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Saudi J Kidney Dis Transpl 2013;24(4):743-750
© 2013 Saudi Center for Organ Transplantation
Original Article
Alveolar Hemorrhage and Kidney Disease: Characteristics and Therapy
Lilia Ben Fatma1
, Zohra El Ati1
, Rais Lamia1
, Dorra Ben Aich1
, Krid Madiha1
, Smaoui Wided1
,
Hedi Ben Maiz2
, Somaya Beji1
, Zouaghi Karim1
, Fatma Ben Moussa1
1
Department of Nephrology, La Rabta Hospital, 2
Laboratory of Renal Pathology, LR001SP,
Charles Nicole Hospital, Tunis, Tunisia
ABSTRACT. Anti-neutrophil cytoplasmic antibody-associated vasculitis and Goodpasture’s glo-
merular basement membrane disease are the most common causes of diffuse alveolar hemorrhage,
a life-threatening disease. Systemic lupus erythematosus and the antiphospholipid syndrome are
also causes of alveolar hemorrhage. We retrospectively reviewed 15 cases of diffuse alveolar
hemorrhage (DAH) associated with renal diseases. Diagnosis of DAH was based on the presence
of bloody bronchoalveolar lavage fluid. There were three men and 12 women, with a mean age of
50.5 years (extremes: 24–74 years). Proteinuria and hematuria were observed, respectively, in 15
and 14 cases. Six patients revealed arterial hypertension. Crescentic glomerulonephritis was diag-
nosed with kidney biopsies in ten cases. The etiology of renal disease was microscopic poly-
angiitis (MPA) in seven cases, Wegener disease in four cases, systemic lupus erythematous in one
case, cryoglobulinemia in one case, myeloma in one case and propyl-thiouracil-induced MPA in
one case. Hemoptysis occurred in 14 cases. The mean serum level of hemoglobin was 7.1 g/dL
(5.1–10 g/dL). The mean serum creatinine concentration was 7.07 mg/dL (2.4–13.7 mg/dL). Gas
exchange was severely compromised, with an oxygenation index <80 mmHg in 14 patients and
<60 mmHg in seven patients. Bronchoalveolar lavage was performed in 11 cases, and had posi-
tive findings for hemorrhage in all. Methylprednisolone pulses and cyclophosphamide were used
in 14 patients. Plasmapheresis was performed in three cases. One patient received cycles of
Dexamethasome–Melphalan. Three patients died as a result of DAH. The mortality rate in our
study was 20%.
Introduction
Diffuse alveolar hemorrhage (DAH) is a cli-
nical syndrome that can be life-threatening if
Correspondence to:
Dr. Lilia Ben Fatma,
Department of Nephrology, La Rabta
Hospital, Jabbari, 2007, Tunis, Tunisia
E-mail: lilia.benfatma@rns.tn
if not diagnosed and treated in time.1
In most
cases, it occurs largely as a result of small-
vessel vasculitis of the lungs. Antineutrophil
cytoplasmic antibodies (ANCA) and Good-
pasture’s diseases are the most common causes
of DAH, while other pathologies including sys-
temic lupus erythematosus, antiphospholipid
syndrome and multiple myeloma, are rare cau-
ses of this syndrome. Diagnosis of DAH is
based on a combination of signs, symptoms,
Saudi Journal
of Kidney Diseases
and Transplantation
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biological tests and histology. Hemoptysis, de-
creased hemoglobin levels and/or hematocrit,
diffusion capacity for carbon monoxide
(DLCO) of more than 30% and bronchoalveo-
lar lavage (BAL)-positive findings of hemosi-
derin are relatively common features in DAH.2
The aim of our study was to collect cases of
patients with DAH and kidney disease, to des-
cribe their clinical, radiological and histological
characteristics and approach for treatment.
Patients and Methods
A group of 15 patients (12 females, three
males) with DAH and renal disease were re-
trospectively identified from September 2007
to September 2010 in the Nephrology Depart-
ment in La Rabta Hospital in Tunis, Tunisia.
Their clinical presentations and laboratory, ra-
diographic and pathologic findings and re-
sponse to therapy were reviewed.
Characteristics of the patients were recorded
from the medical files and the following items
were analyzed: Demographic characteristics,
pulmonary and renal tract involvement, etio-
logies of the DAH, response to therapy and
outcome of patients.
Results
There were 12 women and three men, with a
mean age of 50.5 years (extreme: 24–74 years).
Two patients had pulmonary fibrosis and one
patient had diabetes. Proteinuria and hematuria
were observed, respectively, in 15 and 14
cases. Six patients revealed arterial hyperten-
sion. Crescentic glomerulonephritis was diag-
nosed in ten cases. The mean serum creatinine
concentration was 7.07 mg/dL (range from 2.4
to 13.7 mg/dL), requiring hemodialysis in ten
cases. Thirteen patients had a kidney biopsy.
Pauci-immune extracapillary glomeruloneph-
ritis with necrosis was diagnosed in ten cases.
Only in our patient no. 7, kidney biopsy diag-
nosed pauci-immune extracapillary glomerulo-
nephritis associated with IgG linear deposit.
Hemoptysis was present in 14 cases. The me-
dian serum level of hemoglobin was 7.1 g/dL
(5.1–10 g/dL). Gas exchange was severely
compromised, with an oxygenation index <80
mmHg in ten cases and <60 mmHg in seven
cases. Thirteen patients presented with alveo-
lar hemorrhage at disease onset. The two re-
maining patients revealed signs of DAH few
days after starting the treatment.
BAL was performed in 11 cases. Evidence of
microscopic alveolar hemorrhage was con-
firmed in BAL, defined as more than 20%
siderophages and Gold score superior to 100;
seven patients had more than 20% sidero-
phages and 11 patients had Gold score supe-
rior to 100. The DLCO performed in only one
case was positive. The remaining 14 patients
did not have DLCO testing because they were
too ill to cooperate. Our patients did not un-
dergo transbronchial biopsies and hence no
pulmonary histological reports were available.
Wegener’s disease was diagnosed in four ca-
ses because of the presence of a pauci-immune
extra-capillary glomerulonephritis with peri-
glomerular granulomatous reaction; anti-PR3
type C-ANCA was found in all these cases,
retro-orbital granulomatous mass and pansinu-
sitis was seen in two cases and epistaxis with
pulmonary nodules was seen in one case. The
characteristics of our patients are summarized
in Tables 1 and 2 and Figures 1 and 2.
All the patients received intravenous (i.v.)
high-dose steroids. In addition, 14 patients re-
ceived an i.v. pulse of cyclophosphamide. Two
patients received ten cycles of plasmapheresis
and one patient received seven cycles. In our
study, the mean period of follow-up was 9.5
months (1–20 months). The renal function im-
proved in only seven cases and the rest re-
quired chronic hemodialysis. Pulmonary in-
volvement improved in 12 cases, and without
relapse in 11 cases. Only one relapse of DAH
was observed in patient no. 7 after 12 months
of follow-up. This patient was maintained on
chronic hemodialysis and required immuno-
suppression withdrawal because of the occur-
rence of a Kaposi sarcoma. Three patients died
as a result of severe hypoxemia related to
DAH, with a mortality rate of 20%.
Treatment and outcome of the patients are
summarized in Table 3.
744 Ben Fatma L, El Ati Z, Lamia R, et al

Table 1. Patients’ characteristics of diffuse alveolar hemorrhage syndrome.
Patient/gender/age
(years)
Hemoptysis
Hb
(g/dL)
O2i Chest Rx CCT BAL
1//F/27 Yes 5.5 35 Normal -
2/F/24 Yes 10 51 Interstitial syndrome FG -
3/F/58 Yes 6.4 63 Interstitial syndrome Interstitial syndrome pneumonia
Cellularity: 120,000
GS: 175
4/F/29 Yes 5.8 73 Normal -
GS: 178
5/F/72 Yes 7.3 78
Alveolar opacities
(Figure 1)
FG + pleural thickening
GS: 130
6/M/47 Yes 7.3 53
Pleural extrusion +
Alveolar opacities
FG
GS: 123
7/F/74 Yes 5.8 60 Alveolar opacities -
GS: 180
8/F/51 No 8.3 63 Normal -
GS: 280
9/F/54 Yes 5.6 53 Normal -
Cellularity:350,000
GS: 210
10/M/47 Yes 9.5 56 Alveolar opacities -
Cellularity:220,000
GS: 115
11/F/67 Yes 7.3 62 Alveolar opacities FG
Cellularity:1255,000
GS: 150
12/F/45 Yes 8.5 82 Alveolar opacities FG -
13/F/65 Yes 8.8 65 Alveolar opacities FG + Pulmonary fibrosis -
14/F/44 Yes 5.3 47 Normal -
GS: 236
15/M/57 Yes 5.1 47 Alveolar opacities FG (Figure 2)
GS: 234
M: Male, F: Female, Hb: Hemoglobin serum level, O2i: Oxygenation index, Chest Rx: Chest radiographs, CCT: Chest computed tomography, FG:
Frosted glass aspect, BAL: Bronchoalveolar lavage; GS: Gold score.
Alveolarhemorrhageandkidneydisease745
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Table 2. Study patients’ characteristics of kidney involvement.
Patient/gender/
age (years)
H
Urine
Proteinuria HT
Serum
creatinine
(mg/dL)
ANCA Kidney biopsy Renal disease
1/F/27 Yes Yes Yes 10.9 P-ANCA Pauci-immune ECGN + Necrosis MPA
2/F/24 Yes Yes No 25 Negative Diffuse proliferative GN class IV SLE
3/F/58 Yes Yes Yes 7.5 C-ANCA Pauci-immune ECGN + Necrosis WD
4/F/29 Yes Yes No 2.4 C-ANCA Pauci-immune ECGN + Necrosis WD
6/M/47 Yes Yes No 10.6 C-ANCA ECGN WD
7/F/74 Yes Yes No 7.7
PANCA +
MBG ab
Pauci-immune ECGN + Necrosis +
Linear depots of IgG
MPA + GP
9/F/54 Yes Yes Yes 2.8 Negative
Membranous proliferative GN +
Intracapillary thrombi
Cryo
10/M/47 Yes Yes No 4 P-ANCA Pauci-immune ECGN + Necrosis MPA
11/F/67 Yes No Yes 2.5 Negative - Myeloma
12/F/45 Yes Yes No 9.1 C-ANCA Pauci-immune ECGN + Necrosis WD
13/F/65 Yes Yes No 9.5 P-ANCA Pauci-immune ECGN + Necrosis MPA
14/F/44 Yes Yes No 8.9 P-ANCA -
Propyl-thiouracil-
induced MPA
15/M/57 Yes Yes No 13.7 P-ANCA Pauci-immune ECGN + Necrosis MPA
ANCA: Antineutrophil cytoplasmic antibody, P-ANCA: Perinuclear antineutrophil cytoplasmic antibody, C-ANCA: Cytoplasmic antineutrophil
cytoplasmic antibody, MBG ab: Anti-glomerular basement membrane, ECGN: Extra-capillary glomerulonephritis, GN: glomerulonephritis, MPA:
Microscopic polyangiitis, WD: Wegener disease, GP: Goodpasture’s syndrome, SLE: Systemic lupus erythematous, Cryo: Cryoglobulinemia, H urine:
Hematuria, HT: Hypertension
746BenFatmaL,ElAtiZ,LamiaR,etal

Figure 1. Chest X-ray of patient no. 5, diffuse
bilateral alveolar opacities.
Discussion
The pulmonary–renal syndrome is a com-
bination of DAH and glomerulonephritis.3
Our
study described the clinical, radiographical
characteristics, etiologies and outcome of a
group of 15 patients with pulmonary–renal
syndrome.
In earlier studies, the hemoptysis frequency
ranged from 25% to 100%.4
Definite diagnosis
is based on the BAL findings. New infiltrates
on chest X-rays accompanied by abrupt drop
in Hb appear to be a more sensitive sign of
DAH. However, radiographic findings range
from diffuse alveolar infiltrates to lobar infil-
trates, and are not specific.5,6
The classic sign
of a raised DLCO on pulmonary function tests
is useful and suggestive of DAH.7,8
However,
this test has limited value in the acutely ill
patients. In our study, the DLCO contributed
to the diagnosis in only one case, and the rest
were too ill to cooperate with this test. Evi-
dence of microscopic alveolar hemorrhage was
observed in all patients who underwent bron-
choscopy.
In our study, DAH was clearly definite in
only 11 cases who underwent BAL. In the other
four cases, diagnosis of DAH was probable
because of clinical, biologic and radiologic
features. The many different forms of DAH can
Figure 2. Chest computed tomography of patient
no. 15, extensive and bilateral lesions.
be classified into three large groups: Pauci-
immune diseases, syndromes caused by immune
deposits and a large miscellaneous group that
includes drug reactions, infections and idio-
pathic diseases.9
Most studies on DAH emphasize that it is
immunologically mediated and associated with
MPA or rapidly progressive glomerulonephritis
in patients with anti-MPO type P-ANCA;10,11
DAH occurs at a rate of 12–29% in MPA pa-
tients.11,12
In our study, DAH was associated
with MPA in seven (49%) patients. Four more
cases were due to Wegener’s disease.13-15
Typical pulmonary lesions of DAH on chest
X-ray include bilateral, reticular or nodular opa-
cities. Chest computed tomography is required
to accurately characterize the pattern and ex-
tent of pulmonary disease.16,17
In our study, the
chest computed tomography was performed in
only eight cases and showed extensive bila-
teral lesions in all cases. Typical lesions such
as frosted glass were observed in seven cases.
DAH is a rare complication of systemic lupus
erythematous, with a reported frequency ranging
from 1% to 5.4% of lupus cohorts.18-21
How-
ever, it is often serious, requiring early, inten-
sive therapy and is associated with high mor-
tality, ranging from 23% to 92%.22
Propyl-thiouracil-induced P-ANCA vasculitis
may be responsible for DAH in less than 1%
Alveolar hemorrhage and kidney disease 747

Table 3. Treatment and outcome of the study patients.
Patients Treatment
Flow-up
(months)
Outcome Death Cause of death
1
MP 1 g/day × 3 days and P 1 mg/kg/day
CP (1 g/1.73 m2
CS adapted to RF): 1 pulse
1
RFi not improved
SRI
Yes
SRI
DAH
2
MP 1 g/day × 3 days and P 1 mg/kg/day
CP (1 g/1.73 m2
CS adapted to RF): 3 pulses
2
RFi not improved
SRI
Yes
SRI
DAH
3
MP 1 g/day × 3 days and P 1 mg/kg/day × 2 months then withdrawal 5 mg/15 days
CP (1 g/1.73 m2
CS adapted to RF): 4 pulses (1/15 days)
4
Improvement of RF
SRI
Yes
SRI
Pulmonary fibrosis
4
CP (1 g/1.73 m2
CS adapted to RF): 6 pulses (1/15 days) then AZA
12
Improvement of RF
Improvement of AH
No
5
CP (1 g/1.73 m2
20
ESRF
Improvement of AH
No
6
CP (1 g/1.73 m2
CS adapted to RF): 7 pulses (1/15 days) then AZ
PEx: 10 cycles
20
ESRF
Improvement of AH No
7
CP (1 g/1.73 m2
13
Improvement of RF
Improvement of AH
No
8
CP (1 g/1.73 m2
10
ESRF
Improvement of AH
No
9
CP (1 g/1.73 m2
9
Improvement of RF
Improvement of AH
No
10
CP (1 g/1.73 m2
14
ESRF
Improvement of AH
No
11 Melphalan + Dexamethasome (6 cycles) 6
Improvement of RF
Hemoptysis
No
12
CP (1 g/1.73 m2
7
ESRF
Improvement of AH
No
13
MP 1 g/day × 3 days and P 1 mg/kg/day x 2 months then withdrawal 5 mg/15 days
CP (1 g/1.73 m2
PEx: 10 cycles
15
ESRF
Improvement of AH No
14
CP (1 g/1.73 m2
CS adapted to RF): 6 pulses (1/15 days) then MMF
9
Improvement of RF
Improvement of AH
No
15
MP 1 g/day × 3 days and P 1 mg/kg/day × 1 month
CP (1 g/1.73 m2
CS adapted to RF): 2 pulses (1/15 days) PEx: 7 cycles
1
Improvement of RF
Improvement of AH
No
MP: Methylprednisolone, P: Prednisone, CP: Cyclophosphamide, CS: Corporeal surface, RF: Renal function, AZA: Azathioprine, PEx: Plasmepheresis, MMF:
Mycophenolate mofetil, DAH: Diffuse alveolar hemorrhage, SRI: Severe respiratory insufficiency, RFi: Renal failure, ESRF: End-stage renal failure, AV: Alveolar
hemorrhage.
748BenFatmaL,ElAtiZ,LamiaR,etal

of the patients receiving this drug.23-25
Symp-
toms resolved completely after propyl-thio-
uracil withdrawal and steroid therapy.24,25
In patients with evidence of DAH and renal
involvement, kidney biopsy may be considered
to identify the etiology and guide the therapy.26
In this study, 13 patients of 15 patients had a
kidney biopsy.
Similar to the literature, we used in our study
methylprednisolone and cyclophosphamide
pulses and plasmapheresis. Actually, the plasma
exchanges are a component of regimens pres-
cribed to treat systemic necrotizing vasculi-
tis.27
It can remove putative pathogenic auto-
antibodies and circulating immune complexes
from the blood of patients.
Recent reports have described the successful
use of recombinant factor VIIa (rFVIIa) and
intravenous immunoglobulin (IVIg) in severe
DAH.28-30
Experience with more aggressive immuno-
suppression in severe diffuse alveolar hemor-
rhage-associated vasculitis, such as T-cell de-
pletion or autologous stem cell transplantation,
has been limited to a few centers. B-cell de-
pletion with rituximab is currently attracting
most attention with good success in refractory
disease.31
DAH in multiple myeloma was reported in
allogenic bone marrow transplantation, but
rarely as an initial feature.32
Alveolar capillary
membrane lesions are related to the parapro-
tein-mediated mechanism (immunoglobulin A)
sometimes associated with pulmonary hyper-
tension.33,34
In our myeloma case, improvement
of DAH was observed 15 days after initiation
of dexamethasome and Alkylan treatment,
with no relapse after nine months of follow-up.
DAH associated with kidney disease should
be diagnosed promptly in all patients with
falling red cell indices and new infiltrates on
chest radiographs, even in the absence of he-
moptysis or acute dyspnea. Bronchoscopy,
imaging, spirometry, serology and histology
are all appropriate to use for the diagnosis of
DAH. The underlying kidney disease is va-
riable and frequently related to immunologi-
cally mediated disease. Despite advances in
treatment, DAH usually heralds severe vascu-
litis and mortality remains high. Early treat-
ment with frequent i.v. pulse methylpredniso-
lone and i.v. cyclophosphamide and/or plasma
exchange should be instituted for a better
outcome.
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750 Ben Fatma L, El Ati Z, Lamia R, et al

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