Lung expansion therapy involves several techniques in respiratory care designed to prevent or correct atelectasis. In this guide, we will discuss the different procedures that can be used to promote lung expansion and treat alveolar collapse.
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What is Atelectasis?
Atelectasis is a term that refers to a collapse in the alveoli of the lungs. It could be a total collapse of an entire lung or a partial collapse in one or more lobes.
As you take a breath in, air moves through your mouth and trachea down through the airways of the lungs until it reaches the tiny air sacs that are known as alveoli.
This is where the gas exchange of oxygen and carbon dioxide takes place. Therefore, if air fails to reach this region, it can result in many different problems within the body.
When this occurs, the alveoli that are not filled with air cannot expand, and this is what’s known as atelectasis.
Causes of Atelectasis
Atelectasis is common in postoperative patients where it can occur during or after the procedure.
The reason is that surgery often causes shallow breathing, which results in inadequate airflow to the alveolar region of the lungs. Atelectasis can also be caused by:
- Airway obstruction
- Mucus plug
- Lung tumor
- Pleural effusion
- Respiratory muscle weakness
The elderly population and those who smoke cigarettes are also at a higher risk for atelectasis.
Symptoms of Atelectasis
The symptoms of atelectasis will depend on the severity and location of the collapse. In some cases, there may be no symptoms at all. However, in other instances, patients may experience:
- Shortness of breath
- Chest pain
The treatment for atelectasis may vary depending on the patient’s signs and symptoms. However, the most effective treatment method involves correcting the underlying cause of the patient’s alveolar collapse.
In general, post-surgical atelectasis can be treated and prevented with lung expansion therapy.
Lung Expansion Therapy
Lung expansion therapy involves several respiratory care procedures and techniques that are designed to treat atelectasis, pneumonia, acute respiratory failure, and other conditions of the lungs.
The modalities that can be used in lung expansion therapy include:
- Early patient mobilization
- Deep breathing/directed cough
- Incentive spirometry (IS)
- Continuous positive airway pressure (CPAP)
- Positive airway pressure
- Intermittent positive airway pressure breathing (IPPB)
- High-flow nasal cannula (HFNC)
The techniques that are used will be based on the individual patient’s needs and the severity of their condition.
Early Patient Mobilization
One of the best ways to prevent atelectasis is through early patient mobilization. This means that patients should be encouraged to get out of bed and move around as soon as possible after surgery.
Prolonged bed rest is linked to an increased risk of several complications, including pneumonia, pulmonary embolism, deep venous thrombosis (DVT), and atelectasis.
However, early ambulation improves ventilation and gas distribution, which decreases the risk of alveolar collapse.
Deep Breathing and Directed Coughing
Deep breathing exercises and directed coughing can help treat patients with atelectasis by clearing secretions and recruiting collapsed alveoli.
Patients who are able to do deep breathing exercises on their own can be instructed to take slow, deep breaths in through the nose and out through the mouth. Then they can follow up a deep breathing cycle with a forceful cough. Patients who are unable will need to use a different treatment method.
Incentive spirometry (IS) is a technique in which patients use a hand-held device to take sustained maximum inspirations (SMI). The goal is to reach a predetermined volume of air that is initially set by the respiratory therapist.
This technique can help improve lung function and prevent atelectasis by:
- Mimicking natural sighing
- Stimulating deep breathing
- Expanding the lungs
- Increasing alveolar ventilation
- Improving inspiratory muscle performance
The potential outcomes of incentive spirometry include decreased atelectasis, improved breath sounds, improved chest x-ray, increased SpO2, increased vital capacity, stronger cough, and improved respiratory muscle performance.
Continuous Positive Airway Pressure
Continuous positive airway pressure (CPAP) is a technique in which a machine delivers air through a mask that covers the nose and mouth. The air pressure is adjusted so that it is slightly higher than the atmospheric pressure.
This technique is commonly used to treat sleep apnea, but it can also be used to treat atelectasis. CPAP helps to prevent atelectasis by:
- Keeping the airways open
- Improving gas exchange
- Providing positive end-expiratory pressure.
Other potential outcomes of CPAP therapy include increased oxygenation, improved vital capacity, stronger cough, and improved patient comfort.
Positive Airway Pressure
Positive airway pressure (PAP) is a technique in which a device delivers positive pressure to improve lung expansion. It involves the use of PEP, flutter, and CPAP.
PEP and flutter can be used for airway clearance therapy, however, we’re looking at how PAP can be used to treat and prevent atelectasis.
In general, PAP therapy helps increase the patient’s functional residual capacity (FRC). This results in the opening of collapsed alveoli, increased lung compliance, decreased work of breathing, improved collateral ventilation, and enhanced secretion removal.
Intermittent Positive Airway Pressure Breathing (IPPB)
IPPB is a type of noninvasive ventilation (NIV) that delivers positive pressure during inspiration and then returns to atmospheric pressure during expiration. The machine is capable of providing full ventilatory support. However, that is not its intended use.
IPPB was designed to help patients take deeper breaths, stimulate a cough, and prevent or decrease atelectasis. It’s effective in doing so because it improves gas exchange, increases lung compliance, and reduces work of breathing.
Other potential outcomes of IPPB therapy include improved breath sounds, increased oxygenation, improved vital capacity, improved chest x-ray, and a stronger cough.
High-Flow Nasal Cannula
High-flow nasal cannula (HFNC) is a type of NIV that delivers a high flow of warm, humidified oxygen through a nasal cannula with larger prongs. This allows higher flow rates to be delivered, which provides the patient with a high level of comfort.
HFNC has many potential benefits for patients with atelectasis. It provides enhanced flow, which helps wash out CO2 from anatomic deadspace. It also can provide a more stable FiO2.
In addition, this device also delivers a small amount of positive pressure as the patient’s breaths against higher inspiratory flows. This helps with the recruitment of collapsed alveoli, which explains why a high-flow nasal cannula is effective in treating and preventing atelectasis.
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Lung Expansion Therapy Practice Questions:
1. What is lung expansion therapy used for?
It is used to prevent or correct atelectasis and respiratory complications, often in postoperative patients.
2. What is gas absorption atelectasis?
Gas absorption atelectasis occurs when a mucus plug blocks ventilation to selected regions of the lung.
3. What is compression atelectasis?
A type of atelectasis caused by persistent breathing with small tidal volumes that is common in certain types of restrictive chest wall disorders
4. What factors can cause atelectasis?
Obesity, neuromuscular disorders, heavy sedation, surgery near the
5. What does atelectasis cause?
Decreased FRC, V/Q mismatch, arterial hypoxemia, decreased surfactant production, and an ineffective cough, which leads to retained secretions and possible pneumonia
6. What are the clinical signs of atelectasis?
History of recent major surgery, tachypnea, fine late inspiratory crackles, bronchial or diminished breath sounds, tachycardia, and signs of volume loss on a chest radiograph
7. How does lung expansion therapy work?
It works by increasing the transpulmonary pressure gradient, which is the difference between alveolar and pleural pressure. The greater the transpulmonary pressure gradient, the more alveolar expansion will occur.
8. How can you increase the transpulmonary pressure gradient?
It can be increased by decreasing the surrounding pleural pressure, or by increasing the alveolar pressure.
9. What therapy decreases pleural pressure?
10. What therapy increases alveolar pressure?
IPPB and positive pressure therapies
11. What is another name for incentive spirometry?
Sustained maximal inspiration (SMI)
12. How does incentive spirometry work?
It mimics natural sighing by encouraging patients to take slow, deep breaths.
13. What are the indications for incentive spirometry?
The presence of pulmonary atelectasis; the presence of conditions that could cause atelectasis, like upper abdominal surgery, thoracic surgery, and surgery in patients with COPD; the presence of a restrictive lung defect associated with quadriplegia or a dysfunctional diaphragm
14. What are the contraindications for incentive spirometry?
Unconscious patients or those unable to cooperate, inability to comprehend instructions, and patients unable to generate adequate inspiratory flow
15. What are the hazards and complications of incentive spirometry?
Hyperventilation, discomfort, fatigue or overexertion, pulmonary barotrauma, and hypoxemia
16. How do you teach incentive spirometry?
Demonstrate, then observe the patient
17. When is the best time to teach incentive spirometry?
Prior to surgery
18. What must be performed before and after incentive spirometry?
19. What are the outcomes of incentive spirometry therapy?
Improvement of atelectasis, decreased respiratory rate, normal pulse rate, resolution of abnormal breath sounds, improved chest radiograph, improved PaO2, decreased PaCO2, increased SpO2, increased VC and peak expiratory flow, restoration of preoperative FRC or VC, improved inspiratory muscle performance and cough, attainment of preoperative flow and volume levels, and increased FVC
20. What instructions are given for incentive spirometry?
Exhale normally, take slow deep inspirations, perform an inspiratory pause/breath-hold, take slow and passive exhalations, rest between breaths, and perform 10 breaths every hour while awake
21. What has to be documented during incentive spirometry?
Date and time given, type of treatment, goals reached and number of times, breath sounds before and after, cough and nature of secretions, and any adverse reactions
22. What is intermittent positive pressure breathing?
A noninvasive technique that uses positive airway pressure to provide machine-assisted deep breaths and stimulates coughing
23. How does IPPB work?
Positive pressure is applied to the airway and is transmitted to the alveoli and pleural space during inspiration. Gas flows into the lungs due to the pressure differences, and exhalation is passive.
24. What are the indications for IPPB therapy?
It is indicated in patients with atelectasis that aren’t responsive to other therapies and in patients who are at a high risk for atelectasis but can’t perform incentive spirometry.
25. What are the contraindications for IPPB?
Tension pneumothorax, ICP greater than 15 mmHg, hemodynamic instability, active hemoptysis, tracheoesophageal fistula, recent esophageal surgery, active untreated tuberculosis, radiographic evidence of blebs, recent facial oral or skull surgery, hiccups, air swallowing, and nausea
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26. What are the hazards and complications of IPPB?
Increased airway resistance, pulmonary barotrauma, nosocomial infections, respiratory alkalosis, hyperoxia, impaired venous return, gastric distension, air trapping, auto-PEEP, overdistention, and psychological dependence
27. What baseline assessment should be performed before IPPB?
Medical history, vital signs, sensorium and appearance, breathing pattern, and auscultation
28. What are the outcomes of IPPB?
Improved VC, increased FEV, enhanced cough and secretion clearance, improved chest radiograph, improved breath sounds, and improved oxygenation
29. What are the alternative therapeutic methods to IPPB?
EzPAP, incentive spirometry, or pursed-lip breathing
30. What has to be documented when administering IPPB?
Pre-assessment, post-assessment, adverse effects, medications used, settings used, volume achieved, and length of the treatment
31. What is the “triple S” rule for IPPB?
If a patient has a severe adverse reaction, you should stop the treatment, stay with the patient, and stabilize the patient.
32. What do PEP, EPAP, and CPAP stand for?
Positive expiratory pressure, expiratory positive airway pressure, and continuous positive airway pressure
33. What is CPAP therapy?
A type of therapy where patients breathe through pressurized circuit against a threshold resistor at pressures between 5 and 20 cmH2o. The CPAP machine maintains positive pressure during inspiration and expiration.
34. What are the indications for CPAP?
To recruit collapsed alveoli, decrease work of breathing, improve the distribution of ventilation, enhance secretion removal, treat cardiogenic pulmonary edema, and improve oxygenation
35. What are the contraindications for CPAP?
Hemodynamic instability and hypoventilation
36. What are the hazards and complications of CPAP?
Barotrauma, hypoventilation, gastric distention, vomiting, and aspiration
37. What is the most common problem with CPAP?
38. What should be monitored during CPAP?
Monitor for hypoventilation and an elevated PaCO2
39. How do you choose an approach for CPAP?
Choose the one that is safest, simplest, and most effective, and evaluate the patient’s level of cooperation, amount of pulmonary secretions, and spontaneous vital capacity.
40. What type of patients are at risk for postoperative atelectasis?
Patients with a history of lung disease that causes increased mucus production, patients with chronic bronchitis, patients who smoke cigarettes, and patients with a history of inadequate nutritional intake
41. What is the cause of postoperative atelectasis?
An ineffective cough
42. What type of lung expansion therapy is physiologically most common?
43. What is monitored during incentive spirometry?
Patient performance, frequency of sessions, number of breaths per session, inspiratory volume or flow goals, effort and motivation, compliance with technique, device within reach and encouragement for the patient to do it independently, new and increasing inspiratory volumes each day, and vital signs
44. What are the symptoms of hyperventilation during incentive spirometry?
Lightheadedness and dizziness
45. What are the two types of incentive spirometry?
Volumetric and flow-oriented
46. How does volumetric incentive spirometry work?
Volumetric incentive spirometry devices measure and visually indicate the volume achieved during a maneuver. They employ a bellow that rises according to the inhaled volume. When the patient reaches the target inspiratory volume, a controlled leak in the device allows the patient to sustain inspiratory effort for a short period of time.
47. How does flow-oriented incentive spirometry work?
Flow-oriented devices measure and visually indicate the degree of inspiratory flow. This flow can be equated with volume by assessing the duration of inspiration.
48. What do both types of incentive spirometers do?
They attempt to encourage the same goal for a patient, which is to achieve a sustained maximum inspiratory effort in order to prevent or correct atelectasis.
49. What patients benefit from IPPB?
Patients who are at a high risk for atelectasis but are unable to participate in patient-directed techniques, such as incentive spirometry or deep breathing.
50. What are the goals of IPPB?To help the patient take deeper breaths, promote a cough, improve the distribution of ventilation, and to achieve improved ABG results
51. What is the purpose of a cough?
To clear secretions from the airways
52. Which of the following is not a potential hazard of IPPB?
Increased cardiac output
53. Which of the following statements is not true about IPPB?
IPPB should be the single treatment modality for resorption atelectasis.
54. All of the following parameters should be evaluated after intermittent positive-pressure breathing therapy except:
55. All of the following machine performance characteristics should be monitored during IPPB except:
56. Which of the following initial flow settings would you select when setting up a continuous positive airway pressure flow-mask system for a patient with atelectasis?
2 to 3 times the patient’s minute ventilation
57. In order to eliminate leaks in an alert patient receiving intermittent positive-pressure breathing therapy, which of the following adjuncts would you try first?
58. Which of the following patient groups should be considered for lung expansion therapy using IPPB?
Patients with clinically diagnosed atelectasis who are not responsive to other therapies and patients who are at a high risk for atelectasis who cannot cooperate with other methods
59. Which of the following positions is ideal for intermittent positive-pressure breathing therapy?
60. What are appropriate initial settings for intermittent positive-pressure breathing?
Sensitivity: -1 to -2 cmHO; Pressure 10 to 15 cmH2O; Flow: moderate
61. While administering IPPB, you notice that the device will not cycle off, even when you occlude the mouthpiece. What would be the most appropriate action to take?
Check the circuit for leaks
62. What is the minimum airway pressure at which the esophagus opens, allowing gas to pass directly into the stomach?
63. Which of the following will make an IPPB device cycle off prematurely?
Airflow obstruction, kinked tubing, occluded mouthpiece, and active resistance to inhalation
64. What is an absolute contraindication for using intermittent positive-pressure breathing?
65. During the administration of a continuous positive airway pressure through a mask to a patient with atelectasis, you find it difficult to maintain the prescribed airway pressure. Which of the following is the most common explanation?
System or mask leaks
66. Which of the following is NOT a potential contraindication for intermittent positive-pressure breathing?
67. Which of the following are potential desirable outcomes of IPPB?
Improved oxygenation, increased cough and secretion clearance, improved breath sounds, and reduced dyspnea
68. The general assessment for IPPB should include which of the following?
Measurement of vital signs, appearance and sensorium, and chest auscultation
69. What is the most common complication associated with IPPB?
70. Which of the following should be charted in the patient’s medical record after completion of an intermittent positive-pressure breathing treatment?
Results of pre-and post-treatment assessment, any side effects, and succinct but complete account of the treatment session
71. Which of the following are contraindications for continuous positive airway pressure (CPAP) therapy?
Hemodynamic instability, hypoventilation, and facial trauma
72. Which of the following are appropriate volume goals for IPPB?
10 to 15 mL/kg and at least 30% of the inspiratory capacity (IC)
73. Prior to starting IPPB on a new patient, what should the practitioner explain?
Why the physician ordered the treatment, what the treatment will do, how the treatment will feel, and what the expected results are
74. Which of the following are potential complications of CPAP therapy?
Barotrauma, gastric distention, and hypercapnia
75. Which of the following is FALSE about gastric distention with IPPB?
Gastric distention is a relatively harmless effect of IPPB.
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76. Which of the following mechanisms probably contribute to the beneficial effects of CPAP in treating atelectasis?
Recruitment of collapsed alveoli, decreased work of breathing, improved distribution of ventilation, and increased efficiency of secretion removal
77. What is the optimal breathing pattern when using IPPB for the treatment of atelectasis?
Slow, deep breaths held at end-inspiration
78. Which of the following modes of lung expansion therapy is physiologically most normal?
79. Which of the following are essential components of a CPAP system?
Blended source of pressurized gas, breathing circuit with reservoir bag, low-pressure or disconnect alarm, and expiratory threshold resistor
80. Intermittent positive-pressure breathing is associated with what?
81. While administering intermittent positive-pressure breathing therapy, which of the following breathing patterns would be most desirable?
6 to 8 breaths/min with an I:E ratio of 1:3
82. The administration of IPPB should include which of the following?
The evaluation of alternative approaches to the patient’s problem, setting specific and individual clinical goals or objectives, and conducting a baseline assessment of the patient
83. What do large negative pressure swings during inspiration indicate when IPPB is being administered?
84. When adjusting the sensitivity control on an intermittent positive-pressure breathing device, which of the following parameters are you changing?
The effort required to cycle the device on
85. When you decrease the flow during IPPB, what happens to the inspiratory time?
86. What are the two types of atelectasis?
Passive and resorption
87. What is passive atelectasis?
It is the result of shallow breathing and is caused by the persistent use of small tidal volumes.
88. Passive atelectasis can occur with what?
Surgery medications, neurological disorders, neuromuscular weakness, bed rest, and immobility
89. Resorption atelectasis is the result of what?
It results from an airway obstruction (e.g., mucus plugs).
90. What is lobar atelectasis?
When an entire lobe of the lung has atelectasis
91. What factors cause atelectasis?
Obesity, neuromuscular disease, sedation, surgery, spinal injury, bedridden immobility, and a decreased cough
92. What are the clinical signs of atelectasis?
Decreased breath sound with crackles, tachycardia, tachypnea, cyanosis, hypoxemia, and increased opacity on a chest x-ray
93. Lung expansion therapy increases lung volumes by increasing what?
The transpulmonary pressure gradient
94. What happens if the transpulmonary pressure gradient is increased?
The lungs expand more
95. How does incentive spirometry work?
It increases the transpulmonary pressure gradient by lowering the pleural pressure. It is the most effective type of lung expansion therapy because it mimics the normal physiology of breathing.
96. How does IPPB work?
It increases the transpulmonary pressure gradient by increasing the alveolar pressure.
97. How do you know which lung expansion therapy method to choose?
It depends on the needed equipment, personnel, risk, and cost.
98. How does incentive spirometry mimic natural sighing?
By encouraging slow, deep breathing
99. Is IPPB used for short-term or long-term therapy?
100. How frequently can IPPB be administered?
It can be administered several times a day or as frequently as once per hour.
101. What does IPPB require?
It requires a spontaneously breathing patient.
102. What are the four IPPB interfaces?
Mask, flange, trach adapter, and mouthpiece
103. What is the Bird Mark 7?
It is the most common type of IPPB that is pneumatically powered.
104. What are the IPPB controls?
Pressure, flow, sensitivity, air mix control, and apnea timer
105. Which of the following situations is a contraindication for incentive spirometry?
A patient with a vital capacity that is less than 10 ml/kg and a patient who cannot cooperate or follow instructions (e.g., unconscious patient)
106. Which of the following conditions is most likely to predispose a patient to atelectasis?
107. When should high-risk surgical patients be oriented to incentive spirometry?
Before the surgical procedure
108. A patient complains of numbness around his lips during IS. What should the therapist recommend?
Tell the patient to slow their breathing rate
109. Physical signs of atelectasis that involves a significant portion of the lungs include:
Decreased or bronchial/tubular breath sounds, tachypnea, and tachycardia when hypoxemia is present
110. In teaching a patient to perform the sustained maximal inspiration maneuver during incentive spirometry, what would you say?
“Exhale normally, then inhale as deeply as you can, then hold your breath for 5 to 10 seconds.”
111. A postoperative patient using incentive spirometry complains of dizziness and numbness. What is the most likely cause of these symptoms?
112. Which of the following is FALSE about flow-oriented incentive spirometry devices?
They have proved less effective than volumetric systems.
113. Which of the outcomes would indicate improvement in a patient previously diagnosed with atelectasis who has been receiving incentive spirometry?
Improved PaO2, decreased respiratory rate, and improved chest radiograph findings
114. Persistent breathing at small tidal volumes can result in which of the following?
115. Correct instruction in the technique of incentive spirometry should include which of the following?
Diaphragmatic breathing at slow to moderate flows
116. Lung expansion therapy works because of an increase in what pressure gradient?
117. How often should a patient perform incentive spirometry?
118. Lung expansion methods that increase the transpulmonary pressure gradients by increasing alveolar pressure include which of the following?
Positive end-expiratory pressure therapy, intermittent positive-pressure breathing (IPPB), and expiratory positive airway pressure (EPAP)
119. In observing a postoperative woman conduct incentive spirometry, you note the repetitive performance of the sustained maximal inspiration maneuver at a rate of about 10 to 12/min. Which of the following would you recommend?
Take a 30-second rest between breaths
120. Which of the following patient categories are at a high risk for developing atelectasis?
Those who are heavily sedated, those with upper abdominal or thoracic pain following surgery, and those with neuromuscular disorders
121. Which of the following is not a potential hazard or complication of incentive spirometry?
Decreased cardiac output
122. How do all modes of lung expansion therapy aid in lung expansion?
By increasing the transpulmonary pressure gradient
123. When does acute respiratory alkalosis occur during incentive spirometry?
When the patient is breathing too quickly
124. An alert, cooperative 28-year-old female with no prior history of lung disease, underwent a cesarean section, and her x-ray film is clear. Which of the following approaches to preventing atelectasis would you recommend?
125. The successful application of incentive spirometry depends on what?
The effectiveness of patient teaching
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126. How can the transpulmonary pressure gradient be increased?
By increasing the alveolar pressure or decreasing the pleural pressure
127. Incentive spirometry devices can generally be categorized as which of the following?
Flow-oriented or volume-oriented
128. Which of the following is not at high risk for developing postoperative atelectasis?
Those with a non-smoking history
129. What is the pressure setting for IPPB?
130. What would you increase during IPPB to increase the patient’s tidal volume?
The pressure setting
131. If the patient can’t trigger an IPPB breath and the manometer needle is not moving off of the zero mark, what would you expect?
The patient is breathing through their nose
132. What is a device for lung expansion that requires negative transpulmonary pressure?
133. What is an ideal I:E ratio when delivering IPPB?
An I:E ratio with a higher expiratory time
134. What is the purpose of EzPAP?
It helps with the prevention and treatment of atelectasis for lung expansion therapy, and it is recommended for patients with a decreased FRC.
135. What are some adverse reactions that occur with EzPAP?
Increased work of breathing that may lead to hypoventilation, increased intracranial pressure, cardiovascular compromise, decreased venous return, air swallowing, and pulmonary barotrauma
Lung expansion therapy is an essential part of respiratory care as it provides multiple effective strategies for treating and preventing atelectasis.
The techniques work to improve lung function by expanding the lungs and increasing alveolar ventilation. As a respiratory therapist, it’s important to develop an understanding of each of the different types. Hopefully, this guide can make the learning process easier for you.
We have a similar guide on medical gas therapy that I think you’ll find helpful. Thanks for reading and, as always, breathe easy, my friend.
John Landry, BS, RRT
John Landry is a registered respiratory therapist from Memphis, TN, and has a bachelor's degree in kinesiology. He enjoys using evidence-based research to help others breathe easier and live a healthier life.
- Egan’s Fundamentals of Respiratory Care. 12th ed., Mosby, 2020.
- Mosby’s Respiratory Care Equipment. 10th ed., Mosby, 2017.
- Wilkins’ Clinical Assessment in Respiratory Care. 8th ed., Mosby, 2017.
- Clinical Manifestations and Assessment of Respiratory Disease. 8th ed., Mosby, 2019.
- “Effects of Lung Expansion Therapy on Lung Function in Patients with Prolonged Mechanical Ventilation.” National Library of Medicine, 2016, www.ncbi.nlm.nih.gov/pmc/articles/PMC4904515.
- “Impact of Lung Expansion Therapy Using Positive End-Expiratory Pressure in Mechanically Ventilated Patients Submitted to Coronary Artery Bypass Grafting.” National Library of Medicine, pubmed.ncbi.nlm.nih.gov/31545577.