Clinical Brief
Pulmonary Arteriovenous Malformations Milind S. Tullu, Murlidhar D. Mahajan, Captain S. Ramchandani, Chandrahas T. Deshmukh,Jaishree R. Kamat, Rajwanti K. Vaswani, Prem K. Pahuja and 1
Venkatesh Rangarajan
1
Department of Pediatrics, Seth G.S. Medical College and KEM Hospital, and Radiation Medicine Centre (BARC), Tata Memorial Hospital, Parel, Mumbai−400 012, Maharashtra, India. Abstract. Pulmonary arteriovenous malformations rarely present in childhood. Two cases are presented in this report. Both the cases presented clinically with cyanosis and clubbing without a cardiac murmur. The second case had cerebral abscess in addition. Both the cases underwent a contrast−enhanced echocardiography which suggested the presence of pulmonary arteriovenous malformations. The first case also underwent 99mTc radionuclide scan and pulmonary angiography. The cases are being reported for their characteristic clinical features and for emphasizing the role of non−invasive modalities like contrast−enhanced echocardiography and radionuclide scan in reaching the diagnosis.[Indian J Pediatr 2001; 68 (9) : −894] Key words : Pulmonary arteriovenous fistula; Cyanosis; Cerebral abscess; Echocardiography; Embolization Pulmonary arteriovenous malformations (PAVM’s) are rare abnormal
Intravenous injection of 99mTc labelled macroaggregated albumin revealed
communications (single or multiple) between the pulmonary arterial and venous
normally perfused lungs with radioactivity seen in both the kidneys suggesting the
systems (bypassing the pulmonary capillary bed).1,2 Most of the patients with
presence of PAVM’s (Fig. 1). The child underwent a pulmonary angiography which
PAVM’s present in adulthood and only few pediatric cases have been reported in
confirmed the presence of the PAVM’s which were bilateral and in the lower lobes
literature.1,3,4 This article describes two cases of PAVM’s.
of the lungs. The parents refused for any therapeutic intervention for the PAVM’s.
Case Reports
Case 2 : A ten−year−old female child born of a non−consanguineous marriage presented with fever, headache, decreased movements of the right upper and lower
Case 1: A five−year−old female child born of a non−consanguineous marriage
limb with slurred speech, and dribbling of the saliva from angle of mouth. There was
presented with fever and cough of one months’ duration and breathlessness on
no history suggestive of cardiac disease for four days. On examination, the vital
exertion since the age of three years. There was no history suggestive of
parameters were normal; central cyanosis and grade III clubbing was present. The
congenital heart disease. On examination, the vital parameters were normal.
child had right−sided upper motor neuron type of facial palsy and right hemiparesis.
Central cyanosis, grade III clubbing, and generalized lymphadenopathy were
The cardiovascular system was normal. Soft hepatomegaly (span of
noted. The cardiovascular system was normal. Abdominal examination revealed hepatomegaly (of 4 cm with span of 7 cm) and splenomegaly of 4 cm. The patient was anemic (hemoglobin: 9.7 gm%; packed cell volume: 30%); arterial blood gas showed hypoxia (pO2: 53; SaO2: 87%); electrocardiogram (ECG), routine colour doppler of the heart, and computed tomographic scan of the chest were normal. The child was human immunod− eficiency virus antibody positive by the ELISA test. On a contrast−enhanced echocardiography, using agitated saline injected in peripheral vein, there was appearance of contrast bubbles on the right side of the heart and then on the left side after 3 cardiac cycles (which suggested the presence of PAVM’s).
Reprint requests : Dr. Milind S. Tullu, ‘Sankalp Siddhi’, Block No. 1, Ground floor, Kher Nagar, Bandra (East), Mumbai 400051, Maharashtra, India. E−mail :
[email protected]
Fig. 1. Case 1−99mTc labelled macroaggregated albumin radionuclide scan showing normally perfused lungs. Also, radioactivity is seen in both the kidneys (arrows) suggesting the presence of pulmonary arteriovenous malformations.
Milind S. Tullu et al
14 cm) and firm splenomegaly of 3 cm was present. Investigations revealed
11 have reported series of pediatric cases with PAVM’s. PAVM’s are more
anemia (hemoglobin : 10 gm%; packed cell volume : 33%), leukocytosis
common in the right lung and are frequently located in the lower lobe (right or left
(count : 12,700/cumm), and hypoxia (pO2 : 62; SaO2: 90%). Computed
lung) or the right middle lobe.1,4,11−13 Occasionally, a pulmonary artery may be
tomographic scan of the brain revealed a cerebral abscess in the left
connected directly to the left atrium.14 The PAVM’s permit blood from pulmonary
temporo−parietal region. The ECG was normal. Contrast−enhanced
arteries to reach left atrium (without being oxygenated or filtered).2,10 This
echocardiography of the heart using agitated saline revealed contrast bubbles
shunting increases chances of producing emboli which reach the systemic
on the right side of the heart (Fig. 2A), followed by the left side (Fig. 2B)
circulation directly.2 Systemic desaturation occurs when more than 20% of the
after 3 cardiac cycles. This suggested the presence of pulmonary
blood flow is shunted.15 In severe cases, it causes polycythemia and
arteriovenous fistula (PAVM's). The patient was treated with intravenous
cyanosis.1,2,4−6,10 Sometimes, only orthocyanosis may be seen.16
antibiotics and anticonvulsants. The patient did not follow−up further.
Clinically, the patient may present with cyanosis, respiratory distress, and heart failure at birth14 (if the communication is large or if the pulmonary arteries
Discussion
communicate with the left atrium directly); thus mimicking a cyanotic congenital heart disease. In adults, the main symptom is breathlessness while children mainly
Pulmonary arteriovenous malformations (also called arteriovenous aneurysm
have cyanosis.2,4,5,10 Adults may have history of cyanosis from childhood.15 As
or arteriovenous fistula) are rarely diagnosed in children. Keith et al5 found
seen in our patients, central cyanosis and clubbing are the cardinal features on
only six cases of PAVM’s in a total of 15,104 cases of congenital heart
examination.1−5,12,15 Hemoptysis and cerebral symptoms (headache, dizziness,
disease. There is a strong association between
confusion, convulsions) due to cerebral malformations, hypoxia, and polycythemia may complicate the clinical course as also a cerebrovascular accident or a cerebral abscess.1−5,6,10,11,15 The cardiovascular system examination is normal. A systolic or continuous murmur of a superficial PAVM may be heard at atypical extra−cardiac locations on the chest wall.1−5,7,11,12,15 The intensity of the murmur may be augmented by inspiration or Muller maneuver and diminished by Valsalva maneuver.5,7,15 Nose bleeds indicate the presence of telangiectasia in the nasal mucosa.3−5,7 The disorder may be revealed while investigating asymptomatic family members of a patient with hereditary hemorrhagic telangiectasia or as an incidental finding on the chest radiograph.2,4 The ECG is usually normal.4,5,7 Cardiac chamber hypertrophy may be seen in patients presenting in infancy.2 Chest radiograph may reveal normal heart shape and size or rarely, mild cardiomegaly (in very large PAVM’s).10,12,14,15 The lung fields frequently show rounded or slightly nodular opacities ranging in size and shape and rarely calcifications; the afferent pulmonary arterial and efferent venous
Fig. 2. Case 2. Contrast−enhanced echocardiography of the heart with the
channels may also be seen.2−7,10−12,15 The chest radiograph may be normal in
agitated saline test. A. Initially, the contrast bubbles are seen only on right
those with diffuse microscopic telangiectasia17 or solitary lesions obscured by the
side of the heart.
heart or the diaphragm. Fluoroscopy reveals pulsations of the aneurysmal shadow in most cases.1,5
B. Later, after 3 cardiac cycles, the contrast bubbles are also visualized on the left side of the heart. PAVM’s and hereditary hemorrhagic telangiectasia (Rendu−Osler−Weber disease).1,3,5,6 PAVM’s may run in families.1,2,6 Most PAVM’s are congenital. Acquired PAVM’s may be seen after trauma,7 post−Glenn shunt or post−Fontan procedure8 and may even complicate liver disease.9 Shumacker et al10 and Dines et al7,
Pulmonary Arteriovenous Malformations
Mild arterial desaturation is seen.1,4 A useful screening test is
coil into the systemic circulation.2,3,13,19,20 Various surgeries (like vessel
contrast−enhanced echocardiography using agitated saline or indocyanine green
ligation, wedge resection, suturing of the fistula, lobectomy, segmental resection,
dye.7 Normally, the contrast injected in a peripheral vein appears on the right
and rarely pneumonectomy) can be performed (with a mortality of about
side of the heart (right atrium and ventricle) and does not appear on the left side
5−10%); but these need to be conservative as far as possible.1,2,4,5,7,10−13,15
(left atrium and ventricle).8 In the patients with PAVM’s, the contrast appears
In asymptomatic patients, it may be safer to observe the patient for some period
on the left side of the heart after a delay of about three cardiac cycles.18 This
before contemplating surgery,5 though some surgeons believe that asymptomatic
was seen in both of our cases (Figs. 2A and 2B). In the patients with an
cases should be operated to prevent life−threatening complications.10,12
intracardiac shunt, the contrast appears on the right side and then immediately on
The prognosis is good post−operatively and also depends on the remaining
the left side of the heart without any delay.18 Cardiac catheterization can be
aneurysms in the lung and pulmonary insufficiency.4,5,11 Unoperated patients
avoided by doing this study.7 Radionuclide techniques can also be used.8,9,15
may die of rupture of the PAVM’s, massive hemoptysis, brain abscess or
99mTc labelled macroaggregated albumin particles injected in a peripheral vein
convulsions.5,11 Patients with PAVM’s and hereditary hemorrhagic
do not normally pass into the systemic circulation as they have a larger size
telangiectasia have a higher incidence of multiple fistulas, increased rate of
(20−30 mm) than the pulmonary capillaries (8−15mm). The rapid appearance of
fistula growth, and an increased frequency of complications.11 We have
radioactivity in the systemic high flow organs such as the kidneys, brain, spleen,
reported these two cases to describe the clinical features in PAVM’s and to
and thyroid (Case 1; Fig. 1) confirms the presence of PAVM’s.9 Hence, in
highlight the importance of contrast−enhanced echocardiography and
suspected cases of PAVM’s, while performing lung scintigraphy, it is mandatory
radionuclide scan in reaching the diagnosis. Presence of PAVM’s should be
to do the abdominal views (to detect the radioactivity in the kidneys) in addition
considered in the patients presenting with cyanosis and clubbing without a
to the lung views. Definitive diagnosis is established by cardiac catheterization
cardiac murmur. Such cases should be referred to a centre where further
and pulmonary angiography.1,4,5,7,10−12 Thrombosis and cerebral embolism
diagnostic and therapeutic facilities are available.
may complicate the procedure. One of our patients underwent pulmonary
Abbreviations :
angiography. Thrombosed fistulas and diffuse microscopic malformations may
pO2 : Partial Pressure of Oxygen
not be visualized and may need an open lung biopsy.17
SaO2 : Oxygen Saturation and
The differential diagnosis consists of conditions like cyanotic congenital heart
Tc : Technetium
disease, abnormal hemoglobins (sulphemoglobinemia or methemoglobinemia),
Acknowledgements
polycythemia rubra vera, chronic lung diseases, primary pulmonary
The authors thank Dr. R.G. Shirahatti − Dean, Seth G. S. Medical College and
hypertension, etc.4,12,14,15 Local complications include rupture leading to
KEM Hospital for granting permission to publish this article. The authors also
hemothorax or hemoptysis, infection, and rarely calcification.2,4,10,15 The
acknowledge Dr. Bharat V. Dalvi, MD, DM (Cardiology), FACC (USA),
systemic complications are thrombosis and embolism.2,15 Abscesses (in brain,
Consultant Cardiologist, Glenmark Cardiac Centre, Mumbai, for performing the
liver, spleen) may occur, as also myocardial infarction.2,10,15 Cardiac failure is
contrast−enhanced echocardiography of one of the cases reported.
rare as the cardiac output remains normal in these patients but may be seen in neonates with pulmonary artery to left atrial connection.14
References
The management options include conservative treatment, transcatheter embolization, and surgery. Intervention is necessary for symptomatic patients
1. Sluiter−Eringa H, Orie NGM, Sluiter HJ. Pulmonary arteriovenous fistula:
and for those with large shunts.2,5,13 Patients with enlarging fistulas, multiple
Diagnosis and prognosis in noncomplainant patients. Am Rev Respir Dis 1969;
bilateral fistulas, and hereditary hemorrhagic telangiectasia also benefit from
100: 177−188.
treatment.2 It is possible that treatment of major PAVM’s may lead to
2. Bush A. The child with continuous murmur. In Anderson RH, Macartney FJ,
enlargement of the smaller lesions by increasing the blood flow through them.13
Shinebourne EA, Tynan M, eds. Paediatr Cardiology. Edinburg; Churchill
Transcatheter embolization of all the malformations using balloons or steel coils
Livingstone, 1987; 1001−1022.
can be attempted if technically feasible.2,19,20 Complications of the procedure
3. Swanson KL, Prakash UB, Stanson AW. Pulmonary arteriovenous fistulas:
include pulmonary infarction syndrome, hemothorax, balloon foldover,
Mayo Clinic experience, 1982−1997. Mayo Clin Proc 1999; 74 : 671−680.
premature or difficult detachment of balloons, and migration of the balloon or
4. Jeresaty RM, Knight HF, Hart WE. Pulmonary arteriovenous fistulas in children : Report of two cases and review of literature. Am J Dis Child 1966; 111 : 256−261. 5. Keith JD. Congenital pulmonary arteriovenous aneurysm. In Keith JD, Rowe RD, Vlad P, eds. Heart Disease in Infancy and Childhood. 3rd edn, New York; MacMillan Publishing Co. Inc, 1978; 887−889.
Milind S. Tullu et al
6. Chandler D. Pulmonary and cerebral arteriovenous fistula with Osler’s
14. Clarke CP, Goh TH, Blackwood A, Venables AW. Massive pulmonary
disease. Arch Intern Med 1965; 116 : 277−282.
arteriovenous fistula in the newborn. Br Heart J 1976; 38 : 1092−1095.
7. Dines DE, Seward JB, Bernatz PE. Pulmonary arteriovenous fistulas. Mayo
15. Prager RL, Laws KH, Bender HW. Arteriovenous fistula of the lung. Ann
Clin Proc 1983; 58 : 176−181.
Thorac Surg 1983; 36 : 231−239.
8. Cloutier A, Ash JM, Smallhorn JF et al. Abnormal distribution of pulmonary
16. Hoeppner VH. Orthocyanosis : A sign of pulmonary arteriovenous
blood flow after the Glenn shunt or Fontan procedure : Risk of development of
malformation. Thorax 1982; 37 : 952−953.
arteriovenous fistulae. Circulation 1985; 72 : 471−479.
17. MacNee W, Buist T, Finlayson NDC et al. Multiple microscopic pulmonary
9. Keren G, Boichis H, Zwas TS, Frand M. Pulmonary arterio−venous fistulae in
arteriovenous connections in the lungs presenting as cyanosis. Thorax 1985; 40 :
hepatic cirrhosis. Arch Dis Child 1983; 58 : 302−304.
316−318.
10. Shumacker HB Jr, Waldhausen JA. Pulmonary arteriovenous fistulas in
18. Shub C, Tajik AJ, Seward JB, Dines DE. Detecting intrapulmonary
children. Ann Surg 1963; 158 : 713−720.
right−to−left shunt with contrast echocardiography : Observations in a patient
11. Dines DE, Arms RA, Bernatz PE, Gomes MR. Pulmonary arteriovenous
with diffuse pulmonary arteriovenous fistulas. Mayo Clin Proc 1976; 51: 81−84.
fistulas. Mayo Clin Proc 1974; 49 : 460−465.
19. Barth KH, White RI Jr, Kaufman SL, Terry PB, Roland JM. Embolotherapy
12. Moyer JH, Glantz G, Brest AN. Pulmonary arteriovenous fistulas :
of pulmonary arteriovenous malformations with detachable balloons. Radiology
Physiologic and clinical considerations. Am J Med 1962; 32 : 417−435.
1982; 142 : 599−606.
13. White RI Jr, Mitchell SE, Barth KH et al. Angioarchitecture of pulmonary
20. Reidy JF, Jones ODH, Tynan MJ, Baker EJ, Joseph MC. Embolisation
arteriovenous malformations: An important consideration before embolotherapy.
procedures in congenital heart disease. Br Heart J 1985; 54 : 184−192.
Am J Roentgenol 1983; 140 : 681−686.
