Drugs used in asthma

Drugs Used In Asthma
By
M. H. Farjoo, M.D., Ph.D. Bioanimator
Shahid Beheshti University of Medical Sciences

Drugs Used In Asthma
 Introduction
 Classification
 Beta Agonists
 Methylxanthines
 Antimuscarinic Agents
 Corticosteroids
 Cromolyn & nedocromil
 Leukotriene Pathway Inhibitors
 Anti-IgE Antibodies
 Treatment strategy
 Acute Asthma
 3 films about COPD
 Clinical Cases
 Drug delivery devices and Drug Pictures

Introduction
 Asthma is characterized by:
 Increased responsiveness of the bronchi
 Contraction of airway smooth muscle
 Mucosal thickening
 Viscid plugs of mucus
The most easily
reversed pathology

Many cells and mediators are involved in asthma and
lead to several effects on the airways.

Classification
 Asthma may be treated by different drugs.
 Relax smooth muscle
 Drugs that reduce the amount of IgE bound to
mast cells
 Prevent mast cell degranulation
 Block the action of the products released
 Inhibit acetylcholine released from vagus
nerve
Anti-IgE antibody
Cromolyn, Nedocromil
Leukotriene antagonists
Muscarinic antagonists
Sympathomimetics,
Methylxanthines

Beta Agonists
 Along with corticosteroids, are the most widely
used drugs for asthma.
 They relax smooth muscle and inhibit release of
bronchoconstricting substances from mast cells.
 They also inhibit microvascular leakage,
increase ciliary activity and increase cAMP.
 They cause tachycardia, nervousness, and
tremor as side effects.

Beta Agonists (Cont’d)
 Adrenoceptor agonists are best delivered by
inhalation for greatest effect and least systemic
toxicity.
 Even in best conditions, 80-90% of the aerosol
is deposited in the mouth or pharynx.
 Effectiveness can be increased by holding the
breath in inspiration.

 Short acting β2 selective drugs:
 Albuterol (salbutamol)
 Terbutaline
 Metaproterenol
 Pirbuterol
 Bronchodilation is maximal within 15-30 min.
and persists for 3-4 hr.
 All can be diluted in saline for administration
from a nebulizer.

 Long-acting β2 selective agonists:
 Salmeterol
 Formoterol
 Their duration of action is ≥12 hr.
 They are usually used with other drugs (eg:
inhaled corticosteroids)

Methylxanthines
 Methylxanthines:
 Theophylline (tea)
 Theobromine (cocoa)
 Caffeine (coffee)
 Theophylline is most selective in its smooth muscle
effects.
 Caffeine has the most marked CNS effects.

Methylxanthines
 Theophylline is not an ideal drug, but has a low cost.
 Aminophylline is an injectable derivative of
theophylline.
 They Inhibit phosphodiesterase (PDE) and increase
cAMP.
 Adenosine causes airway contraction and histamine
release.
 Theophylline derivatives also may inhibit adenosine
receptors.

Methylxanthines (Cont’d)
 Theophylline also improves contractility and
reverses fatigue of the diaphragm in patients
with COPD.
 So theophylline can diminish dyspnea even in
patients with irreversible airflow obstruction.
 Rate of metabolism: Children > adults >
neonates and young infants
 Cigarette smoking induces metabolizing
enzymes.

 Theophylline has a narrow therapeutic window.
 Improvement in lung function is seen at 5-20
mg/L.
 Vomiting, abdominal discomfort, and anxiety
occur at 15 mg/L in some, and at >20 mg/L in all
patients.
 Higher levels (> 40 mg/L) causes seizures or
arrhythmias.
 These may NOT be preceded by GI or neurologic
warning symptoms.

 Methylxanthines stimulate secretion of both
gastric acid and digestive enzymes.
 Even decaffeinated coffee has a potent
stimulant effect on GI secretion.
 Methylxanthines decrease blood viscosity and
may improve blood flow.
 For this reason pentoxifylline is used in the
treatment of intermittent claudication.

 Caffeine causes mild arousal with increased
alertness and deferral of fatigue.
 Very high doses cause convulsions and even
death.
 Caffeine has positive chronotropic and
inotropic effects on the heart.
 In very sensitive individuals, consumption of a
few cups of coffee may result in arrhythmias.

Amount (gram) Caffeine (mg)
Coffee
Brewed, regular
Instant
Espresso
142–227
142–227
57
40–180
30–120
120
Tea
Brewed, leaf or bag
Instant
Iced
227
227
340
80
50
70
Soft Drinks
Pepsi, Diet Pepsi 340 38
Caffeine Amount In Drinks

Antimuscarinic Agents
 Involvement of parasympathetic system in
respiratory diseases varies among individuals.
 Antimuscarinic agents are used:
 Instead of inhaled β-agonists in asthmatics
 In addition to inhaled β-agonists in asthmatics
 In COPD patients
 Ipratropium is a polar drug used for asthma.
 Tiotropium is used for COPD.

Corticosteroids
 Their most important action is inhibition of airway
mucosal inflammation.
 The inhalational form is the drug of choice for
prophylaxis of asthma.
 Duration of action for inhalational form is 10 – 12 hrs.
 Inhalational therapy minimizes their adverse effects.
 Inhalational drugs include:
 Beclomethasone
 Budesonide
 Fluticasone
 Triamcinolone

Corticosteroids (Cont’d)
 They do not relax airway smooth muscle
directly.
 To prevent adrenal insufficiency they are used
in the morning.
 If nocturnal asthma happens they have to be
given in the afternoon.

Corticosteroids (Cont’d)
 Oropharyngeal candidiasis may occur which can be
managed by gargling water and spit after each dose.
 Hoarseness happens by their effect on vocal cords.
 Chronic use of inhaled corticosteroids reduces
bronchial reactivity.
 Corticosteroids are not curative, asthma returns after
stopping them even if they have been taken for > 2
years.

Cromolyn & nedocromil
 They effectively inhibit both antigen and
exercise induced asthma.
 Alter the function of delayed chloride channels
in the cell membrane, inhibiting cellular
activation.
 They inhibit cough and mast cell (but not
basophil) degranulation in the lung.
 Are only of value when taken prophylactically.

Cromolyn & nedocromil (Cont’d)
 Young patients with extrinsic asthma are most
likely to respond.
 A 4 weeks trial determines whether a patient
will respond.
 Cromolyn solution is also useful for allergic
rhinoconjunctivitis.
 Because the drugs are so poorly absorbed,
adverse effects are minor and rare.

Leukotriene Pathway Inhibitors
 LTC4 & LTD4 exert many effects known to
occur in asthma
 There are two treatment strategy:
 Inhibition of lipoxygenase and leukotriene
synthesis
 Antagonizing leukotriene D4 receptor
 They are weaker than inhaled corticosteroids,
but reduce the frequency of exacerbations.
Zileuton
Zafirlukast,
montelukast

Leukotriene Pathway Inhibitors (Cont’d)
 One advantage is that they are taken orally; children
comply poorly with inhaled therapies.
 Montelukast is approved for children as young as 6 years
of age.
 5-10% of asthmatics are exquisitely sensitive to aspirin
and other NSAIDs.
 It is thought to result from inhibition of cyclooxygenase.
 LT antagonists are useful for preventing this problem.

Anti-IgE Antibodies
 Omalizumab inhibits the binding of IgE to mast
cells but does not activate IgE already bound.
 It also inhibits IgE synthesis by B lymphocytes.
 The murine antibody has been humanized and it
does not cause sensitization.
 Omalizumab's effect is reduction of both the
severity of asthma and corticosteroid dosage.

Anti-IgE Antibodies (Cont’d)
 Patients most likely to respond are those with the
greatest need:
 Patients with a history of repeated exacerbations
 A high requirement for corticosteroid treatment
 Poor pulmonary function
 Omalizumab treatment reduced exacerbations
requiring hospitalization by 88%.
 These benefits justify the high cost of this treatment
in severe disease.
 1 ampule of the drug costs 1,200,000 Tomans in
Iran.

Treatment strategy
 All asthmatics should be instructed for severe,
attacks:
 To take up to four puffs of albuterol every 20
minutes over 1 hour.
 If they do not note clear improvement after the
first four puffs, refer to emergency department.

Treatment strategy (Cont’d)
 Mild asthma
 In these cases inhaled corticosteroid is added:
 Asthma attacks more than twice a week
 Nocturnal symptoms more than twice a month
 FEV1 less than 80% predicted
 Cromolyn or LT antagonist may be used
alternatively, but inhalational steroids are
superior.
Inhaled beta receptor
agonist (Albuterol) on an
"as-needed" basis

Treatment strategy (Cont’d)
 If FEV1 is <50% predicted, oral corticosteroid
is added to control the symptoms and then
stopped.
 Anti-IgE antibody, is reserved for Patients :
 Unresposive to long-acting β-agonist plus high-dose
inhaled corticosteroid
 With demonstrated IgE-mediated sensitivity

Approach to therapy.
ICS, inhaled corticosteroid; LABA, long-acting beta agonists; OCS, oral
corticosteroid.

Acute Asthma
 In mild attacks subcutaneous epinephrine or
inhalation of a β receptor agonist are equally
effective.
 Both of them are superior to IV aminophylline.
 For severe attacks:
 Oxygen
 Frequent administration of aerosolized albuterol
 Systemic treatment with corticosteroids.
 Patients should be closely watched.

A 20-year-old woman with a history of allergic
rhinitis presented to her physician in the autumn
with persistent cough and shortness of breath.
She had been seen 6 weeks earlier for nasal
congestion, rhinorrhea, postnasal drip, and cough
that had bothered her on and off throughout the
summer. Her symptoms occurred at home and at
work. Just recently she had begun to have
shortness of breath while walking to the bus stop.
During coughing episodes, she could hear herself
wheezing. Her grandmother’s albuterol inhaler
had given her some relief from wheezing at night.
The nasal congestion abated when she used
fluticasone nasal spray and loratadine, but the
cough persisted. The patient reported no fevers,
chills, sputum production, headache, joint or
muscle aches, heartburn, nausea, vomiting, or
frequent throat clearing.
The patient’s physician
performed a focused
examination. The oxygen
saturation was 96% while she
was breathing ambient air.
Diffuse, high-pitched,
expiratory wheezing was
heard on auscultation of her
lungs, and there was a
decreased ratio of inspiratory-
to-expiratory time. The
nasopharyngeal mucosa was
normal in appearance.

Medical History
• Migraine headaches
• Allergic rhinitis
• Overweight
Family History
• Mother has allergic rhinitis
• Sister had childhood asthma
• Maternal uncle and cousin have
lymphoma
Social History
• Born in Dominican Republic but now
lives in the Boston area with her
mother
• Works full-time at a day-care center,
where children she cares for are
frequently ill with upper respiratory
infections
• Has a dog
• Reports no exposure to mold, smoke,
cockroaches, or mice
• Reports no history of tobacco, alcohol,
or drug use
Medications
• Fluticasone nasal spray, two
sprays into each nostril daily
• Loratadine, 10 mg daily by
mouth, as needed for allergies
• Benzonatate, 100 mg three
times daily by mouth, as needed
for cough
Allergies
• No known drug allergies

Question 1
Which two of the following are most consistent with the patient’s
presentation?

Spirometric measurements revealed a forced
expiratory volume in 1 second (FEV1) of 1.37
liters (35% of the predicted value). The ratio of
FEV1 to forced vital capacity (FVC) was 0.58
(67% of the predicted value). The post-
bronchodilator FEV1 increased by 300 ml (22%)
to 1.67 liters. The patient’s flow-volume loops are
shown above.
A preliminary diagnosis of
asthma was made on the
basis of the presence of
expiratory wheezing and the
observation that the
symptoms of coughing and
wheezing abated after
treatment with albuterol. An
albuterol inhaler was
prescribed on a trial basis for
use as needed, and the
patient was referred for
pulmonary-function testing.

Question 2
Which one of the following choices best describes the underlying airway
physiology suggested by the results of the patient’s pulmonary-function tests?

On the basis of her clinical presentation and the
results of pulmonary-function testing, which
showed bronchodilator-responsive obstructive
lung disease, the patient received a diagnosis of
asthma. Treatment was started with an inhaled
glucocorticoid and a long-acting beta-agonist
bronchodilator, together with a short-acting beta-
agonist bronchodilator for “rescue” from acute
symptoms.
Despite adherence to her medication regimen for
2 to 3 months, the patient’s wheezing and
shortness of breath worsened. Montelukast, a
selective leukotriene-receptor antagonist, and
tiotropium, a long-acting anticholinergic
bronchodilator, were added to her regimen, but
symptoms persisted.

On one occasion, the patient had severe, acute
coughing spasms that were accompanied by
nausea and loss of appetite. She went to the
emergency department during this episode. A
chest radiograph was obtained and was normal
(see image below). Empirical treatment for
bronchitis was prescribed in the form of
azithromycin plus a 5-day prescription for 40 mg
of prednisone per day, after which her symptoms
resolved.
The patient continued to use fluticasone–
salmeterol, tiotropium, and albuterol inhalers and
to take loratadine and montelukast for the next 4
months, after which her symptoms returned. She
went back to the hospital with unabated
coughing, shortness of breath on exertion, and
wheezing. A complete physical examination was
performed.

Vital Signs and General Appearance
• Temperature, 37.0°C
• Heart rate, 69 beats per minute and
regular
• Blood pressure, 108/57 mm Hg
• Respiratory rate,18 breaths per
minute
• Oxygen saturation, 97% while
breathing ambient air
• Anxious and uncomfortable but not
in acute respiratory distress

Head, eyes, ears, nose, and throat
• Normal-appearing
conjunctiva
• No oropharyngeal erythema
or edema
• Normal-appearing
nasopharyngeal mucosa
• No tenderness to palpation
or discharge from sinuses
• No cervical, supraclavicular,
or axillary lymphadenopathy
• No thyromegaly or thyroid
nodules
Abdomen
• Nontender
• No distention
• No organomegaly
Extremities
No clubbing, cyanosis, or edema
Nervous system
• Normal cranial nerves
• Normal motor strength,
sensation, and gait
Heart:
• No jugular venous
distention
• Regular rate
• No murmurs or gallops
Lungs
• Prolonged expiratory phase
with mild, diffuse
polyphonic wheezing in
both lungs
• No inspiratory crackles,
egophony, abnormal tactile
fremitus, or dullness to
percussion in either lungSkin
No rashes, erythema, or urticaria

Question 3
The patient underwent computed tomography (CT) of the
chest for further evaluation of her cough and wheezing.
(Click the CT below to see representative images.) Which
one of the following abnormalities can be seen?

The results of laboratory tests showed:
• Elevated serum IgE levels (1600 IU per milliliter; reference range, 0–100),
• Levels of aspergillus-specific IgE were normal (<0.35 kU per liter; reference
range, <0.35) and skin tests for aspergillus species were also negative.
• Tests for antinuclear antibodies and antineutrophil cytoplasmic antibodies were
negative.
• No ova or parasites were found in a stool sample.
• A test for strongyloides antibodies was negative.
The results of other laboratory tests are shown in the next slide.
Laboratory Results
What kind of tests would you order for this patient
and why?

Variable Result Normal Range Flag
Hematocrit (%) 39.9 36.0–48.0 Normal
Hemoglobin (g/dl) 13.8 11.5–16.4 Normal
WBC (per mm3) 20,730 4000–10,000 High
Lymphocytes (%) 11.0 18.0–41.0 Low
Monocytes (%) 1.0 4.0–11.0 Low
Neutrophils (%) 35.0 48.0–76.0 Low
Eosinophils (%) 53.0 <5.0 High
Basophils (%) 0 0–1.5 Normal
Lymphocytes (Count) 2280 720–4100 Normal
Monocytes (Count) 210 160–1100 Normal
Neutrophils (Count) 7260 1920–7600 Normal
Eosinophils (Count) 10,990 <500 High
Platelet (Count) 196,000 150,000–450,000 Normal
ESR (mm/hr) 31 0–12 High
Sodium (mmol/L) 138 136–145 Normal
Potassium (mmol/L) 4.3 3.4–5.0 Normal
Chloride (mmol/L) 101 98–107 Normal
Bicarbonate(mmol/L) 23 22–31 Normal
Urea nitrogen (mg/dl) 8 6–23 Normal
Creatinine (mg/dl) 0.8 0.5–1.2 Normal
Calcium (mg/dl) 9.4 8.8–10.7 Normal
Albumin (g/dl) 3.8 3.5–5.2 Normal

This learning element reviews the functions of eosinophils, the types and
causes of diseases in which eosinophilia plays a role, and the approaches to
treating a patient with both asthma and eosinophilia.

Question 4
Which two of the following diagnoses are the most likely, given the patient’s
history, results on physical examination, and findings on laboratory studies,
pulmonary-function tests, and imaging studies?

Question 5
A biopsy specimen from one of the subpleural opacities was obtained. Analysis of
the specimen is most likely to reveal which one of the following findings?

The analysis of specimens
obtained on wedge biopsy
revealed eosinophilic
pneumonia with necrotizing
vasculitis.
These specimens from the lung
biopsy show features of asthma
(Panel A, which reveals mucus-
cell hyperplasia [asterisk],
smooth-muscle hypertrophy
[arrowheads], and an eosinophil-
rich inflammatory infiltrate
[arrows]), eosinophilic
pneumonia (Panel B),
eosinophilic vasculitis (Panel C,
which shows the vessel wall
[asterisk] and eosinophils
[arrowheads]), and areas of
infarction (Panel D).

Question 6
Which one of the following treatments is the most appropriate for this patient at this
time?

The patient received a diagnosis of eosinophilic
granulomatosis with polyangiitis and was started on 60 mg
of prednisone daily. She was discharged home and seen 3
days later at a clinic, where she reported dramatic
resolution of her dyspnea and wheezing. At this visit, her
absolute peripheral eosinophil count was 1.63 per cubic
millimeter (as compared with 10.99 per cubic millimeter at
her initial presentation). The count fell to within normal limits
during the following 2 weeks.
The prednisone was tapered, and azathioprine was started,
initially at 100 mg daily. The dose of azathioprine was
increased to 150 mg daily during the next month, and the
prednisone continued to be tapered slowly, by 10 mg every
month, until a dose of 10 mg per day was reached. The
prednisone was then reduced by 1 mg each month until it
was discontinued. The patient is currently doing well with
150 mg of azathioprine per day.
The patient continued to do well on
maintenance therapy of 150 mg of
azathioprine daily.

• Asthma is a chronic inflammatory disease of the airways that is characterized
by hyperresponsiveness to a variety of stimuli, with symptoms that include
episodic wheezing and dyspnea. Most patients with asthma have baseline
obstruction detected on spirometry. They also have a response to
bronchodilator therapy.
• Asthma therapies include inhaled short-acting beta-agonists, inhaled and oral
glucocorticoids, inhaled long-acting beta-agonist–glucocorticoid combination
inhalers, leukotriene-receptor antagonists, leukotriene-synthesis inhibitors,
and anti-IgE antibodies. These drugs treat the disease process by decreasing
airway inflammation, airway hyperresponsiveness, and bronchoconstriction.
• Eosinophilic granulomatosis with polyangiitis is a vasculitis of small and
medium-sized arteries that affects multiple organs, most often the lungs, and
is characterized by chronic rhinosinusitis, asthma, and eosinophilia. Patients
frequently present with symptoms resembling those of asthma, allergic rhinitis,
and atopic disease.
• Glucocorticoids are the first-line treatment for eosinophilic granulomatosis with
polyangiitis.
Teaching Points

History:
A 43-year-old woman presented with an 8-month history of progressively
worsening nonproductive cough. She had been treated with antibiotic agents
for presumed bronchitis, but her cough continued to worsen.
Clinical Examination
Her vital signs were normal, the pulmonary examination was notable for
wheezing in both lungs
Laboratory findings
the white-cell count, including the absolute number of eosinophils, was normal.
Other procedures
Results of pulmonary-function tests suggested an obstructive defect that did
not respond to bronchodilators. Bronchoscopy revealed diffuse nodules in the
tracheobronchial mucosa (Panel A). Biopsy of a nodule revealed eosinophilic
infiltration of the bronchial mucosa. There was no evidence of tumor, infection,
vasculitis, or granulomas.
What is the diagnosis? What do you do for the patient?

Diagnosis:
Eosinophilic bronchitis
Treatment
The patient was treated with systemic glucocorticoids and inhaled budesonide
for 1 month. At 1 month after the start of therapy, follow-up bronchoscopy
revealed a considerable decrease in the size of the nodules in the
tracheobronchial mucosa (Panel B), repeat pulmonary-function tests revealed
resolution of the obstructive defect, and the patient’s clinical symptoms had
resolved completely. Because small nodules were still visible, the patient
received inhaled budesonide for 2 additional months, after which the mucosal
nodules in the trachea were no longer present. At follow-up 6 months after the
start of therapy, the clinical symptoms had not recurred.
Patients with eosinophilic bronchitis usually have normal results on spirometry,
but diffuse nodules in the tracheobronchial mucosa cause obstruction that does
not respond to bronchodilators.
Yanhong Ren, M.D., Ph.D.
Huaping Dai, M.D.
China–Japan Friendship Hospital, Beijing, China

History:
A 10-year-old previously healthy girl presented with episodic wheezing,
dyspnea, and progressive exercise intolerance, which had developed during
the preceding 9 months.
Clinical Examination
the patient had moderate bilateral expiratory wheezing. She was treated for
presumed asthma with multiple courses of inhaled bronchodilators, inhaled
corticosteroids, montelukast, and oral corticosteroids. Though the patient
reported that her condition had improved somewhat, there was no
demonstrable objective improvement.
Other procedures:
spirometry revealed severe expiratory obstruction (Panel A). The patient
underwent flexible fiberoptic bronchoscopy, which revealed nearly complete
(>90%) occlusion of the distal trachea by a vascular mass. Computed
tomographic angiography showed that the mass did not extend beyond the
trachea (Panel B, arrow).
What is the diagnosis? What do you do for the patient?

Diagnosis:
Pathological analysis revealed an inflammatory pseudotumor, a benign
tumor composed of a proliferation of inflammatory cells, which are
rarely invasive.
Treatment
This type of tumor is usually cured by local excision, and the mass was
ablated endoscopically with the use of a potassium titanyl phosphate
laser.
One month after surgery, the patient was free of symptoms and had
normal results on spirometry (Panel C). Pulmonary pseudotumors are
rarely the cause of wheezing. However, a lack of response to first-line
therapies warrants further investigation, including spirographic analysis.
Inderpal Randhawa, M.D.
Eliezer Nussbaum, M.D.
Miller Children's Hospital, Long Beach, CA

A 79-year-old woman with chronic obstructive pulmonary
disease and a 40-pack-year history of cigarette smoking
reports 3 months of right shoulder pain that radiates down her
arm. Her symptoms have persisted and progressed despite a
course of physical therapy and use of nonsteroidal
antiinflammatory medications and acetaminophen.
On examination, her right shoulder has full range of motion
and is not swollen or tender to palpation. She has wasting of
the intrinsic muscles of the right hand. Lung examination is
remarkable for mild bilateral expiratory wheezing. Palpation of
her right axilla reveals no masses.

Which one of the following tests is most appropriate to
evaluate this patient’s symptoms?
1. MRI of the right shoulder
2. Electromyography and nerve-conduction studies
3. Chest radiograph
4. Radiograph of the right shoulder
5. Radiographs of the cervical spine

Which one of the following tests is most appropriate to
evaluate this patient’s symptoms?
1. MRI of the right shoulder
2. Electromyography and nerve-conduction studies
3. Chest radiograph
4. Radiograph of the right shoulder
5. Radiographs of the cervical spine
Key Learning Point :
The most appropriate step in evaluating a smoker with chronic obstructive
pulmonary disease who has shoulder pain and wasting of the small muscles
of the hand is a chest radiograph to detect a possible Pancoast tumor.

A 21-year-old woman presented to the
emergency department with an 8-month history
of swelling and pain in the right thigh.
MRI of the right leg revealed a large periosteal
femoral mass and thrombus in the right femoral
vein, for which she received anticoagulation
therapy.
The patient subsequently experienced dyspnea
and pleuritic chest pain. A chest x-ray and CT
was done (next slides).

What is the likely diagnosis?
1. Pulmonary embolism
2. Pulmonary sarcoidosis
3. Eosinophilic granulomatosis with polyangiitis
4. Chondroblastic osteosarcoma
5. Miliary tuberculosis

What is the likely diagnosis?
1. Pulmonary embolism
2. Pulmonary sarcoidosis
3. Eosinophilic granulomatosis with polyangiitis
4. Chondroblastic osteosarcoma
5. Miliary tuberculosis
The correct answer is chondroblastic osteosarcoma. This is a bone
cancer typically originating in the metaphysis of long bones, commonly
the femur, in children and young adults. The diagnosis was confirmed by
biopsy of the periosteal leg mass, and chest radiography confirmed the
presence of partially calcified masses throughout both lungs, suggestive
of pulmonary metastases.

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