Review of Respiratory Medicine - Volumen 22, Número 4 - December 22

Review Article

Whole Lung Lavage Protocol at Hospital Santa Clara of Bogotá: Presentation of a Patient with Resistant Pulmonary Alveolar Proteinosis

Protocolo de lavado pulmonar total del Hospital Santa Clara de Bogotá, a propósito de una paciente con proteinosis alveolar pulmonar resistente

Autor Osejo-Betancourt, Miguel1, Moreno-Ramírez, Carlos Ernesto2, Chaparro-Mutiz, Pedro3

1Specialist in Internal Medicine, Universidad Nacional Autónoma de Honduras, and in Pulmonology, Hospital Santa Clara, Bogotá, Colombia. 2Specialist in Epidemiology and Resident in Internal Medicine, Hospital Santa Clara, Bogotá, Colombia 3Specialist in Internal Medicine and Pulmonology, Hospital Santa Clara, Bogotá, Colombia.

Correspondencia : Miguel Osejo Betancourt. E-mail:


Pulmonary alveolar proteinosis is a clinical entity characterized by the accumulation of proteinaceous material, rich in surfactant, mediated by reduced clearance by alveolar macrophages. In adult patients, it is commonly associated with autoimmune phenomena resulting in a deficiency of the granulocyte-macrophage colony stimulating factor, which implies alterations in cell maturation and dysfunction, causing a decrease in surfactant degradation and its accumulation in the alveolar space. Its diagnosis poses a challenge to the clinician, based on the findings of pulmonary function tests and the crazy paving pattern of the high-resolution computed tomography of the chest, and is confirmed by obtaining the proteinaceous material in the bronchoalveolar lavage. Given its rarity, the ideal treatment remains to be elucidated, with whole lung lavage currently being the cor­nerstone of treatment. We report an anecdotal case of a 41-year-old female patient suf­fering from pulmonary alveolar proteinosis since 2011, who has required multiple whole lung lavages, with poor response to these, with persistent dyspnea and supplemental oxygen requirement even though she has performed the procedure, but with a progres­sive tendency towards improvement in the last 2 years. The lavage technique is not com­pletely standardized and its use in Latin America is still limited, which is why we publish the protocol used in the Hospital Santa Clara of Bogotá, Colombia.

Key words: Pulmonary alveolar proteinosis; Pulmonology; Protocol; Whole lung lavage; Rare diseases


La proteinosis alveolar pulmonar es una entidad clínica caracterizada por la acumula­ción de material proteinaceo, con alta riqueza en surfactante, mediado por una menor aclaración por parte de los macrófagos alveolares. En pacientes adultos, comúnmente se asocia a fenómenos autoinmunes que tienen como resultado una deficiencia del factor estimulante de colonias de granulocitos y macrófagos, lo que implica alteracio­nes en la maduración y disfunción celular, lo que provoca disminución de la degrada­ción del surfactante y su acumulación en el espacio alveolar. Su diagnóstico corres­ponde a un reto para el clínico, sobre la base de los hallazgos en pruebas de función pulmonar, el patrón en “empedrado” (crazy paving) en la tomografía computarizada de tórax de alta resolución y que se confirma al obtener el material proteínico en el lavado broncoalveolar. Dada su rareza, el tratamiento ideal permanece por ser elucidado y en la actualidad el pilar del tratamiento es el lavado pulmonar total. Reportamos un caso anecdótico de una paciente de 41 años con proteinosis alveolar pulmonar desde 2011, que ha requerido múltiples lavados pulmonares totales, con pobre respuesta a estos, persistencia de disnea y necesidad de oxígeno suplementario a pesar de realizar el procedimiento, pero con tendencia progresiva a la mejoría en los últimos 2 años. La técnica del lavado no está completamente estandarizada y su uso en América Latina es aún limitado, por lo que publicamos el protocolo utilizado en el Hospital Santa Clara de Bogotá, Colombia.

Palabras clave: Proteinosis alveolar pulmonar; Neumología, Protocolo; Lavado pulmonar to­tal; Enfermedades raras

Received: 12/20/2021

Accepted: 8/5/2022


Pulmonary alveolar proteinosis (PAP) is a pul­monary disease caused by the accumulation of surfactant in the alveolar space mediated by a reduced clearance by alveolar macrophages. It was first described in 1958 by Rosen et al.1, 2

The altered macrophage function is the effect of the reduced availability of the granulocyte-macrophage colony stimulating factor (GM-CSF) mediated by the production of autoantibodies against this protein in up to 90% of adult patients. Other causes include mutations in the GM-CSF receptors, hematologic disorders, infections, drugs and exposure factors (silica, cellulose, heavy metals and some organic materials).1

PAP symptoms are non-specific, with progres­sive dyspnea as the main symptom. Lung function tests show reduced diffusing capacity of the lungs for carbon monoxide (DLCO), and the spirometry might show a restrictive pattern.3 The high-reso­lution chest tomography (HRCT) shows the crazy paving pattern, with ground glass opacities super­imposed on interlobular septal thickening that is characteristic of this condition, though it may also be present in other diseases, and in the cases of autoimmune etiology, the presence of antibodies against GM-CSF confirms the diagnosis.4-6

The diagnosis must be confirmed through bronchoalveolar lavage collecting whitish, milky proteinaceous material with precipitating amor­phous detritus; the microscopy showing oval, acel­lular bodies, basophilic in May-Grünwald-Giemsa Stain and positive for PAS (Periodic acid Schiff) staining.1, 7

The treatment includes smoking cessation and vaccination against influenza and pneumococcus for the prevention of respiratory infections. The cornerstone of treatment for symptomatic patients with reduced vital forced capacity (VFC), reduced DLCO or hypoxemia is whole lung lavage. At pres­ent there are other treatments such as inhaled or subcutaneous GM-CSF, and for treatment-refractory patients, additional interventions may be used, such as the use of rituximab, plasmapher­esis or lung transplantation, with studies of highly variable results.1, 8-10

Since it is a rare disease, there aren’t any ran­domized clinical studies that standardize the whole lung lavage technique; there are some descriptions in languages other than Spanish and modifications in accordance with the Center’s experience, with­out any established protocols in Latin America. Taking that into consideration, the objective of this review was to describe the protocol for the whole lung lavage procedure that has been followed in the Hospital Santa Clara of Bogota, which has been used for the treatment of several PAP patients in that institution; and in comparison with the techniques described in the literature review, we will briefly describe the experience of one case that was refractory to treatment.


Female patient, 41 years old, who presented to the institution in 2011 with chronic dyspnea. Chest tomography showed crazy paving pattern (Figure 1). A bronchoscopy was performed and proteinaceous material was collected. Gram, Ziehl Neelsen and Grocott stains were performed, as well as cultures for bacteria, mycobacteria and fungi, all with negative results but with PAS-positive stain­ing. PAP diagnosis was confirmed through clinical symptoms, tomography, lavage findings, and PAS-positive staining, without the need to perform a biopsy. The patient proceeded with the whole lung lavage in the Pulmonology Department, with unsatisfactory evolution, even though she had per­formed multiple procedures. The patient showed a partial response, and required lung lavages every 6 months on average, 26 lung lavages in total (13 right, 13 left) since she was first treated at the in­stitution; and the protocol described in Table 1 was followed at all times. No complications occurred during the procedure; during the postoperative period, she only had some isolated fever spikes. The patient presented pulmonary hypertension, with a 2018 echocardiogram showing calculated pulmonary artery systolic pressure (PASP) of 70 mmHg. In September 2020, she went to the emer­gency department with exacerbation of respiratory symptoms, no fever, oxygen saturation of 65% on admission, and the last lung lavage having been done in August 2019. Once SARS-CoV-2 infection was discarded, a new lung lavage was scheduled. During the lung lavage, a thick, yellowish protein­aceous material was obtained (Figure 2), and then washed with 25 L. As there were no complications, a new lavage was scheduled for the following week, and was also performed without complica­tions. The patient was discharged with clinical improvement, saturation 90% on supplemental oxygen. She reported significant improvement with a few symptoms. New control echocardiogram in April 2021; PSAP of 20 mmHg reported with normal systolic function. The dyspnea improved and as regards the functional limitation, she no longer required oxygen for daily activities (it was necessary only at night). She was admit­ted on November 2021 with dyspnea class 2 according to the mMRC (Modified Medical Research Council) scale, saturation 88% on room air. Control chest X-ray (Figure 3) show­ing bibasilar alveolar opacities with significant improvement compared to previous tests. New whole lung lavage scheduled. Lavage performed in two sessions; the second one, with 20 L. Fluid cleared completely (Figure 4) for the first time in this patient. PAS staining requested (Figure 5) in the last lavage. There weren’t any complications and the patient was discharged without symptoms, with saturation 91% without supplemental oxygen. She had a follow-up plan for external consultation, with tomographic control and new echocardiogram to confirm previous findings.

Figura 1. TACAR inicial: Antes del primer lavado; se observa el patrón de «empedrado» de opa­cidades en «vidrio esmerilado» sobrepuestas a un engrosamiento septal interlobulillar.
Table 1. Whole lung lavage protocol


Figure 2. 2020 lung lavage: thick, yellowish proteinaceous material, which cleared during the procedure.


Figure 3. Initial HRCT: before the first lavage; crazy paving pattern with ground glass opacities superimposed on interlobular septal thickening.


Figure 4. 2021 lung lavage: slightly pink proteinaceous material that cleared completely at the end of the procedure.


Figure 5. PAS staining: photography taken with the microscope with 100x magnification. Amor­phous material observed that stained pink. Courtesy of Dr. Constanza Franco and Dr. Diana Caballero, Pathology Service, Hospital Santa Clara.


A narrative review was performed of the bibli­ography using the PubMed, Google Scholar and ScienceDirect databases between January 1st, 2014 and September 30th, 2021. Also, the search of relevant bibliography was complemented with the review of the references of articles selected by the authors. For the bibliography search we used the MeSH Terms and selected the following as key words: «whole lung lavage» and «pulmonary alveolar proteinosis» and their combinations, using AND and OR as Boolean operators.


When searching and writing the summary of the bibliography, articles were selected according to the preferences of the topic to be discussed, includ­ing review articles, case reports, guidelines and protocols, observational studies and clinical trials.


In 1953, Dr. Benjamin Castle described a patient with alveolar filling of proteinaceous material stained with PAS staining, and in the following 5 years accumulated 27 patients with the same findings, making the first report about this new disease which subsequently received the name of pulmonary alveolar proteinosis. It is a progressive, fatal disease with no suitable treatment, for which many therapies have been tested with unfavorable results.11 In 1963, Dr. José Ramírez Rivera used a transtracheal catheter placed in one lung at a time and instilled 100 ml saline solution aliquots at 50-60 drops per minute, four times a day, 2 to 3 times a week which, despite being a stressful and long process, improved the opacities in the radiological images, the oxygenation and DLCO.11 In 1964, he used a double lumen tube to instill 3 L of saline solution to an isolated lung together with heparin or N-acetylcysteine and showed that the instillation of large volumes is a safe procedure. During the following decades, the procedure has been perfected and the whole lung lavage as we know it today was first described in 1994.12

Indications and contraindications

The main indication is considered to be dyspnea with functional limitation, worsening of radiologi­cal images and hypoxemia.9, 11 The use of other clin­ical and paraclinical parameters to define whether or not a lavage should be performed is variable according to the experience of each center, and other causes of hypoxemia should be discarded, for example pulmonary embolism or infection.12

The main contraindications to the procedure include severe heart disease, findings of pulmo­nary fibrosis or sepsis.13 It is not recommended for patients with untreated coagulopathy, especially in cases of thrombocytopenia with platelet count below 50 000 /mm³ or an INR (International Nor­malized Ratio) of more than 1.5; however, given the rarity of this condition, there aren’t any ran­domized studies that guide the procedure, thus explaining the high variability of the different institutions.11

In most centers, lung lavage is preferably car­ried out in two sessions (one for each lung), with 1-3 weeks in-between sessions; however, cases have been reported of bilateral lung lavages performed in only one session.11 Most patients will require separate lung lavages, and even a considerable number of patients will require only one proce­dure to reach spontaneous remission; that is why it is preferred as first-line treatment in contrast to the administration of GM-CSF, which is more expensive and not easily available in most Latin American countries.9, 12

The objective of lung lavage is to remove as much proteinaceous material as possible, hav­ing instilled the least amount of solution, while reducing complications related to anesthesia and post-procedure hospitalization.


We suggest a suitable preanesthetic assessment including pulmonary function tests and radio­graphic control, and during the visit, advice should be given on the management of the airway and of the double-lumen endotracheal tube.9, 12

For the induction and maintenance of anes­thesia use endovenous anesthetic agents to avoid leakage during the lavage and contamination of the area, with fluid restriction to avoid fluid overload, continuous hemodynamic monitoring, arterial gasometry and a patient warming device so as to prevent hypothermia, especially in patients with unstable cardiovascular disease.14, 15 In patients with significant polycythemia, a phlebotomy could be considered before the procedure to reduce the risk of thromboembolic complications.12

Protocol description

The procedure is carried out in the operating room by trained staff including a pulmonologist, respi­ratory therapy and an anaesthesiologist.11, 12 It is done with general anesthesia with neuromuscular blockade, using a left double-lumen tube (because the placement of the right tube is more complicated and might obstruct the bronchus of the upper lobe). There must be an air column at both ends, and generally the anesthesiologist does resistance tests to verify the position of the tube, which is then confirmed with the bronchoscopy; this step is fundamental for the procedure.8, 11, 12, 14, 16

The procedure is carried out in supine position because it is more comfortable and to prevent the double-lumen tube from moving out of its place, a common complication of this procedure. Some authors report cases of the procedure being performed with the patient lying on a side, in the direction of the lung to be washed, to reduce the probability of leakage towards the contralateral lung.11, 12

The lung to be washed is selected with the sup­port of radiological images and confirmed during the procedure with the evaluation of lung compli­ance: the most affected lung is the least compliant. After the intubation, denitrogenation of both lungs is carried out to avoid the formation of bubbles during the procedure through the administration of a fraction of inspired oxygen (FiO2) of 100% for 5-15 min. During that time, the saline solution is heated to 37 °C to reduce hypothermia, and approximately 20 L - 40 L are prepared for the procedure.8, 11, 12, 14, 16 A closed system is prepared with the Y-shaped connector, with one end con­nected to the saline solution bags and the other one to the double-lumen tube towards the side of the lung to be washed, and the other one, to the drainage system.14 When it is ready, the instilla­tion of the first aliquot begins slowly to avoid the formation of bubbles and barotrauma, until the pressures are equal and no more liquid enters the system.14 The inlet valve is closed and the drain valve is opened (it may or may not be connected to a suction system). The drain valve can be opened immediately after finishing the instillation of the solution, because it seems to be as effective as keeping it for a few minutes, and apparently it reduces absorption to the systemic circulation and secondary hypervolemia.12

Once the drainage has begun, chest percus­sion is carried out to facilitate the mixture of the proteinaceous material with the instilled solution. Percussion can be carried out with kinesiotherapy or percussion equipment, like the one we use in our center, but it can also be administered manu­ally. If done manually, it is exhausting for the staff and the patient complains of more pain after the procedure.11, 12 The first drained material will be whitish and milky, or from yellowish to reddish if there are microhemorrhages, and will clear while aliquots are instilled.

The procedure is repeated with aliquots of 1000 ml on average, the flow rate being deter­mined by the infusion system, and performing the percussion only during drainage. The amount of fluid entering and leaving the system must be strictly calculated and monitored; drips of more than 1000 ml might indicate system leakage to­wards the contralateral lung or the pleural space.8, 14 This could occur if the double-lumen tube moves out of its place, and it could be necessary to replace it and confirm with a new bronchoscopy; that is why it is important to pay attention to bubbles going out from the contralateral lumen.8, 14

Cycles will be repeated until the fluid drainage is as clear as possible. On average, most patients need 20 L per procedure and may require up to 40 L.17

Physiological changes during whole lung lavage

During the filling phase, blood is physiologically sent from the non-ventilated lung to the ventilated one due to hypoxic pulmonary vasoconstriction and pressure changes induced by the instillation of the solution. This change in the physiological shunt results in higher oxygenation, since the he­moglobin saturation increases and, once drainage is completed, oxygen saturation decreases again as a consequence of airway pressure drop and pulmo­nary perfusion towards the non-instilled lung.17 In addition, fluid overload during the filling phase might increase pulmonary vascular resistance, thus causing right ventricular overload, especially in patients with pulmonary hypertension or left ventricular dysfunction.14

Post-procedure care

Once the procedure is completed, the remaining liquid is absorbed from the lung. Then, ventilation and recruitment of both lungs are carried out. If liquid is observed coming out from the tube, it is absorbed. Subsequently, the lung that has been washed is recruited and liquid is absorbed as needed.12, 14, 16

It is important to remember that drained proteinaceous material is pulmonary surfactant lost during lavage, even the amount necessary to maintain surface tension is lost, thus facilitating alveolar collapse; that is why post-lavage recruit­ment is routinely done.11, 12

Taking into account the patient’s conditions, extubation can be an option and transferring the patient to the Intensive Care Unit to be surveilled during 12 to 24 hours. Patients with severely com­promised oxygenation or hemodynamic instability are recommended to replace the double-lumen tube with a conventional orotracheal tube after the procedure and continue postoperative manage­ment in the Intensive Care Unit with protective mechanical ventilation, with or without loop di­uretics, using the therapeutic strategies indicated for other causes of pulmonary edema.12

Technique variations

Some centers report the use of the bilateral proce­dure, which starts with the most affected lung and once the liquid is clear, continues with the other. It is a much longer procedure, which lasts up to 8 hours, then the orotracheal tube is replaced with a conventional one and the patient is subsequently managed in the Intensive Care Unit.11 The ad­vantage of this method is that it reduces hospital costs and the time until the patient is discharged, enhancing patient comfort earlier. Silva et al pub­lished in 2014 a series of 3 cases of bilateral lung lavage, in accordance with their specific protocol.16

There are also some reports of PAP patients with respiratory failure who didn’t tolerate single-lung ventilation, so in those cases the procedure was performed with extracorporeal membrane oxygenation.9, 11, 15, 16

Microbiological studies of drained material can be conducted to study Nocardia, Actinomyces, mycobacteria and fungi, such as Aspergillus and Cryptococcus, because, given the dysfunction of alveolar macrophages, there is predisposition towards these infections.17

The use of dynamic ultrasound imaging has also been reported to guide the procedure and ob­serve the way in which lung echogenicity changes, from being ventilated to achieving a consolidation pattern after the solution has been instilled or evidencing complete atelectasis after drainage. Echocardiographic guideline could reduce pul­monary stress and help prevent volutrauma and barotrauma, and also check for fluid leaks.18

Since 1988, Bingisser et al described the use of manual ventilation during the procedure, and in 2012, Bonella et al added intermittent percussion (both for instillation and drainage) as a strategy to recruit a larger amount of proteinaceous mate­rial during the procedure with the least amount of solution.19 In 2021, Grutters et al modified the Bonella technique and performed manual hyperin­flation every 3 aliquots, with intermittent percus­sion. So, they found that the amount of solution necessary for performing the lavage was reduced, with an average of 15 L with the largest amount of drained material (91%) after 3 cycles with this maneuver.19

The work of Akasaka et al in 2014 designed a mathematical model to predict the number of pro­teins that were going to be removed during lung lavage, for the purpose of predicting or modifying filling and drainage times. However, the calcula­tion didn’t modify the number of cycles or liquid retention time, compared to the standard treat­ment, and the measurements of different proteins would increase procedure costs.20

There is a report of a patient with a bad re­sponse to lavage, similar to our patient, that used treatment combination, lung lavage with cycles of inhaled GM-CSF after the procedure for up to 6 months, showing evident improvement; but this pharmacological intervention isn’t easily available and its cost limits its administration significantly, like in the case reported in this article.21

Segmental lavages are also performed through flexible bronchoscopy in patients who don’t toler­ate single lung ventilation or pediatric patients, but with lower fluid volumes and reduced effi­cacy.13, 22

Follow-up and efficacy

Given the heterogeneous condition of this disease, improvement of the various clinical parameters is different and variable. In 2015, a retrospective study was carried out of 120 PAP adult patients in China, 80 of which required lung lavage; they were followed-up for 8 years and after the procedure, the oxygen arterial pressure (PaO2), FVC, total lung capacity, DLCO and distance travelled in the 6-Minute Walk Test (6MWT) all improved: the most significant changes occurred in the DLCO, with an average increase of 10 points, and in the 6MWT, with an average of 100 m, without any dead patients in the follow-up period.23

In 2016, a meta-analysis was published evaluat­ing the efficacy of the lavage; it included twelve studies and reported significant improvement in the DLCO, FVC, PaO2 and forced expiratory vol­ume on the first second (FEV1), with no changes in the arterial pressure of the carbon dioxide or the arterial oxygen saturation.24

Another 2020 report of 10 patients in India showed clear improvement in oxygenation, but only stabilization or mild improvement in the other parameters of lung function.25 Another report of fifty lung lavages conducted in a reference center in Thailand showed improvement in oxygenation, DLCO, and radiographic findings, with 42% of patients showing partial improvement and 47% complete improvement after the procedure.26

It has also been found that smoking alters the efficacy of the procedure, that is why in smokers more lavages were necessary to achieve disease remission or stabilization.17 Survival after the procedure ranges from 63% to 94%, so it is part of the cornerstone of treatment of PAP patients.17, 26


The most frequently reported complications are: fever (18%), hypoxemia (14%), sibilance (6%), pneumonia (5%), fluid leakage (4%), pleural effu­sion (3.1%) and pneumothorax (0.8).9, 11, 13, 27 Hy­poxemia is particularly relevant, and is related to hospital readmission within 30 days following the procedure in up to 5% of the cases, with patients re­quiring treatment with high FiO2 and recruitment with positive end-expiratory pressure (PEEP), trying to avoid barotrauma (pneumothorax).11, 28 Exacerbation of the symptoms was also reported within the first 30 days following the procedure, together with respiratory infections, though there was no association with opportunistic infections.17, 28 Bad positioning of the double-lumen tube may cause fluid leakage towards the other lung, but this rarely occurs with highly-trained professionals and after confirmation with bronchoscopy. The rapid instillation of large volumes might cause baro­trauma with hydropneumothorax or significant pleural effusion, which could require management with chest tube or thoracentesis.8, 11

Another important effect is hypothermia. Body temperature should be monitored using physical media and the aliquots should be heated before instillation, thus avoiding the appearance of in­traoperative arrhythmia and other hypothermia-derived complications.8

It has been reported that up to 10% of patients resist whole lung lavage, with no significant im­provement, and require more lavages plus other treatments.23 Our patient is included in that group, though she has shown evident clinical improve­ment in the last 2 years of treatment.


Pulmonary alveolar proteinosis is a rare disease, generally unknown to primary care physicians. This situation could delay the diagnosis and, even though there are several treatment alternatives, these are expensive and not easily available for most Latin American countries. Cases have been reported of patients who respond to treatment with stimulating factors, but whole lung lavage is still the treatment standard and although the pro­cedure is expensive, it is cost-effective, given the rapid improvement of the patient and long-term maintenance. However, the procedure remains largely unknown, and many physicians are afraid to use it due to the already mentioned implica­tions, and the need for specific supplies, such as the double-lumen tube, and of staff trained in the procedure and perioperative management; this indicates that it is necessary to standardize some therapeutic strategies. For that reason, we decided to write this protocol for the purpose of simplify­ing the available information, with an approach that can be easily replicated in most of the Latin American territory.

Conflicts of interest

The authors have no conflict of interest to declare in rela­tion to writing or publishing this article.


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