Skip to main content
Log in

Clinical Features of Patients with Diffuse Alveolar Hemorrhage due to Negative-Pressure Pulmonary Edema

  • Published:
Lung Aims and scope Submit manuscript

Abstract

Purpose

Diffuse alveolar hemorrhage (DAH) with negative-pressure pulmonary edema (NPPE) is an uncommon yet life-threatening condition. We aimed at describing the circumstances, clinical, radiological, and bronchoscopic features, as well as the outcome of patients with NPPE-related DAH.

Methods

We performed a retrospective, observational cohort study, using data prospectively collected over 35 years in an intensive care unit (ICU).

Results

Of the 149 patients admitted for DAH, we identified 18 NPPE episodes in 15 patients, one admitted four times for recurrent NPPE-related DAH. The patients were primarily young, male, and athletic. The NPPE setting was postoperative (n = 12/18, 67%) or following generalized tonic–clonic seizures (n = 6/18, 33%). Hemoptysis was almost constant (n = 17/18, 94%), yet rarely massive (>200 cc, n = 1/18, 6%), with anemia observed in 10 (56%) episodes. The DAH triad (hemoptysis, anemia, and pulmonary infiltrates) was observed in 50% of episodes (n = 9/18), and acute respiratory failure in 94% (n = 17/18). Chest computed tomography revealed diffuse bilateral ground glass opacities (n = 10/10, 100%), while bronchoscopy detected bilateral hemorrhage (n = 12/12, 100%) and macroscopically bloody bronchoalveolar lavage, with siderophage absence in most (n = 7/8, 88%), indicating acute DAH. While one episode proved fatal, the other 17 recovered rapidly, with a mean ICU stay lasting 4.6 (2–15) days. Typically, the evolution was rapidly favorable under supportive care.

Conclusion

NPPE-related DAH is a rare life-threatening condition occurring primarily after tonic–clonic generalized seizure or generalized anesthesia. Clinical circumstances are a key to its diagnosis. Early diagnosis and recognition likely allow for successful management of this potentially serious complication, whereas ictal-DAH appears ominous in epileptic patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. de Prost N, Parrot A, Cuquemelle E, Picard C, Antoine M, Fleury-Feith J, Mayaud C, Boffa JJ, Fartoukh M, Cadranel J (2012) Diffuse alveolar hemorrhage in immunocompetent patients: etiologies and prognosis revisited. Respir Med 106(7):1021–1032. doi:10.1016/j.rmed.2012.03.015

    Article  PubMed  Google Scholar 

  2. Fremont RD, Kallet RH, Matthay MA, Ware LB (2007) Postobstructive pulmonary edema: a case for hydrostatic mechanisms. Chest 131(6):1742–1746. doi:10.1378/chest.06-2934

    Article  PubMed  PubMed Central  Google Scholar 

  3. Remy C, Parrot A, Lembert N, Marret E, Bonnet F (2006) Haemoptysis after anesthesia. Ann Fr Anesth Reanim 25(8):895–898. doi:10.1016/j.annfar.2006.03.039

    Article  CAS  PubMed  Google Scholar 

  4. Koh MS, Hsu AA, Eng P (2003) Negative pressure pulmonary oedema in the medical intensive care unit. Intensive Care Med 29(9):1601–1604. doi:10.1007/s00134-003-1896-7

    Article  PubMed  Google Scholar 

  5. Benson A, Schwarz M (2008) A 26-year-old woman with recurrent hemoptysis and a sleep disturbance. Chest 134(6):1325–1331. doi:10.1378/chest.08-1410

    Article  PubMed  Google Scholar 

  6. Sow Nam Y, Garewal D (2001) Pulmonary hemorrhage in association with negative pressure edema in an intubated patient. Acta Anaesthesiol Scand 45(7):911–913

    Article  CAS  PubMed  Google Scholar 

  7. Zulueta JJ, Gerblich AA (1992) Upper airway obstruction due to inhalation of a tracheal T-tube resulting in pulmonary edema. Chest 102(2):644–645

    Article  CAS  PubMed  Google Scholar 

  8. Bachmeyer C, Ferrari M, Muresan IP, d’Huart S, Langman B, Parrot A (2012) Generalised tonic-clonic seizure and diffuse alveolar haemorrhage. Neth J Med 71(1):34–37

    Google Scholar 

  9. Azuma M, Ito I, Matsumoto R, Hirai T, Mishima M (2012) Pulmonary hemorrhage induced by epileptic seizure. Heart Lung 41(3):290–293. doi:10.1016/j.hrtlng.2011.08.003

    Article  PubMed  Google Scholar 

  10. Meysman M, Noppen M, Herregodts P, Vincken W (1995) A patient with seizures, haemoptysis and dyspnoea. Eur Respir J 8(8):1433–1434

    Article  CAS  PubMed  Google Scholar 

  11. Ryu JS, Cho JH, Kwak SM, Lee HL, Lee IK (2002) Massive hemoptysis after generalized tonic clonic seizure requiring mechanical ventilation. Yonsei Med J 43(4):543–546

    Article  PubMed  Google Scholar 

  12. Darnell JC, Jay SJ (1982) Recurrent postictal pulmonary edema: a case report and review of the literature. Epilepsia 23(1):71–83

    Article  CAS  PubMed  Google Scholar 

  13. Dolinski SY, MacGregor DA, Scuderi PE (2000) Pulmonary hemorrhage associated with negative-pressure pulmonary edema. Anesthesiology 93(3):888–890

    Article  CAS  PubMed  Google Scholar 

  14. Koch SM, Abramson DC, Ford M, Peterson D, Katz J (1996) Bronchoscopic findings in post-obstructive pulmonary oedema. Can J Anaesth 43(1):73–76. doi:10.1007/BF03015962

    Article  CAS  PubMed  Google Scholar 

  15. McConkey P (2001) Airway bleeding in negative-pressure pulmonary edema. Anesthesiology 95(1):272

    Article  CAS  PubMed  Google Scholar 

  16. Le Gall JR, Lemeshow S, Saulnier F (1993) A new simplified acute physiology score (SAPS II) based on a European/North American multicenter study. JAMA 270(24):2957–2963

    Article  PubMed  Google Scholar 

  17. Jin SM, Yim JJ, Yoo CG, Kim YW, Han SK, Shim YS, Lee SM (2009) Aetiologies and outcomes of diffuse alveolar haemorrhage presenting as acute respiratory failure of uncertain cause. Respirology 14(2):290–294. doi:10.1111/j.1440-1843.2008.01444.x

    Article  PubMed  Google Scholar 

  18. Leatherman JW, Davies SF, Hoidal JR (1984) Alveolar hemorrhage syndromes: diffuse microvascular lung hemorrhage in immune and idiopathic disorders. Medicine 63(6):343–361 (Baltimore)

    Article  CAS  PubMed  Google Scholar 

  19. Roopa S (2012) Recurrent unilateral negative pressure pulmonary oedema. Anaesthesia 67(8):931–932. doi:10.1111/j.1365-2044.2012.07252.x

    Article  CAS  PubMed  Google Scholar 

  20. Sherman JM, Winnie G, Thomassen MJ, Abdul-Karim FW, Boat TF (1984) Time course of hemosiderin production and clearance by human pulmonary macrophages. Chest 86(3):409–411

    Article  CAS  PubMed  Google Scholar 

  21. Goli AK, Goli SA, Byrd RP Jr, Roy TM (2003) Spontaneous negative pressure changes: an unusual cause of noncardiogenic pulmonary edema. J Ky Med Assoc 101(8):317–320

    PubMed  Google Scholar 

  22. McConkey PP (2000) Postobstructive pulmonary oedema–a case series and review. Anaesth Intensive Care 28(1):72–76

    CAS  PubMed  Google Scholar 

  23. Visvanathan T, Kluger MT, Webb RK, Westhorpe RN (2005) Crisis management during anaesthesia: laryngospasm. Qual Saf Health Care 14(3):e3. doi:10.1136/qshc.2002.004275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ezri T, Priscu V, Szmuk P, Soroker D (1993) Laryngeal mask and pulmonary edema. Anesthesiology 78(1):219

    Article  CAS  PubMed  Google Scholar 

  25. Bhavani-Shankar K, Hart NS, Mushlin PS (1997) Negative pressure induced airway and pulmonary injury. Can J Anaesth 44(1):78–81. doi:10.1007/BF03014328

    Article  CAS  PubMed  Google Scholar 

  26. Saeed AI, Quintana C, McGuire FR, Barker JA (2012) Delayed presentation: negative pressure pulmonary hemorrhage. J Clin Anesth 24(6):490–493. doi:10.1016/j.jclinane.2012.02.001

    Article  PubMed  Google Scholar 

  27. Pacht ER (1988) Postictal pulmonary edema and hemoptysis. J Natl Med Assoc 80 (3):337–339, 342

  28. Tavee J, Morris H 3rd (2008) Severe postictal laryngospasm as a potential mechanism for sudden unexpected death in epilepsy: a near-miss in an EMU. Epilepsia 49(12):2113–2117. doi:10.1111/j.1528-1167.2008.01781.x

    Article  PubMed  Google Scholar 

  29. Tsuchihashi K, Ueshima K, Uchida T, Oh-mura N, Kimura K, Owa M, Yoshiyama M, Miyazaki S, Haze K, Ogawa H, Honda T, Hase M, Kai R, Morii I (2001) Transient left ventricular apical ballooning without coronary artery stenosis: a novel heart syndrome mimicking acute myocardial infarction. J Am Coll Cardiol 38(1):11–18 Angina Pectoris-Myocardial Infarction Investigations in Japan

    Article  CAS  PubMed  Google Scholar 

  30. Lemke DM, Hussain SI, Wolfe TJ, Torbey MA, Lynch JR, Carlin A, Fitzsimmons BF, Zaidat OO (2008) Takotsubo cardiomyopathy associated with seizures. Neurocritical Care 9(1):112–117. doi:10.1007/s12028-008-9075-x

    Article  PubMed  Google Scholar 

  31. Sleiman C, Raffy O, Roue C, Mal H (2000) Fatal pulmonary hemorrhage during high-dose valproate monotherapy. Chest 117(2):613

    Article  CAS  PubMed  Google Scholar 

  32. Wilschut FA, Cobben NA, Thunnissen FB, Lamers RJ, Wouters EF, Drent M (1997) Recurrent respiratory distress associated with carbamazepine overdose. Eur Respir J 10(9):2163–2165

    Article  CAS  PubMed  Google Scholar 

  33. Rahn H, Otis AB et al (1946) The pressure-volume diagram of the thorax and lung. Am J Physiol 146(2):161–178

    CAS  PubMed  Google Scholar 

  34. Kopterides P, Tsangaris I, Armaganidis A (2007) Postobstructive pulmonary edema: a case for hydrostatic mechanisms. Chest 132(6):2056. doi:10.1378/chest.07-1650 author reply 2057

    Article  PubMed  Google Scholar 

  35. Lorch DG, Sahn SA (1986) Post-extubation pulmonary edema following anesthesia induced by upper airway obstruction. Are certain patients at increased risk? Chest 90(6):802–805

    Article  CAS  PubMed  Google Scholar 

  36. Mehta VM, Har-El G, Goldstein NA (2006) Postobstructive pulmonary edema after laryngospasm in the otolaryngology patient. Laryngoscope 116(9):1693–1696. doi:10.1097/01.mlg.0000231762.91541.3a

    Article  PubMed  Google Scholar 

  37. Schwartz DR, Maroo A, Malhotra A, Kesselman H (1999) Negative pressure pulmonary hemorrhage. Chest 115(4):1194–1197

    Article  CAS  PubMed  Google Scholar 

  38. Oswalt CE, Gates GA, Holmstrom MG (1977) Pulmonary edema as a complication of acute airway obstruction. JAMA 238(17):1833–1835

    Article  CAS  PubMed  Google Scholar 

  39. Jackson FN, Rowland V, Corssen G (1980) Laryngospasm-induced pulmonary edema. Chest 78(6):819–821

    Article  CAS  PubMed  Google Scholar 

  40. Attias D, Mansencal N, Auvert B, Vieillard-Baron A, Delos A, Lacombe P, N’Guetta R, Jardin F, Dubourg O (2010) Prevalence, characteristics, and outcomes of patients presenting with cardiogenic unilateral pulmonary edema. Circulation 122(11):1109–1115. doi:10.1161/CIRCULATIONAHA.109.934950

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Damien Contou.

Ethics declarations

Conflict of interest

None of the authors have any conflict of interest associated with the work presented in this manuscript.

Ethical Approval

The institutional review board of the French learned society for respiratory medicine (Société de Pneumologie de Langue Française) approved this retrospective non-interventional study, waiving the need for informed consent.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 19 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Contou, D., Voiriot, G., Djibré, M. et al. Clinical Features of Patients with Diffuse Alveolar Hemorrhage due to Negative-Pressure Pulmonary Edema. Lung 195, 477–487 (2017). https://doi.org/10.1007/s00408-017-0011-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00408-017-0011-8

Keywords

Navigation