Chest ACCP Career Connection
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Guest Access | Sign In via User Name/Password
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via ISI Web of Science (2)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Vincent, B.
Right arrow Articles by Cadranel, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Vincent, B.
Right arrow Articles by Cadranel, J.
(Chest. 2001;120:1078-1084.)
© 2001 American College of Chest Physicians

AIDS-Related Alveolar Hemorrhage*

A Prospective Study of 273 BAL Procedures

Benoît Vincent, MD; Antoine Flahault, MD; Martine Antoine, MD; Marie Wislez, MD; Antoine Parrot, MD; Charles Mayaud, MD and Jacques Cadranel, MD, PhD

* From the Service de Pneumologie et de Réanimation Respiratoire (Drs. Vincent, Wislez, Parrot, Mayaud, and Cadranel), Unité de Biostatistique INSERM U444 (Dr. Flahault), et Service d’Anatomie-Pathologique (Dr. Antoine), Hôpital Tenon, Paris, France.

Correspondence to: Jacques Cadranel, MD, PhD, Service de Pneumologie et de Réanimation Respiratoire, Hôpital Tenon AP-HP, 4 rue de la Chine, 75020 Paris, France; e-mail: jacques.cadranel{at}tnn.ap-hop-paris.fr


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: To evaluate the frequency and diagnostic significance of alveolar hemorrhage (AH) in HIV-infected patients.

Design: A 3-year prospective cohort study.

Setting: A university hospital in Paris, France.

Patients: Two hundred forty-three HIV-infected patients undergoing 273 BAL procedures during the study period.

Methods: AH was assessed by using the Golde score. Data on the patients treated and observed in our institution were collected, as well as on their survival rate 12 months after undergoing BAL. Risk factors for AH were sought by comparing patients with AH (cases) and those without AH (control subjects).

Results: AH frequently occurred but usually was subclinical and cytologically mild. AH did not alter the 12-month survival rate. AH always was associated with at least one specific AIDS-related pulmonary disorder, and the following four independent risk factors were identified in a stepwise forward logistic regression model: pulmonary Kaposi’s sarcoma (KS; odds ratio [OR], 5.3; 95% confidence interval [CI], 1.8 to 16.7; p = 0.003), cytomegalovirus (CMV) pneumonia (OR, 9.8; 95% CI, 1 to 100; p = 0.05), hydrostatic pulmonary edema (OR, 16.4; 95% CI, 1.8 to 142; p = 0.01), and platelet count < 60,000 cells/µL (OR, 5.6; 95% CI, 1.5 to 20; p = 0.009).

Conclusions: AH is frequently diagnosed during BAL in HIV-infected patients. Its presence may point to an underlying cause, such as pulmonary KS, CMV pneumonia, or hydrostatic pulmonary edema, or to triggering factors such as thrombocytopenia.

Key Words: AIDS • alveolar hemorrhage • cytomegalovirus • Kaposi’s sarcoma • pulmonary edema • thrombocytopenia


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
HIV infection predisposes patients to several infectious and noninfectious pulmonary diseases. The spectrum of noninfectious pulmonary diseases includes neoplasms (especially Kaposi’s sarcoma [KS]) and nonspecific disorders such as lymphocytic and nonspecific interstitial pneumonitis, primary pulmonary hypertension, emphysema, and bronchiolitis-organizing pneumonia.1 2

Alveolar hemorrhage (AH), a feature of several immune and idiopathic disorders, corresponds to diffuse bleeding into the acinar portion of the lung. It is routinely diagnosed by macroscopic and cytologic examination of BAL fluid, especially in immunocompromised patients.3 During the past decade, BAL also has taken on a central role in the diagnosis of AIDS-related pulmonary disorders, but to our knowledge, the frequency of AH in this setting has never been studied specifically, except in patients with pulmonary KS4 and cytomegalovirus (CMV) pneumonia.5

The aim of this prospective study of HIV-infected patients was to evaluate the following: (1) the frequency and severity of AH and its effect on survival; and (2) the connection between AH and underlying AIDS-related pulmonary disorders and known AH triggering factors, such as thrombocytopenia, renal failure, and clotting disorders.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Design
Between January 1994 and December 1996, all BAL procedures performed in our institution on HIV-infected patients who had pulmonary symptoms and/or fever were evaluated prospectively for evidence of AH.

The characteristics of the patients, who were treated and observed in our institution, were collected from their medical charts. The group with AH (cases) was compared with the group without AH (control subjects) by using a stepwise forward logistic regression model to identify the risk factors associated with the occurrence of AH. The 12-month survival rate after BAL also was studied according to the presence or absence of AH.

Published cases of AIDS-related AH and associated risk factors were identified by a MEDLINE search performed from 1980 to 1998 with the following key words: (alveolar or pulmonary or lung) and (hemorrhage or hemosiderosis) and HIV or AIDS. Only well-documented reports of AIDS-related AH were analyzed.

Fiberoptic Bronchoscopy, BAL Analysis, and AH Definition
Fiberoptic bronchoscopy and BAL were performed as previously described.6 BAL was conducted, after macroscopic examination for KS lesions and bronchial suppuration, in the middle lobe or in the most affected lung segment seen on the chest radiograph, using four 50-mL aliquots of warm sterile isotonic saline solution. The macroscopic aspect of recovered BAL fluid was noted, with special attention to signs of hemorrhage. BAL smears were stained for differential cell counts, the identification of pathogens (ie, mycobacteria, viruses [CMV and herpes viruses], fungi, and parasites), and the detection of hemosiderin-containing alveolar macrophages. Briefly, 200 macrophages were examined after staining by Perl’s Prussian blue method. Each cell was ranked for hemosiderin content by using the following scale: 0, no color; 1, faint blue in one portion of the cytoplasm; 2, deep blue in a minor portion of the cell; 3, deep blue in most areas of the cytoplasm; and 4, deep blue throughout the cell. The total score for an average of 200 cells was divided by two to obtain the Golde score (GS). As reported by Kahn et al,3 AH was defined by a GS >= 20 and was considered mild and severe when the GS was 20 to 100 and > 100, respectively. The percentage of Prussian blue-stained siderophages among the alveolar macrophage population was noted. Aliquots of BAL fluid also were cultured for bacteria, mycobacteria, fungi, and viruses (ie, CMV and herpes viruses).

Bronchial, transbronchial, and protected brush specimens, bacteriologic assessment of sputum, blood culture, and pleural fluid, and transparietal biopsies were performed when indicated by clinical and radiologic findings.

Diagnostic Criteria for Pulmonary Disorders
The diagnosis of Pneumocystis carinii, Toxoplasma gondii, Cryptococcus neoformans, Mycobacterium tuberculosis, or non-tuberculosis mycobacterial pneumonia was established by the presence of these organisms in BAL fluid or histologic samples, as identified by specific staining, immunofluorescence, or culture. The diagnosis of invasive Aspergillosis pneumonia was based on the presence of the organism in BAL fluid or bronchial aspirates that was associated with histologic evidence of invasive infection.7 Bacterial pneumonia was defined by the presence of >= 104 colony-forming units/mL in BAL fluid or >= 103 colony-forming units/mL on the protected brush specimen, or by positive results of pleural fluid cultures or blood cultures in patients with focal pulmonary infiltrates.8 Diagnostic criteria for CMV pneumonia were the following: (1) the presence of viral inclusions in BAL or transbronchial biopsy specimens; (2) the absence of other demonstrable pathogens; and (3) a marked improvement after specific treatment.9 Pulmonary KS was diagnosed on tissue specimens or when the operator described compatible endobronchial lesions associated with histologically proven skin lesions.10 Pulmonary lymphoma was established by the histologic analysis of tissue specimens. The diagnosis of lymphoid interstitial pneumonitis was confirmed after 3 months of follow-up of patients with intense CD8 lymphocytic alveolitis seen in BAL fluid specimens and a compatible histology in transbronchial biopsy specimens.11 The diagnosis of primary pulmonary hypertension and congestive heart failure was based on echocardiography examination and/or invasive hemodynamic evaluation by right-sided heart catheterization when indicated. Hydrostatic pulmonary edema was diagnosed in the presence of the following: (1) a diffuse alveolar and interstitial pattern on chest radiographs; (2) renal or cardiac failure; and (3) rapid and complete resolution of respiratory symptoms after fluid withdrawal by diuretic administration or hemodialysis. Finally, a diagnosis of nonpulmonary disease was considered when the pulmonary workup showed no lung disorder in patients with fever.

Data Collection and Follow-up
The following epidemiologic data were recorded at the time of BAL: sex; age; race; HIV transmission category; CD4+ lymphocyte count; prior AIDS-defining conditions, according to the Centers for Disease Control and Prevention classification12 ; previous treatments; and P carinii pneumonia (PCP) prophylaxis. Particular attention was paid to the presence of mucocutaneous KS. The usual features of AH13 (ie, hemoptysis, anemia [hemoglobin concentration], hypoxemia [PaO2/fraction of inspired oxygen ratio], and new pulmonary infiltrates on the chest radiographs) also were recorded. In addition, chest radiographs were reviewed and classified in the following manner: (1) normal; (2) alveolointerstitial pattern; and (3) nodular pattern. Finally, the following factors that have been reported classically to trigger or aggravate AH were noted: smoking history (pack-years); thrombocytopenia (ie, platelet count, < 60,000 cells/µL); clotting abnormalities (ie, patient-to-control subject ratio of the activated partial thromboplastin time [APTT] of > 1.5 and thromboplastin time of < 60%), renal failure (ie, creatinine concentration of > 130 µmol/L), congestive heart disease, and mechanical ventilation.

Statistical Analysis
Only the results of first BAL procedures performed during the study period were included in the analysis to ensure the independence of observations. Results were expressed as the mean ± SD. Univariate comparisons between cases (patients with AH) and controls (control subjects without AH) were performed with the Wald test by using nonconditional logistic regression for computing odds ratios (ORs) with 95% confidence intervals (95% CIs). A value of 0.5 was used as for 0 in any cell for computing the 95% CI. Then, factors associated with AH (p < 0.1) in univariate analysis were entered into a stepwise forward logistic regression model to determine which of them were significantly and independently associated with the occurrence of AH (p < 0.05; two-sided test). Finally, the survival rate 12 months after the BAL procedure was compared between patients and control subjects by using a log rank test. Data were processed with computer software (StatView and Survival Tools F-4.11; Abacus Concepts; Berkeley, CA).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Frequency, Severity, and Clinical Features of HIV-Related AH
Two hundred seventy-three consecutive BAL procedures were performed in 243 patients during the 3-year study period. Eighty-eight samples (32%) revealed AH (mean GS, 65; GS range, 20 to 221). AH was severe (GS > 100) in 11 of the 88 patients (13%). As expected, there was a good correlation between the GS and the percentage of siderophages recovered by BAL in cases of AH (R2 = 0.9; p < 0.01; data not shown). Total and differential cell counts did not differ between BAL fluid from patients with AH and those without AH (data not shown).

Data corresponding to the first BAL procedures undergone by the 203 patients treated and followed in our institution then were analyzed. In this group, the frequency and severity of AH were not different from those of the total sample (n = 273). AH was detected in 73 of these 203 samples (36%) (mean GS, 54.5; range, 20 to 201) and was severe in six patients (8%). The 12-month cumulative patient survival rates were 76% and 80%, respectively, in the patients and control subjects (not significant), indicating that AH did not affect the survival of these patients.

Only one patient (1.4%) with AH had hemoptysis. The mean hemoglobin and PaO2/fraction of inspired oxygen ratio values were 10.5 ± 2.5 g/dL and 316.3 ± 73.2, respectively, and did not differ between the patients and control subjects. Chest radiograph findings were never normal in patients with AH and were normal in 27 of the 130 patients (21%) without AH. Eight patients with AH (10.4%) and no patients without AH had grossly bloody BAL fluid.

Risk Factors for HIV-Related AH in Univariate Analysis
Characteristics of HIV Infection and Potential Triggering Factors: As shown in Table 1 , AH was associated with several factors. Compared with control subjects, patients were significantly more likely to be male, to belong to the homosexual HIV transmission category, and to have mucocutaneous KS. Immunodeficiency was also more severe in the patients, as shown by the higher frequency of prior AIDS-defining conditions, antiretroviral therapy, and PCP prophylaxis, and by a lower mean CD4+ cell count. No differences in age or race were found. The factors reported to trigger AH are analyzed in Table 2 . Thrombocytopenia, a patient-to-control subject APTT ratio exceeding 1.5, and renal failure were significantly more frequent in patients than in control subjects. Conversely, prior congestive heart failure, smoking history, and mechanical ventilation were not significantly associated with AH.


View this table:
[in this window]
[in a new window]

  		Table 1.. Comparison Between Patients (With AH) and Control Subjects (Without AH) for Main Characteristics of Patients and HIV Infection (Univariate Analysis)*

 

View this table:
[in this window]
[in a new window]

  		Table 2.. Comparison Between Patients (With AH) and Control Subjects (Without AH) for Parameters That Have Already Been Associated With AH in Literature (Univariate Analysis)*

 
Underlying HIV-Related Pulmonary Disorders: At least one associated pulmonary disorder was found in each patient with AH. Conversely, AH was never found in the 17 HIV-infected control subjects without pulmonary symptoms and with normal chest radiograph findings. As expected, PCP and bacterial pneumonia were the most frequent pulmonary disorders in both groups. More interestingly, pulmonary KS, CMV pneumonia, and hydrostatic pulmonary edema were significantly more frequent in patients than in control subjects. Hydrostatic pulmonary edema resulted from HIV-related cardiomyopathy in two patients and from severe renal failure in six patients. Patients with renal failure also had the following very homogeneous clinical features: all were black Africans; and all had a nephrotic syndrome attributed, by renal biopsy specimen, to idiopathic focal and segmental glomerulosclerosis and hyalinosis. Figure 1 shows the frequency of AH according to intercurrent pulmonary conditions. AH was present in most patients with pulmonary KS (75%), CMV pneumonia (83%), and hydrostatic pulmonary edema (100%). The underlying pulmonary diseases in the eight patients with grossly bloody BAL fluid were pulmonary KS (n = 4), CMV pneumonia (n = 2), and PCP (n = 2). The two patients with PCP also had thrombocytopenia (< 60,000 cells/µL).



View larger version (25K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1.. In parentheses are the numbers of diagnoses of pulmonary disorders. Note that the total number of diagnoses is greater than the total number of patients because 18 patients each had two diagnoses. Other diagnoses are detailed in Table 4 . The bars represent the percentage of BAL specimens with AH. MB = tuberculosis and nontuberculosis Mycobacterium; IA = invasive aspergillosis.

 
Risk Factors for HIV-Related AH in Multivariate Analysis
The following four independent risk factors for AH were identified by multivariate analysis (Table 4) : pulmonary KS; hydrostatic pulmonary edema; CMV pneumonia; and thrombocytopenia. Conversely, the absence of underlying pulmonary disease was negatively associated with AH.


View this table:
[in this window]
[in a new window]

  		Table 4.. Stepwise Logistic Nonconditional Multivariate Regression Analysis for AH-Associated Risk Factors

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
This analysis of 273 consecutive BAL specimens from HIV-infected patients showed the following: (1) that AH was present in about one third of patients but was usually clinically occult and cytologically mild; (2) AH was clearly associated with specific underlying AIDS-associated pulmonary disorders, namely, pulmonary KS, CMV pneumonia, and hydrostatic pulmonary edema; and (3) AH was favored by triggering factors, especially thrombocytopenia. The high frequency of AH in this series is in keeping with that in a previous study.14

As HIV infection indirectly causes nonspecific lesions of the pulmonary artery,2 it might also lead to inflammatory lesions of the alveolar capillaries similar to those described in some immunologic disorders and referred to as capillaritis.15 However, although HIV-related vasculitis has been described,16 to our knowledge, capillaritis has never been reported in the lungs of patients with AIDS. Several findings in the present study suggest that HIV-related pulmonary vasculitis was not responsible for AH. First, AH was never found in the 17 subjects who had no underlying pulmonary disorders. Second, all the patients with AH had at least one AIDS-related pulmonary disorder. Patients with AH were more profoundly immunodeficient (Table 1) , raising the possibility of an indirect contribution of HIV to the onset of AH. Indeed, HIV disease progression is associated with an increase in alveolar permeability17 and a rising incidence of AH risk factors, such as pulmonary KS,4 CMV pneumonia,5 and clotting disorders.18

Even if AH should be observed in all patients with AIDS-related pulmonary disorders, only three of the latter (ie, pulmonary KS [OR, 5.3], CMV pneumonia [OR, 10], and hydrostatic pulmonary edema [OR, 16.4]) were identified as independent risk factors for AH in a stepwise forward logistic regression model (Table 3 ). Interestingly, these disorders are also known to interact with the vascular or blood flow pulmonary system through pulmonary vascular angiogenesis, capillary endothelial lesions, and a rise in capillary hydrostatic pressure, respectively. This larger series confirms the high rate of AH (75%) that we observed in a previous study of patients with pulmonary KS.4 The apparent conflict with the results of another study19 might simply reflect differences in the status of the patients studied, as bleeding complications are mainly reported in those with advanced pulmonary diseases.10 The association between AH and pulmonary KS is clearly explained by pathologic studies. KS lesions are characterized by the proliferation of endothelial and spindle cells and by the extravasation of erythrocytes into the alveolar spaces.20 Interestingly, human herpesvirus type 8, which is consistently detected in KS lesions, can promote both angiogenesis and vessel permeability by activating its encoded G-protein-coupled receptor.21 Moreover, spindle cells produce several mediators (interleukin-1, interleukin-6, fibroblast growth factor, and vascular endothelial growth factor) that influence endothelial cell proliferation and permeability.10 22


View this table:
[in this window]
[in a new window]

  		Table 3.. Comparison Between Patients (With AH) and Control Subjects (Without AH) for Diagnoses of Pulmonary Disorders (Univariate Analysis)*

 
Although CMV is frequently recovered from the lung, CMV pneumonia is rare in HIV-infected patients.23 We have previously demonstrated that AH can be associated with diffuse thrombotic microangiopathy related to specific CMV infection of lung capillary endothelial cells.5 In the present study, all the patients with CMV-associated AH had similar clinical features, except for a patient who also had symptomatic pulmonary KS. Thus, the detection of both AH and CMV in BAL fluid would point to CMV-induced AH, especially in a patient with thrombotic microangiopathy. Pulmonary invasive aspergillosis is another angioinvasive infection leading to pulmonary complications in HIV-infected patients.7 Although statistically meaningless, it is noteworthy that both patients with invasive pulmonary aspergillosis in this series had AH.

An increase in pulmonary circulation hydrostatic pressure is a frequent complication of severe renal impairment and left heart failure, sometimes creating the clinical and radiologic features of pulmonary edema. Studies of animal models have demonstrated the relationship between the increase in hydrostatic pressure in the pulmonary circulation and the occurrence of AH,24 showing "capillary stress failure" characterized by structural alteration of capillary basal membrane collagen IV.25 In this study, AH was present in all the BAL fluid samples obtained from patients with hydrostatic pulmonary edema. Edema was associated with HIV-related dilated cardiomyopathy (n = 3) and severe renal failure (n = 5) due to idiopathic focal and segmental glomerulosclerosis and hyalinosis. It is noteworthy that vasculitis, and especially pulmonary capillaritis, has never been reported in these so-called HIV-associated glomerular diseases.26

It is interesting that AH can be associated with all AIDS-related pulmonary disorders, even those in which the pulmonary vessels are never involved (ie, PCP and bacterial pneumonia). In a previous series involving uninfected HIV-immunocompromised patients, AH triggering factors included smoking,14 15 renal failure,14 15 and, especially, all causes of clotting disorders (ie, disseminated intravascular coagulation, profound thrombocytopenia, and treatment with anticoagulants, antiplatelet agents, and fibrinolytics).27 28 Except for smoking, the present study confirms the role of these factors in patients with AIDS-related AH (Table 2) . After multivariate analysis, only thrombocytopenia was an independent risk factor (OR, 5.6) (Table 4) .

In conclusion, AH is a frequent finding in BAL specimens from HIV-infected patients with pulmonary symptoms and/or fever. However, the AH is usually occult and mild, and does not affect survival.


   Acknowledgements
 
We thank Isabelle Herry, Gilles Mangiapan, Jean-Marc Naccache, Fayçal Saïdi, and Kader Souidi for patient care and Jean-François Bernaudin for helpful criticism.


   Footnotes
 
Abbreviations: AH = alveolar hemorrhage; APTT = activated partial thromboplastin time; CI = confidence interval; CMV = cytomegalovirus; GS = Golde score; KS = Kaposi’s sarcoma; OR = odds ratio; PCP = Pneumocystis carinii pneumonia

Received for publication August 30, 2000. Accepted for publication April 25, 2001.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. White, DA, Matthay, RA (1989) Noninfectious pulmonary complications of infection with the human immunodeficiency virus. Am Rev Respir Dis 140,1763-1787[ISI][Medline]
  2. Morse, JH, Barst, RJ, Irescu, S, et al (1996) Primary pulmonary hypertension in HIV infection: an outcome determined by particular HLA class II alleles. Am J Respir Crit Care 153,1299-1301[Abstract]
  3. Kahn, FW, Jones, JM, England, DM (1987) Diagnosis of pulmonary hemorrhage in the immunocompromised host. Am Rev Respir Dis 136,155-160[ISI][Medline]
  4. Fouret, PJ, Touboul, J-L, Mayaud, CM, et al (1987) Pulmonary Kaposi’s sarcoma in patients with acquired immune deficiency syndrome: a clinicopathological study. Thorax 42,262-268[Abstract]
  5. Herry, I, Cadranel, J, Antoine, M, et al (1996) Cytomegalovirus-induced alveolar hemorrage in patients with AIDS: a new clinical entity? Clin Infect Dis 22,616-620[Medline]
  6. Golden, JA, Hollander, H, Stulbarg, MS, et al (1986) Bronchoalveolar lavage as the exclusive diagnosis modality for Pneumocystis carinii pneumonia: a prospective study among patients with acquired immunodeficiency syndrome. Chest 90,18-22[Abstract/Free Full Text]
  7. Lortholary, O, Meyohas, M-C, Dupont, B, et al (1993) Invasive aspergillosis in patients with acquired immunodeficiency syndrome: report of 33 cases. Am J Med 95,177-187[CrossRef][ISI][Medline]
  8. Pham, L, Brun-Buisson, C, Legrand, P, et al (1991) Diagnosis of nosocomial pneumonia in mechanically ventilated patients. Am Rev Respir Dis 143,1055-1061[ISI][Medline]
  9. Masur, H, Lane, C, Palestine, A, et al (1986) Effect of 1,3-dihydroxy-2-propoxymethyl guanine on serious cytomegalovirus disease in eight immunosuppressed homosexual men. Ann Intern Med 1104,41-44
  10. Cadranel, J, Mayaud, C (1995) Intra thoracic Kaposi’s sarcoma in patients with AIDS. Thorax 50,407-414[ISI][Medline]
  11. Suffredini, AF, Ognibene, FP, Lack, EE, et al (1987) Non specific interstitial pneumonitis: a common cause of pulmonary disease in the acquired immunodeficiency syndrome. Ann Intern Med 107,7-13
  12. . Centers for Diseases Control and Prevention (1992) 15 revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults MMWR Morb Mortal Wkly Rep 41,1-19
  13. Leatherman, JW, Davies, SF, Hoidal, JR (1984) Alveolar hemorrhage syndromes: diffuse microvascular lung hemorrhage in immune and idiopathic disorders Medicine (Baltimore) 63,343-361[Medline]
  14. De Lassence, A, Fleury-Feith, J, Escudier, E, et al (1995) Alveolar hemorrhage: diagnostic criteria and results in 194 immunocompromised hosts. Am J Respir Crit Care Med 151,157-163[Abstract]
  15. Green, RJ, Ruoss, SJ, Kraft, SA, et al (1996) Pulmonary capillaritis and alveolar hemorrhage. Chest 110,1305-1316[Abstract/Free Full Text]
  16. Guillevin, L, Lhote, F, Gerhardi, R (1997) The spectrum and treatment of virus associated-vasculitides. Curr Opin Rheumatol 9,31-36[CrossRef][Medline]
  17. Mitchell, DM, Fleming, J, Pinching, AJ, et al (1992) Pulmonary function in human immunodeficiency virus infection: a prospective 18-month study of serial lung function in 474 patients. Am Rev Respir Dis 146,745-751[ISI][Medline]
  18. Stricker, RB (1991) Hemostatic abnormalities in HIV disease. Hematol Oncol Clin North Am 5,249-265[ISI][Medline]
  19. Hughes-Davies, L, Cocjan, G, Spittle, MF, et al (1992) Occult alveolar hemorrhage in bronchopulmonary Kaposi’s sarcoma. Clin Pathol 45,536-537
  20. Purdy, LJ, Colby, TV, Yousem, SA, et al (1986) Pulmonary Kaposi’s sarcoma: premortem histologic diagnosis. Am J Surg Pathol 10,301-311[CrossRef][ISI][Medline]
  21. Bais, C, Santomasso, B, Cosso, O, et al (1998) G-protein-coupled receptor of Kaposi’s sarcoma-associated herpes virus is a viral oncogene and angiogenesis activator. Nature 391,86-89[CrossRef][Medline]
  22. Samaniego, F, Markham, PD, Gendelman, R, et al (1998) Vascular endothelial growth factor and basic fibroblast growth factor present in Kaposi’s sarcoma (KS) are induced by inflammatory cytokines and synergize to promote vascular permeability and KS lesion development. Am J Pathol 152,1433-1443[Abstract]
  23. Millar, A, Patou, G, Miller, R, et al (1990) Cytomegalovirus in the lungs of patients with AIDS: respiratory pathogen or passenger? Am Rev Respir Dis 141,1474-1477[ISI][Medline]
  24. Meyer, TS, Fedde, MR, Gaughan, EM, et al (1998) Quantification of exercise-induced pulmonary hemorrhage with bronchoalveolar lavage. Equine Vet J 30,284-288[Medline]
  25. West, JB, Mathieu-Costello, O (1992) Stress failure of pulmonary capillaries: role in lung and heart diseases. Lancet 340,762-767[CrossRef][ISI][Medline]
  26. Stone, HD, Appel, RG (1994) Human immunodeficiency virus-associated nephropathy: current concepts. Am J Med Sci 307,212-217[Medline]
  27. Drew, WL, Finley, TN, Golde, DW (1977) Diagnostic lavage and occult pulmonary hemorrhage in thombocytopenic immunocompromised patients. Am Rev Respir Dis 116,215-219[Medline]
  28. Santalo, M, Domingo, P, Fontcuberta, J, et al (1986) Diffuse pulmonary hemorrhage associated with anticoagulant therapy. Eur J Respir Dis 69,124-129




This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via ISI Web of Science (2)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Vincent, B.
Right arrow Articles by Cadranel, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Vincent, B.
Right arrow Articles by Cadranel, J.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS