Skip to main content
Top
Published in: BMC Infectious Diseases 1/2013

Open Access 01-12-2013 | Research article

Cardiopulmonary involvement in Puumala hantavirus infection

Authors: Johan Rasmuson, Per Lindqvist, Karen Sörensen, Magnus Hedström, Anders Blomberg, Clas Ahlm

Published in: BMC Infectious Diseases | Issue 1/2013

Login to get access

Abstract

Background

Hantavirus infections cause potentially life-threatening disease in humans world-wide. Infections with American hantaviruses may lead to hantavirus pulmonary syndrome characterised by severe cardiopulmonary distress with high mortality. Pulmonary involvement in European Puumala hantavirus (PUUV) infection has been reported, whereas knowledge of potential cardiac manifestations is limited. We aimed to comprehensively investigate cardiopulmonary involvement in patients with PUUV-infection.

Methods

Twenty-seven hospitalised patients with PUUV-infection were examined with lung function tests, chest high-resolution CT (HRCT), echocardiography including speckle tracking strain rate analysis, ECG and measurements of cardiac biomarkers N-terminal pro-B-type natriuretic peptide (NT-ProBNP) and troponin T. Patients were re-evaluated after 3 months. Twenty-five age and sex-matched volunteers acted as controls for echocardiography data.

Results

Two-thirds of the patients experienced respiratory symptoms as dry cough or dyspnoea. Gas diffusing capacity was impaired in most patients, significantly improving at follow-up but still subnormal in 38%. HRCT showed thoracic effusions or pulmonary oedema in 46% of the patients. Compared to controls, the main echocardiographic findings in patients during the acute phase were significantly higher pulmonary vascular resistance, higher systolic pulmonary artery pressure, lower left ventricular ejection fraction and impaired left atrial myocardial motion. Pathological ECG, atrial fibrillation or T-wave changes, was demonstrated in 26% of patients. NT-ProBNP concentrations were markedly increased and were inversely associated with gas diffusing capacity but positively correlated to pulmonary vascular resistance. Furthermore, patients experiencing impaired general condition at follow-up had significantly lower gas diffusing capacity and higher pulmonary vascular resistance, compared to those feeling fully recovered.

Conclusions

In a majority of patients with PUUV-infection, both cardiac and pulmonary involvement was demonstrated with implications on patients’ recovery. The results demonstrate vascular leakage in the lungs that most likely is responsible for impaired gas diffusing capacity and increased pulmonary vascular resistance with secondary pulmonary hypertension and right heart distress. Interestingly, NT-ProBNP was markedly elevated even in the absence of overt ventricular heart failure. The method of simultaneous investigations of important cardiac and respiratory measurements improves the interpretation of the underlying pathophysiologic mechanisms.
Appendix
Available only for authorised users
Literature
1.
go back to reference Jonsson CB, Figueiredo LT, Vapalahti O: A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev. 2010, 23: 412-441. 10.1128/CMR.00062-09.CrossRefPubMedPubMedCentral Jonsson CB, Figueiredo LT, Vapalahti O: A global perspective on hantavirus ecology, epidemiology, and disease. Clin Microbiol Rev. 2010, 23: 412-441. 10.1128/CMR.00062-09.CrossRefPubMedPubMedCentral
2.
go back to reference Botten J, Mirowsky K, Ye C, Gottlieb K, Saavedra M, Ponce L, Hjelle B: Shedding and intracage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model. J Virol. 2002, 76: 7587-7594. 10.1128/JVI.76.15.7587-7594.2002.CrossRefPubMedPubMedCentral Botten J, Mirowsky K, Ye C, Gottlieb K, Saavedra M, Ponce L, Hjelle B: Shedding and intracage transmission of Sin Nombre hantavirus in the deer mouse (Peromyscus maniculatus) model. J Virol. 2002, 76: 7587-7594. 10.1128/JVI.76.15.7587-7594.2002.CrossRefPubMedPubMedCentral
3.
go back to reference Hardestam J, Karlsson M, Falk KI, Olsson G, Klingström J, Lundkvist Å: Puumala hantavirus excretion kinetics in bank voles (Myodes glareolus). Emerg Infect Dis. 2008, 14: 1209-1215. 10.3201/eid1408.080221.CrossRefPubMedPubMedCentral Hardestam J, Karlsson M, Falk KI, Olsson G, Klingström J, Lundkvist Å: Puumala hantavirus excretion kinetics in bank voles (Myodes glareolus). Emerg Infect Dis. 2008, 14: 1209-1215. 10.3201/eid1408.080221.CrossRefPubMedPubMedCentral
4.
go back to reference Duchin JS, Koster FT, Peters CJ, Simpson GL, Tempest B, Zaki SR, Ksiazek TG, Rollin PE, Nichol S, Umland ET, et al: Hantavirus pulmonary syndrome: a clinical description of 17 patients with a newly recognized disease. The Hantavirus Study Group. N Engl J Med. 1994, 330: 949-955. 10.1056/NEJM199404073301401.CrossRefPubMed Duchin JS, Koster FT, Peters CJ, Simpson GL, Tempest B, Zaki SR, Ksiazek TG, Rollin PE, Nichol S, Umland ET, et al: Hantavirus pulmonary syndrome: a clinical description of 17 patients with a newly recognized disease. The Hantavirus Study Group. N Engl J Med. 1994, 330: 949-955. 10.1056/NEJM199404073301401.CrossRefPubMed
5.
go back to reference Hallin GW, Simpson SQ, Crowell RE, James DS, Koster FT, Mertz GJ, Levy H: Cardiopulmonary manifestations of hantavirus pulmonary syndrome. Crit Care Med. 1996, 24: 252-258. 10.1097/00003246-199602000-00012.CrossRefPubMed Hallin GW, Simpson SQ, Crowell RE, James DS, Koster FT, Mertz GJ, Levy H: Cardiopulmonary manifestations of hantavirus pulmonary syndrome. Crit Care Med. 1996, 24: 252-258. 10.1097/00003246-199602000-00012.CrossRefPubMed
6.
go back to reference Castillo C, Naranjo J, Sepulveda A, Ossa G, Levy H: Hantavirus pulmonary syndrome due to Andes virus in Temuco, Chile: clinical experience with 16 adults. Chest. 2001, 120: 548-554. 10.1378/chest.120.2.548.CrossRefPubMed Castillo C, Naranjo J, Sepulveda A, Ossa G, Levy H: Hantavirus pulmonary syndrome due to Andes virus in Temuco, Chile: clinical experience with 16 adults. Chest. 2001, 120: 548-554. 10.1378/chest.120.2.548.CrossRefPubMed
7.
go back to reference Vapalahti O, Mustonen J, Lundkvist Å, Henttonen H, Plyusnin A, Vaheri A: Hantavirus infections in Europe. Lancet Infect Dis. 2003, 3: 653-661. 10.1016/S1473-3099(03)00774-6.CrossRefPubMed Vapalahti O, Mustonen J, Lundkvist Å, Henttonen H, Plyusnin A, Vaheri A: Hantavirus infections in Europe. Lancet Infect Dis. 2003, 3: 653-661. 10.1016/S1473-3099(03)00774-6.CrossRefPubMed
8.
go back to reference Clement J, Colson P, McKenna P: Hantavirus pulmonary syndrome in New England and Europe. N Engl J Med. 1994, 331: 545-546.CrossRefPubMed Clement J, Colson P, McKenna P: Hantavirus pulmonary syndrome in New England and Europe. N Engl J Med. 1994, 331: 545-546.CrossRefPubMed
9.
go back to reference Linderholm M, Sandström T, Rinnström O, Groth S, Blomberg A, Tärnvik A: Impaired pulmonary function in patients with hemorrhagic fever with renal syndrome. Clin Infect Dis. 1997, 25: 1084-1089. 10.1086/516093.CrossRefPubMed Linderholm M, Sandström T, Rinnström O, Groth S, Blomberg A, Tärnvik A: Impaired pulmonary function in patients with hemorrhagic fever with renal syndrome. Clin Infect Dis. 1997, 25: 1084-1089. 10.1086/516093.CrossRefPubMed
10.
go back to reference Seitsonen E, Hynninen M, Kolho E, Kallio-Kokko H, Pettilä V: Corticosteroids combined with continuous veno-venous hemodiafiltration for treatment of hantavirus pulmonary syndrome caused by Puumala virus infection. Eur J Clin Microbiol Infect Dis. 2006, 25: 261-266. 10.1007/s10096-006-0117-z.CrossRefPubMed Seitsonen E, Hynninen M, Kolho E, Kallio-Kokko H, Pettilä V: Corticosteroids combined with continuous veno-venous hemodiafiltration for treatment of hantavirus pulmonary syndrome caused by Puumala virus infection. Eur J Clin Microbiol Infect Dis. 2006, 25: 261-266. 10.1007/s10096-006-0117-z.CrossRefPubMed
11.
go back to reference Rasmuson J, Andersson C, Norrman E, Haney M, Evander M, Ahlm C: Time to revise the paradigm of hantavirus syndromes? Hantavirus pulmonary syndrome caused by European hantavirus. Eur J Clin Microbiol Infect Dis. 2011, 30: 685-690. 10.1007/s10096-010-1141-6.CrossRefPubMedPubMedCentral Rasmuson J, Andersson C, Norrman E, Haney M, Evander M, Ahlm C: Time to revise the paradigm of hantavirus syndromes? Hantavirus pulmonary syndrome caused by European hantavirus. Eur J Clin Microbiol Infect Dis. 2011, 30: 685-690. 10.1007/s10096-010-1141-6.CrossRefPubMedPubMedCentral
12.
go back to reference Rasmuson J, Pourazar J, Linderholm M, Sandström T, Blomberg A, Ahlm C: Presence of activated airway T lymphocytes in human puumala hantavirus disease. Chest. 2011, 140: 715-722. 10.1378/chest.10-2791.CrossRefPubMed Rasmuson J, Pourazar J, Linderholm M, Sandström T, Blomberg A, Ahlm C: Presence of activated airway T lymphocytes in human puumala hantavirus disease. Chest. 2011, 140: 715-722. 10.1378/chest.10-2791.CrossRefPubMed
13.
go back to reference Linderholm M, Billström A, Settergren B, Tärnvik A: Pulmonary involvement in nephropathia epidemica as demonstrated by computed tomography. Infection. 1992, 20: 263-266. 10.1007/BF01710791.CrossRefPubMed Linderholm M, Billström A, Settergren B, Tärnvik A: Pulmonary involvement in nephropathia epidemica as demonstrated by computed tomography. Infection. 1992, 20: 263-266. 10.1007/BF01710791.CrossRefPubMed
14.
go back to reference Paakkala A, Järvenpää R, Mäkelä S, Huhtala H, Mustonen J: Pulmonary high-resolution computed tomography findings in nephropathia epidemica. Eur J Radiol. 2012, 81: 1707-1711. 10.1016/j.ejrad.2011.04.049.CrossRefPubMed Paakkala A, Järvenpää R, Mäkelä S, Huhtala H, Mustonen J: Pulmonary high-resolution computed tomography findings in nephropathia epidemica. Eur J Radiol. 2012, 81: 1707-1711. 10.1016/j.ejrad.2011.04.049.CrossRefPubMed
15.
go back to reference Linderholm M, Bjermer L, Juto P, Roos G, Sandström T, Settergren B, Tärnvik A: Local host response in the lower respiratory tract in nephropathia epidemica. Scand J Infect Dis. 1993, 25: 639-646. 10.3109/00365549309008554.CrossRefPubMed Linderholm M, Bjermer L, Juto P, Roos G, Sandström T, Settergren B, Tärnvik A: Local host response in the lower respiratory tract in nephropathia epidemica. Scand J Infect Dis. 1993, 25: 639-646. 10.3109/00365549309008554.CrossRefPubMed
16.
go back to reference Nolte KB, Feddersen RM, Foucar K, Zaki SR, Koster FT, Madar D, Merlin TL, McFeeley PJ, Umland ET, Zumwalt RE: Hantavirus pulmonary syndrome in the United States: a pathological description of a disease caused by a new agent. Hum Pathol. 1995, 26: 110-120. 10.1016/0046-8177(95)90123-X.CrossRefPubMed Nolte KB, Feddersen RM, Foucar K, Zaki SR, Koster FT, Madar D, Merlin TL, McFeeley PJ, Umland ET, Zumwalt RE: Hantavirus pulmonary syndrome in the United States: a pathological description of a disease caused by a new agent. Hum Pathol. 1995, 26: 110-120. 10.1016/0046-8177(95)90123-X.CrossRefPubMed
17.
go back to reference Zaki SR, Greer PW, Coffield LM, Goldsmith CS, Nolte KB, Foucar K, Feddersen RM, Zumwalt RE, Miller GL, Khan AS, et al: Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am J Pathol. 1995, 146: 552-579.PubMedPubMedCentral Zaki SR, Greer PW, Coffield LM, Goldsmith CS, Nolte KB, Foucar K, Feddersen RM, Zumwalt RE, Miller GL, Khan AS, et al: Hantavirus pulmonary syndrome. Pathogenesis of an emerging infectious disease. Am J Pathol. 1995, 146: 552-579.PubMedPubMedCentral
18.
go back to reference Puljiz I, Kuzman I, Markotic A, Turcinov D, Matic M, Makek N: Electrocardiographic changes in patients with haemorrhagic fever with renal syndrome. Scand J Infect Dis. 2005, 37: 594-598. 10.1080/00365540510036606.CrossRefPubMed Puljiz I, Kuzman I, Markotic A, Turcinov D, Matic M, Makek N: Electrocardiographic changes in patients with haemorrhagic fever with renal syndrome. Scand J Infect Dis. 2005, 37: 594-598. 10.1080/00365540510036606.CrossRefPubMed
19.
go back to reference Mäkelä S, Kokkonen L, Ala-Houhala I, Groundstroem K, Harmoinen A, Huhtala H, Hurme M, Paakkala A, Pörsti I, Virtanen V, et al: More than half of the patients with acute Puumala hantavirus infection have abnormal cardiac findings. Scand J Infect Dis. 2009, 41: 57-62. 10.1080/00365540802502629.CrossRefPubMed Mäkelä S, Kokkonen L, Ala-Houhala I, Groundstroem K, Harmoinen A, Huhtala H, Hurme M, Paakkala A, Pörsti I, Virtanen V, et al: More than half of the patients with acute Puumala hantavirus infection have abnormal cardiac findings. Scand J Infect Dis. 2009, 41: 57-62. 10.1080/00365540802502629.CrossRefPubMed
20.
go back to reference Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CP, Gustafsson P, et al: Standardisation of spirometry. Eur Respir J. 2005, 26: 319-338. 10.1183/09031936.05.00034805.CrossRefPubMed Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CP, Gustafsson P, et al: Standardisation of spirometry. Eur Respir J. 2005, 26: 319-338. 10.1183/09031936.05.00034805.CrossRefPubMed
21.
go back to reference Macintyre N, Crapo RO, Viegi G, Johnson DC, van der Grinten CP, Brusasco V, Burgos F, Casaburi R, Coates A, Enright P, et al: Standardisation of the single-breath determination of carbon monoxide uptake in the lung. Eur Respir J. 2005, 26: 720-735. 10.1183/09031936.05.00034905.CrossRefPubMed Macintyre N, Crapo RO, Viegi G, Johnson DC, van der Grinten CP, Brusasco V, Burgos F, Casaburi R, Coates A, Enright P, et al: Standardisation of the single-breath determination of carbon monoxide uptake in the lung. Eur Respir J. 2005, 26: 720-735. 10.1183/09031936.05.00034905.CrossRefPubMed
22.
go back to reference Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault JC: Lung volumes and forced ventilatory flows. Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society. Eur Respir J Suppl. 1993, 16: 5-40.CrossRefPubMed Quanjer PH, Tammeling GJ, Cotes JE, Pedersen OF, Peslin R, Yernault JC: Lung volumes and forced ventilatory flows. Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society. Eur Respir J Suppl. 1993, 16: 5-40.CrossRefPubMed
23.
go back to reference Cotes JE, Chinn DJ, Quanjer PH, Roca J, Yernault JC: Standardization of the measurement of transfer factor (diffusing capacity). Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society. Eur Respir J Suppl. 1993, 16: 41-52.CrossRefPubMed Cotes JE, Chinn DJ, Quanjer PH, Roca J, Yernault JC: Standardization of the measurement of transfer factor (diffusing capacity). Report Working Party Standardization of Lung Function Tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society. Eur Respir J Suppl. 1993, 16: 41-52.CrossRefPubMed
24.
go back to reference Quinones MA, Otto CM, Stoddard M, Waggoner A, Zoghbi WA: Recommendations for quantification of Doppler echocardiography: a report from the Doppler Quantification Task Force of the Nomenclature and Standards Committee of the American Society of Echocardiography. J Am Soc Echocardiogr. 2002, 15: 167-184. 10.1067/mje.2002.120202.CrossRefPubMed Quinones MA, Otto CM, Stoddard M, Waggoner A, Zoghbi WA: Recommendations for quantification of Doppler echocardiography: a report from the Doppler Quantification Task Force of the Nomenclature and Standards Committee of the American Society of Echocardiography. J Am Soc Echocardiogr. 2002, 15: 167-184. 10.1067/mje.2002.120202.CrossRefPubMed
25.
go back to reference Sahn DJ, DeMaria A, Kisslo J, Weyman A: Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation. 1978, 58: 1072-1083. 10.1161/01.CIR.58.6.1072.CrossRefPubMed Sahn DJ, DeMaria A, Kisslo J, Weyman A: Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation. 1978, 58: 1072-1083. 10.1161/01.CIR.58.6.1072.CrossRefPubMed
26.
go back to reference Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, et al: Recommendations for chamber quantification: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr. 2005, 18: 1440-1463. 10.1016/j.echo.2005.10.005.CrossRefPubMed Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, et al: Recommendations for chamber quantification: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr. 2005, 18: 1440-1463. 10.1016/j.echo.2005.10.005.CrossRefPubMed
27.
go back to reference Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelisa A: Recommendations for the evaluation of left ventricular diastolic function by echocardiography. Eur J Echocardiogr. 2009, 10: 165-193. 10.1093/ejechocard/jen204.CrossRefPubMed Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelisa A: Recommendations for the evaluation of left ventricular diastolic function by echocardiography. Eur J Echocardiogr. 2009, 10: 165-193. 10.1093/ejechocard/jen204.CrossRefPubMed
28.
go back to reference Chemla D, Castelain V, Humbert M, Hebert JL, Simonneau G, Lecarpentier Y, Herve P: New formula for predicting mean pulmonary artery pressure using systolic pulmonary artery pressure. Chest. 2004, 126: 1313-1317. 10.1378/chest.126.4.1313.CrossRefPubMed Chemla D, Castelain V, Humbert M, Hebert JL, Simonneau G, Lecarpentier Y, Herve P: New formula for predicting mean pulmonary artery pressure using systolic pulmonary artery pressure. Chest. 2004, 126: 1313-1317. 10.1378/chest.126.4.1313.CrossRefPubMed
29.
go back to reference Lindqvist P, Söderberg S, Gonzalez MC, Tossavainen E, Henein MY: Echocardiography based estimation of pulmonary vascular resistance in patients with pulmonary hypertension: a simultaneous Doppler echocardiography and cardiac catheterization study. Eur J Echocardiogr. 2011, 12: 961-966. 10.1093/ejechocard/jer222.CrossRefPubMed Lindqvist P, Söderberg S, Gonzalez MC, Tossavainen E, Henein MY: Echocardiography based estimation of pulmonary vascular resistance in patients with pulmonary hypertension: a simultaneous Doppler echocardiography and cardiac catheterization study. Eur J Echocardiogr. 2011, 12: 961-966. 10.1093/ejechocard/jer222.CrossRefPubMed
30.
go back to reference Wahl A, Praz F, Schwerzmann M, Bonel H, Koestner SC, Hullin R, Schmid JP, Stuber T, Delacretaz E, Hess OM, et al: Assessment of right ventricular systolic function: comparison between cardiac magnetic resonance derived ejection fraction and pulsed-wave tissue Doppler imaging of the tricuspid annulus. Int J Cardiol. 2011, 151: 58-62. 10.1016/j.ijcard.2010.04.089.CrossRefPubMed Wahl A, Praz F, Schwerzmann M, Bonel H, Koestner SC, Hullin R, Schmid JP, Stuber T, Delacretaz E, Hess OM, et al: Assessment of right ventricular systolic function: comparison between cardiac magnetic resonance derived ejection fraction and pulsed-wave tissue Doppler imaging of the tricuspid annulus. Int J Cardiol. 2011, 151: 58-62. 10.1016/j.ijcard.2010.04.089.CrossRefPubMed
31.
go back to reference Tossavainen E, Söderberg S, Grönlund C, Gonzalez M, Henein MY, Lindqvist P: Pulmonary artery acceleration time in identifying pulmonary hypertension patients with raised pulmonary vascular resistance. Eur Heart J Cardiovasc Imaging. in press Tossavainen E, Söderberg S, Grönlund C, Gonzalez M, Henein MY, Lindqvist P: Pulmonary artery acceleration time in identifying pulmonary hypertension patients with raised pulmonary vascular resistance. Eur Heart J Cardiovasc Imaging. in press
32.
go back to reference Lindqvist P, Waldenström A, Wikström G, Kazzam E: Right ventricular myocardial isovolumic relaxation time and pulmonary pressure. Clin Physiol Funct Imaging. 2006, 26: 1-8. 10.1111/j.1475-097X.2005.00639.x.CrossRefPubMed Lindqvist P, Waldenström A, Wikström G, Kazzam E: Right ventricular myocardial isovolumic relaxation time and pulmonary pressure. Clin Physiol Funct Imaging. 2006, 26: 1-8. 10.1111/j.1475-097X.2005.00639.x.CrossRefPubMed
33.
go back to reference Henein M, Zhao Y, Henein MY, Lindqvist P: Disturbed left atrial mechanical function in paroxysmal atrial fibrillation: a speckle tracking study. Int J Cardiol. 2012, 155: 437-441. 10.1016/j.ijcard.2011.10.007.CrossRefPubMed Henein M, Zhao Y, Henein MY, Lindqvist P: Disturbed left atrial mechanical function in paroxysmal atrial fibrillation: a speckle tracking study. Int J Cardiol. 2012, 155: 437-441. 10.1016/j.ijcard.2011.10.007.CrossRefPubMed
34.
go back to reference Lindqvist P, Zhao Y, Bajraktari G, Holmgren A, Henein MY: Aortic valve replacement normalizes left ventricular twist function. Interact Cardiovasc Thorac Surg. 2011, 12: 701-706. 10.1510/icvts.2010.262303.CrossRefPubMed Lindqvist P, Zhao Y, Bajraktari G, Holmgren A, Henein MY: Aortic valve replacement normalizes left ventricular twist function. Interact Cardiovasc Thorac Surg. 2011, 12: 701-706. 10.1510/icvts.2010.262303.CrossRefPubMed
35.
go back to reference Sundberg E, Hultdin J, Nilsson S, Ahlm C: Evidence of disseminated intravascular coagulation in a hemorrhagic fever with renal syndrome-scoring models and severe illness. PLoS One. 2011, 6: e21134-10.1371/journal.pone.0021134.CrossRefPubMedPubMedCentral Sundberg E, Hultdin J, Nilsson S, Ahlm C: Evidence of disseminated intravascular coagulation in a hemorrhagic fever with renal syndrome-scoring models and severe illness. PLoS One. 2011, 6: e21134-10.1371/journal.pone.0021134.CrossRefPubMedPubMedCentral
36.
go back to reference Zapol WM, Snider MT: Pulmonary hypertension in severe acute respiratory failure. N Engl J Med. 1977, 296: 476-480. 10.1056/NEJM197703032960903.CrossRefPubMed Zapol WM, Snider MT: Pulmonary hypertension in severe acute respiratory failure. N Engl J Med. 1977, 296: 476-480. 10.1056/NEJM197703032960903.CrossRefPubMed
37.
go back to reference Mackow ER, Gavrilovskaya IN: Hantavirus regulation of endothelial cell functions. Thromb Haemost. 2009, 102: 1030-1041.PubMed Mackow ER, Gavrilovskaya IN: Hantavirus regulation of endothelial cell functions. Thromb Haemost. 2009, 102: 1030-1041.PubMed
38.
go back to reference Geimonen E, Neff S, Raymond T, Kocer SS, Gavrilovskaya IN, Mackow ER: Pathogenic and nonpathogenic hantaviruses differentially regulate endothelial cell responses. Proc Natl Acad Sci U S A. 2002, 99: 13837-13842. 10.1073/pnas.192298899.CrossRefPubMedPubMedCentral Geimonen E, Neff S, Raymond T, Kocer SS, Gavrilovskaya IN, Mackow ER: Pathogenic and nonpathogenic hantaviruses differentially regulate endothelial cell responses. Proc Natl Acad Sci U S A. 2002, 99: 13837-13842. 10.1073/pnas.192298899.CrossRefPubMedPubMedCentral
39.
go back to reference Hayasaka D, Maeda K, Ennis FA, Terajima M: Increased permeability of human endothelial cell line EA.hy926 induced by hantavirus-specific cytotoxic T lymphocytes. Virus Res. 2007, 123: 120-127. 10.1016/j.virusres.2006.08.006.CrossRefPubMed Hayasaka D, Maeda K, Ennis FA, Terajima M: Increased permeability of human endothelial cell line EA.hy926 induced by hantavirus-specific cytotoxic T lymphocytes. Virus Res. 2007, 123: 120-127. 10.1016/j.virusres.2006.08.006.CrossRefPubMed
40.
go back to reference Shrivastava-Ranjan P, Rollin PE, Spiropoulou CF: Andes virus disrupts the endothelial cell barrier by induction of vascular endothelial growth factor and downregulation of VE-cadherin. J Virol. 2010, 84: 11227-11234. 10.1128/JVI.01405-10.CrossRefPubMedPubMedCentral Shrivastava-Ranjan P, Rollin PE, Spiropoulou CF: Andes virus disrupts the endothelial cell barrier by induction of vascular endothelial growth factor and downregulation of VE-cadherin. J Virol. 2010, 84: 11227-11234. 10.1128/JVI.01405-10.CrossRefPubMedPubMedCentral
41.
go back to reference Hassoun PM, Mouthon L, Barbera JA, Eddahibi S, Flores SC, Grimminger F, Jones PL, Maitland ML, Michelakis ED, Morrell NW, et al: Inflammation, growth factors, and pulmonary vascular remodeling. J Am Coll Cardiol. 2009, 54 (1 Suppl): S10-19.CrossRefPubMed Hassoun PM, Mouthon L, Barbera JA, Eddahibi S, Flores SC, Grimminger F, Jones PL, Maitland ML, Michelakis ED, Morrell NW, et al: Inflammation, growth factors, and pulmonary vascular remodeling. J Am Coll Cardiol. 2009, 54 (1 Suppl): S10-19.CrossRefPubMed
42.
go back to reference Laine O, Mäkelä S, Mustonen J, Huhtala H, Szanto T, Vaheri A, Lassila R, Joutsi-Korhonen L: Enhanced thrombin formation and fibrinolysis during acute Puumala hantavirus infection. Thromb Res. 2010, 126: 154-158. 10.1016/j.thromres.2010.05.025.CrossRefPubMed Laine O, Mäkelä S, Mustonen J, Huhtala H, Szanto T, Vaheri A, Lassila R, Joutsi-Korhonen L: Enhanced thrombin formation and fibrinolysis during acute Puumala hantavirus infection. Thromb Res. 2010, 126: 154-158. 10.1016/j.thromres.2010.05.025.CrossRefPubMed
43.
go back to reference Young JD: The heart and circulation in severe sepsis. Br J Anaesth. 2004, 93: 114-120. 10.1093/bja/aeh171.CrossRefPubMed Young JD: The heart and circulation in severe sepsis. Br J Anaesth. 2004, 93: 114-120. 10.1093/bja/aeh171.CrossRefPubMed
44.
go back to reference Finkel MS, Oddis CV, Jacob TD, Watkins SC, Hattler BG, Simmons RL: Negative inotropic effects of cytokines on the heart mediated by nitric oxide. Science. 1992, 257: 387-389. 10.1126/science.1631560.CrossRefPubMed Finkel MS, Oddis CV, Jacob TD, Watkins SC, Hattler BG, Simmons RL: Negative inotropic effects of cytokines on the heart mediated by nitric oxide. Science. 1992, 257: 387-389. 10.1126/science.1631560.CrossRefPubMed
45.
go back to reference Hartemink KJ, Groeneveld AB: The hemodynamics of human septic shock relate to circulating innate immunity factors. Immunol Invest. 2010, 39: 849-862. 10.3109/08820139.2010.502949.CrossRefPubMed Hartemink KJ, Groeneveld AB: The hemodynamics of human septic shock relate to circulating innate immunity factors. Immunol Invest. 2010, 39: 849-862. 10.3109/08820139.2010.502949.CrossRefPubMed
46.
go back to reference Linderholm M, Groeneveld PH, Tärnvik A: Increased production of nitric oxide in patients with hemorrhagic fever with renal syndrome - relation to arterial hypotension and tumor necrosis factor. Infection. 1996, 24: 337-340. 10.1007/BF01716075.CrossRefPubMed Linderholm M, Groeneveld PH, Tärnvik A: Increased production of nitric oxide in patients with hemorrhagic fever with renal syndrome - relation to arterial hypotension and tumor necrosis factor. Infection. 1996, 24: 337-340. 10.1007/BF01716075.CrossRefPubMed
47.
go back to reference Saggioro FP, Rossi MA, Duarte MI, Martin CC, Alves VA, Moreli ML, Figueiredo LT, Moreira JE, Borges AA, Neder L: Hantavirus infection induces a typical myocarditis that may be responsible for myocardial depression and shock in hantavirus pulmonary syndrome. J Infect Dis. 2007, 195: 1541-1549. 10.1086/513874.CrossRefPubMed Saggioro FP, Rossi MA, Duarte MI, Martin CC, Alves VA, Moreli ML, Figueiredo LT, Moreira JE, Borges AA, Neder L: Hantavirus infection induces a typical myocarditis that may be responsible for myocardial depression and shock in hantavirus pulmonary syndrome. J Infect Dis. 2007, 195: 1541-1549. 10.1086/513874.CrossRefPubMed
48.
go back to reference Woods RL: Cardioprotective functions of atrial natriuretic peptide and B-type natriuretic peptide: a brief review. Clin Exp Pharmacol Physiol. 2004, 31: 791-794. 10.1111/j.0305-1870.2004.04073.x.CrossRefPubMed Woods RL: Cardioprotective functions of atrial natriuretic peptide and B-type natriuretic peptide: a brief review. Clin Exp Pharmacol Physiol. 2004, 31: 791-794. 10.1111/j.0305-1870.2004.04073.x.CrossRefPubMed
49.
go back to reference Kim HN, Januzzi JL: Natriuretic peptide testing in heart failure. Circulation. 2011, 123: 2015-2019. 10.1161/CIRCULATIONAHA.110.979500.CrossRefPubMed Kim HN, Januzzi JL: Natriuretic peptide testing in heart failure. Circulation. 2011, 123: 2015-2019. 10.1161/CIRCULATIONAHA.110.979500.CrossRefPubMed
50.
go back to reference Witthaut R, Busch C, Fraunberger P, Walli A, Seidel D, Pilz G, Stuttmann R, Speichermann N, Verner L, Werdan K: Plasma atrial natriuretic peptide and brain natriuretic peptide are increased in septic shock: impact of interleukin-6 and sepsis-associated left ventricular dysfunction. Intensive Care Med. 2003, 29: 1696-1702. 10.1007/s00134-003-1910-0.CrossRefPubMed Witthaut R, Busch C, Fraunberger P, Walli A, Seidel D, Pilz G, Stuttmann R, Speichermann N, Verner L, Werdan K: Plasma atrial natriuretic peptide and brain natriuretic peptide are increased in septic shock: impact of interleukin-6 and sepsis-associated left ventricular dysfunction. Intensive Care Med. 2003, 29: 1696-1702. 10.1007/s00134-003-1910-0.CrossRefPubMed
51.
go back to reference Bar SL, Swiggum E, Straatman L, Ignaszewski A: Nonheart failure-associated elevation of amino terminal pro-brain natriuretic peptide in the setting of sepsis. Can J Cardiol. 2006, 22: 263-266. 10.1016/S0828-282X(06)70908-4.CrossRefPubMedPubMedCentral Bar SL, Swiggum E, Straatman L, Ignaszewski A: Nonheart failure-associated elevation of amino terminal pro-brain natriuretic peptide in the setting of sepsis. Can J Cardiol. 2006, 22: 263-266. 10.1016/S0828-282X(06)70908-4.CrossRefPubMedPubMedCentral
52.
go back to reference Shor R, Rozenman Y, Bolshinsky A, Harpaz D, Tilis Y, Matas Z, Fux A, Boaz M, Halabe A: BNP in septic patients without systolic myocardial dysfunction. Eur J Intern Med. 2006, 17: 536-540. 10.1016/j.ejim.2006.07.013.CrossRefPubMed Shor R, Rozenman Y, Bolshinsky A, Harpaz D, Tilis Y, Matas Z, Fux A, Boaz M, Halabe A: BNP in septic patients without systolic myocardial dysfunction. Eur J Intern Med. 2006, 17: 536-540. 10.1016/j.ejim.2006.07.013.CrossRefPubMed
53.
go back to reference Hartemink KJ, Twisk JW, Groeneveld AB: High circulating N-terminal pro-B-type natriuretic peptide is associated with greater systolic cardiac dysfunction and nonresponsiveness to fluids in septic vs nonseptic critically ill patients. J Crit Care. 2011, 26: 108 e1-8 Hartemink KJ, Twisk JW, Groeneveld AB: High circulating N-terminal pro-B-type natriuretic peptide is associated with greater systolic cardiac dysfunction and nonresponsiveness to fluids in septic vs nonseptic critically ill patients. J Crit Care. 2011, 26: 108 e1-8
54.
go back to reference Bar SL, Sayeh N, Ignaszewski AP: Elevated N-terminal pro-brain natriuretic peptide in Mycobacterium tuberculosis pulmonary infection without myocardial dysfunction. Can J Cardiol. 2009, 25: 223-225. 10.1016/S0828-282X(09)70066-2.CrossRefPubMedPubMedCentral Bar SL, Sayeh N, Ignaszewski AP: Elevated N-terminal pro-brain natriuretic peptide in Mycobacterium tuberculosis pulmonary infection without myocardial dysfunction. Can J Cardiol. 2009, 25: 223-225. 10.1016/S0828-282X(09)70066-2.CrossRefPubMedPubMedCentral
55.
go back to reference Antonelli A, Ferri C, Ferrari SM, Marchi S, De Bortoli N, Sansonno D, Chiavacci C, Ferrannini E, Fallahi P: N-terminal pro-brain natriuretic peptide and tumor necrosis factor-alpha both are increased in patients with Hepatitis C. J Interferon Cytokine Res. 2010, 30: 359-363. 10.1089/jir.2009.0059.CrossRefPubMed Antonelli A, Ferri C, Ferrari SM, Marchi S, De Bortoli N, Sansonno D, Chiavacci C, Ferrannini E, Fallahi P: N-terminal pro-brain natriuretic peptide and tumor necrosis factor-alpha both are increased in patients with Hepatitis C. J Interferon Cytokine Res. 2010, 30: 359-363. 10.1089/jir.2009.0059.CrossRefPubMed
56.
go back to reference Schou M, Dalsgaard MK, Clemmesen O, Dawson EA, Yoshiga CC, Nielsen HB, Gustafsson F, Hildebrandt PR, Secher NH: Kidneys extract BNP and NT-proBNP in healthy young men. J Appl Physiol. 2005, 99: 1676-1680. 10.1152/japplphysiol.00641.2005.CrossRefPubMed Schou M, Dalsgaard MK, Clemmesen O, Dawson EA, Yoshiga CC, Nielsen HB, Gustafsson F, Hildebrandt PR, Secher NH: Kidneys extract BNP and NT-proBNP in healthy young men. J Appl Physiol. 2005, 99: 1676-1680. 10.1152/japplphysiol.00641.2005.CrossRefPubMed
57.
go back to reference van Kimmenade RR, Januzzi JL, Bakker JA, Houben AJ, Rennenberg R, Kroon AA, Crijns HJ, van Dieijen-Visser MP, de Leeuw PW, Pinto YM: Renal clearance of B-type natriuretic peptide and amino terminal pro-B-type natriuretic peptide a mechanistic study in hypertensive subjects. J Am Coll Cardiol. 2009, 53: 884-890. 10.1016/j.jacc.2008.11.032.CrossRefPubMed van Kimmenade RR, Januzzi JL, Bakker JA, Houben AJ, Rennenberg R, Kroon AA, Crijns HJ, van Dieijen-Visser MP, de Leeuw PW, Pinto YM: Renal clearance of B-type natriuretic peptide and amino terminal pro-B-type natriuretic peptide a mechanistic study in hypertensive subjects. J Am Coll Cardiol. 2009, 53: 884-890. 10.1016/j.jacc.2008.11.032.CrossRefPubMed
58.
go back to reference Fijalkowska A, Kurzyna M, Torbicki A, Szewczyk G, Florczyk M, Pruszczyk P, Szturmowicz M: Serum N-terminal brain natriuretic peptide as a prognostic parameter in patients with pulmonary hypertension. Chest. 2006, 129: 1313-1321. 10.1378/chest.129.5.1313.CrossRefPubMed Fijalkowska A, Kurzyna M, Torbicki A, Szewczyk G, Florczyk M, Pruszczyk P, Szturmowicz M: Serum N-terminal brain natriuretic peptide as a prognostic parameter in patients with pulmonary hypertension. Chest. 2006, 129: 1313-1321. 10.1378/chest.129.5.1313.CrossRefPubMed
Metadata
Title
Cardiopulmonary involvement in Puumala hantavirus infection
Authors
Johan Rasmuson
Per Lindqvist
Karen Sörensen
Magnus Hedström
Anders Blomberg
Clas Ahlm
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2013
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/1471-2334-13-501

Other articles of this Issue 1/2013

BMC Infectious Diseases 1/2013 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.