl Acad Sci U S A. 2008;105(36):13562–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Ishiguro T, Kobayashi Y, Uozumi R, Takata N, Takaku Y, Kagiyama N, Kanauchi T, Shimizu Y, Takayanagi N. Viral pneumonia requiring differentiation from Acute and progressive diffuse interstitial lung Diseases. Intern Med. 2019;58(24):3509–19.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Bugin S, Lunardi F, Bertuola F, Snijders D, Bottecchia L, Perissinotto E, Calabrese F, Barbato A. Pediatric chronic lower respiratory disorders: microbiological and immunological phenotype. Pediatr Pulmonol. 2013;48(8):780–8.

    Article  CAS  PubMed  Google Scholar 

  18. van der Sluijs KF, van de Pol MA, Kulik W, Dijkhuis A, Smids BS, van Eijk HW, Karlas JA, Molenkamp R, Wolthers KC, Johnston SL, et al. Systemic tryptophan and kynurenine catabolite levels relate to severity of rhinovirus-induced asthma exacerbation: a prospective study with a parallel-group design. Thorax. 2013;68(12):1122–30.

    Article  PubMed  Google Scholar 

  19. Majoor CJ, van de Pol MA, Kamphuisen PW, Meijers JC, Molenkamp R, Wolthers KC, van der Poll T, Nieuwland R, Johnston SL, Sterk PJ, et al. Evaluation of coagulation activation after rhinovirus infection in patients with asthma and healthy control subjects: an observational study. Respir Res. 2014;15(1):14.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Drake MG, Bivins-Smith ER, Proskocil BJ, Nie Z, Scott GD, Lee JJ, Lee NA, Fryer AD, Jacoby DB. Human and mouse Eosinophils have antiviral activity against Parainfluenza Virus. Am J Respir Cell Mol Biol. 2016;55(3):387–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Phipps S, Lam CE, Mahalingam S, Newhouse M, Ramirez R, Rosenberg HF, Foster PS, Matthaei KI. Eosinophils contribute to innate antiviral immunity and promote clearance of respiratory syncytial virus. Blood. 2007;110(5):1578–86.

    Article  CAS  PubMed  Google Scholar 

  22. Flores-Torres AS, Salinas-Carmona MC, Salinas E, Rosas-Taraco AG. Eosinophils and respiratory viruses. Viral Immunol. 2019;32(5):198–207.

    Article  CAS  PubMed  Google Scholar 

  23. Sabogal Piñeros YS, Bal SM, Dijkhuis A, Majoor CJ, Dierdorp BS, Dekker T, Hoefsmit EP, Bonta PI, Picavet D, van der Wel NN, et al. Eosinophils capture viruses, a capacity that is defective in asthma. Allergy. 2019;74(10):1898–909.

    Article  PubMed  Google Scholar 

  24. Jeon EJ, Kim KH, Min KH. Acute eosinophilic pneumonia associated with 2009 influenza A (H1N1). Thorax. 2010;65(3):268–70.

    Article  PubMed  Google Scholar 

  25. Larrañaga JM, Marcos PJ, Pombo F, Otero-González I. Acute eosinophilic pneumonia as a complication of influenza A (H1N1) pulmonary infection. Sarcoidosis Vasc Diffuse Lung Dis. 2016;33(1):95–7.

    PubMed  Google Scholar 

  26. Araújo M, Correia S, Lima AL, Costa M, Neves I. SARS-CoV-2 as a trigger of eosinophilic pneumonia. Pulmonology. 2022;28(1):62–4.

    Article  PubMed  Google Scholar 

  27. Ishiguro T, Kobayashi Y, Takano K, Ozawa R, Shimizu Y, Takayanagi N. Two cases of primary human parainfluenza virus 1 pneumonia in which Bronchoalveolar Lavage Fluid yielded human parainfluenza virus 1. Intern Med. 2020;59(1):101–5.

    Article  PubMed  Google Scholar 

  28. Kim CK, Choi J, Callaway Z, Kim HB, Chung JY, Koh YY, Shin BM. Clinical and epidemiological comparison of human metapneumovirus and respiratory syncytial virus in seoul, Korea, 2003–2008. J Korean Med Sci. 2010;25(3):342–7.

    Article  PubMed  PubMed Central  Google Scholar 

  29. To KKW, Lu L, Fong CHY, Wu AKL, Mok KY, Yip CCY, Ke YH, Sze KH, Lau SKP, Hung IFN, et al. Rhinovirus respiratory tract infection in hospitalized adult patients is associated with T. J Infect. 2018;76(5):465–74.

    Article  PubMed  Google Scholar 

  30. Hijikata N, Takayanagi N, Sato S, Harasawa K, Miyaoka K, Asanuma K, Kawabata Y. Adenovirus pneumonia in an immunocompetent adult. J Infect Chemother. 2012;18(5):780–5.

    Article  PubMed  Google Scholar 

  31. Midulla F, Scagnolari C, Bonci E, Pierangeli A, Antonelli G, De Angelis D, Berardi R, Moretti C. Respiratory syncytial virus, human bocavirus and rhinovirus bronchiolitis in infants. Arch Dis Child. 2010;95(1):35–41.

    Article  CAS  PubMed  Google Scholar 

  32. Matsumoto K, Inoue H. Viral infections in asthma and COPD. Respir Investig. 2014;52(2):92–100.

    Article  PubMed  Google Scholar 

  33. Lee JY, Park HJ, Kim YK, Yu S, Chong YP, Kim SH, Sung H, Lee SO, Kim MN, Lim CM, et al. Cellular profiles of bronchoalveolar lavage fluid and their prognostic significance for non-HIV-infected patients with pneumocystis jirovecii pneumonia. J Clin Microbiol. 2015;53(4):1310–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Editage (www.editage.com) for providing English language editing assistance.

Funding

This research did not receive any specific grants from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Department of Infectious, Respiratory and Digestive Medicine, Graduate School of Medicine, University of the Ryukyus, 207 Uehara, Nishihara, Okinawa, 903-0215, Japan

    Daijiro Nabeya, Michika Setoguchi, Shiho Ueno & Takeshi Kinjo

Authors
  1. Daijiro Nabeya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michika Setoguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shiho Ueno
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takeshi Kinjo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

DN contributed to the study conception, data acquisition, data analysis, and manuscript drafting. MS contributed to the data acquisition and critical manuscript revision. SU contributed to the data acquisition and critical manuscript revision. TK contributed to the study conception, data acquisition, data analysis, manuscript drafting, and critical manuscript revision. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Daijiro Nabeya.

Ethics declarations

Ethics approval and consent to participate

The requirement for written informed consent was waived because there were no new invasions in the subject cases and no personally identifiable information was handled by Department of Infectious, Respiratory and Digestive Medicine, Graduate School of Medicine, University of the Ryukyus. The study was approved by the Institutional Ethics Committees of the University of the Ryukyus. All methods were performed in accordance with the relevant guidelines and regulations.

Consent for publication

Not applicable. The medical records of all confirmed cases were retrospectively reviewed with identifying information removed.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nabeya, D., Setoguchi, M., Ueno, S. et al. Respiratory virus infections of the lower respiratory tract elevate bronchoalveolar lavage eosinophil fraction: a clinical retrospective study and case review. BMC Pulm Med 23, 111 (2023). https://doi.org/10.1186/s12890-023-02402-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12890-023-02402-x

Keywords

BMC Pulmonary Medicine

ISSN: 1471-2466

Contact us