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The Value and Complications of Percutaneous Transthoracic Lung Aspiration for the Etiologic Diagnosis of Community-Acquired Pneumonia^*

J. Anthony G. Scott, BM, BCh and Andrew J. Hall, BM, BS

^* From the Infectious Disease Epidemiology Unit (Dr. Hall), London School of Hygiene and Tropical Medicine, London, UK; and Wellcome Trust/Kenya Medical Research Institute (Dr. Scott), Centre for Geographic Medicine Research–Coast, Kilifi, Kenya. Currently at Center for Disease Control and Prevention, Atlanta, GA.

Correspondence to: J. Anthony G. Scott, BM, BCh, Wellcome Trust/Kenya Medical Research Institute, Centre for Geographic Medicine Research-Coast, PO Box 230, Kilifi, Kenya; e-mail: Ascott{at}kilifi.mimcom.net

Key Words: etiology • lung puncture • pneumonia • pneumothorax • sensitivity and specificity

	Introduction

TOP Introduction Materials and Methods The Technique Historical Perspective Specificity: Bacteriology of the... Causes of False-Positive Results Sensitivity and Diagnostic Yield Causes of False-Negative Results Complications Investigation of Pneumonia in... Safe Conduct of Lung... Uses of Lung Aspiration References

 
Diagnosis of pneumonia is frustratingly incomplete, with most large studies failing to identify a causative organism in 33 to 45% of patients.^{1 2 3} Diagnosis by blood culture is highly specific, but the sensitivity of blood cultures for bacterial pneumonia is < 25%. An etiology can be obtained in undiagnosed cases by culture of sputum or from serologic diagnoses, but these techniques lack specificity or produce an unconvincing description with multiple pathogens.^{4 5 6} The most convincing evidence of etiology in observational studies of acute pneumonia is the demonstration of a single pathogen in the diseased tissue of the patient and the absence of this same organism from equivalent tissue in healthy control subjects. Percutaneous transthoracic aspiration of "lung juice" is the most acceptable and uncontaminated means of describing the microbiology of pneumonic lung antemortem, but the technique is not widely practiced because of the potential for adverse events. Here, we review the existing data on both the etiologic yield and the frequency of complications in order to evaluate the role of lung puncture in modern diagnostic studies.

	Materials and Methods

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Pertinent studies were identified by a search of the National Library of Medicine MEDLINE database examining all fields for the phrases "lung aspiration," "lung puncture," "lung suction," and "lung tap," and extending retrospectively through secondary, tertiary, and quaternary citations. At the outset, a distinction was drawn between lung aspiration, in which a small, fine-gauge needle is used to diagnose pneumonia, and needle biopsy, in which a longer, thicker needle is used to diagnose malignant or inflammatory focal lung lesions under fluoroscopic or CT guidance.⁷

	The Technique

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After sterilizing the skin, a 20- or 25-gauge needle is attached to a 10-mL syringe and inserted immediately above a rib to the depth of the parietal pleura. While the patient suspends respiration, the needle is pushed rapidly 2 to 3 cm into the consolidated lung, and suction is applied as the needle is steadily withdrawn. The procedure is so quick that it is unnecessary to anesthetize the skin or pleura.⁸ Nonetheless, local anesthetic is used by some authorities to prevent rapid movements of the chest wall in response to pleuritic pain,⁹ and premedication with atropine is practiced by others.^{10 11}

The aspirate, also known as lung juice, lung fluid, or pulmonary exudate, usually has a volume of < 0.5 mL and is expelled by in-and-out movements of the syringe plunger after the needle tip is immersed in broth. A common variant of the technique is to prime the syringe with 0.5 mL of sterile isotonic saline solution and inject this into consolidated lung to increase the volume of the aspirate, although this has not been proven to increase diagnostic yield.⁹ Because preservatives used in clinical supplies of saline solution or buffer may inhibit the growth of bacteria, the results may be improved by using an alternative lavage such as sterile culture broth.¹² Occasionally, the patient will have a small laminar pleural effusion, and a larger volume of aspirate will be obtained as the tip of the needle is withdrawn through the pleural space.

Most commonly, a 21-gauge, 35-mm venipuncture needle is used,¹³ but needles as short as 20 mm¹⁴ or as long as 150 mm¹⁵ have been used on children. Some investigators insert a guide needle to the pleura,^{16 17 18 19} while others use a 22-gauge lumbar puncture needle with a stylet.²⁰ Normally, only one pleural puncture is attempted, but several investigators have repeatedly withdrawn and replunged the needle inside the lung parenchyma to increase the volume of lung juice to 1 to 3 mL,^{20 21} and others have conducted prolonged suctions over 30 s.^{10 11}

Pulmonary consolidation is localized by radiographs in two planes, and is refined by clinical examination, selecting the area of most pronounced bronchial breathing.²² Some authors use the same "safe" locations for disease in any given lobe, eg, the seventh intercostal space in the midscapular line for a lower lobe puncture.^{9 23} Safe surface markings have been described for the whole thorax in children by radiology of punctured cadavers.²⁴ With longer needles (> 4 cm), there is less certainty of the course of the needle in the thorax, and material from liver or spleen has occasionally been extracted.²⁵

	Historical Perspective

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The first accounts of transthoracic percutaneous lung aspiration were published in 1883 in Germany, by Leyden²⁶ and Günther,²⁷ and in France, by Talamon.²⁸ Leyden found the same organisms in lung aspirate and blood of one patient with pneumonia but found no organisms in aspirates from two other patients. The technique was popularized in England in 1909 by Horder,²⁹ who diagnosed five out of six cases of pneumonia or lung abscess by aspiration,^{29 30} and in the United States in the 1920s by Thomas and Parker²² and Lyon,³¹ who together published > 100 cases.

Lung aspirate studies played an important part in elucidating the pathogenesis of pneumococcal pneumonia. Tchistovitch³² demonstrated that lung juice obtained from patients after crisis contained pneumococci virulent for mice and rabbits; crisis was, therefore, not dependent on the clearance of pneumococci from the lungs. From a series of 48 lung punctures at different stages of pneumonia, Rosenow¹³ deduced that the probability of finding pneumococci decreased with time in those who survived but increased with time in those who died. Lister³³ used pneumococci derived from lung aspirates to demonstrate the agglutinating power of convalescent serum from the same patient, paving the way to a strategy of vaccination with capsular antigens.

Without antibiotics or serum therapy, early lung aspirate studies were only of academic interest. Nonetheless, episodes of pneumonia were "treated" with lung puncture, with "good results"³⁴ and, in the days before controlled clinical trials, several authors noted that lung puncture itself hastened the resolution of pneumonia.^{35 36 37} With the advent of serum therapy, it became apparent that specific antiserum was most effective when given early in the course of pneumonia.³⁸ Serotyping the infecting pneumococcus became a medical emergency,⁹ and lung aspirates were used to ensure the timely and economic use of the available sera.^{36 39 40} During the 1930s, lung aspiration became a commonplace medical procedure and was reported in a wide number of scientific publications from Europe,^{36 37 39 41 42 43} the United States,^{9 15 40 44 45 46} and Africa.^{24 47 48}

In the discovery of etiologic agents, lung aspirate studies have a scientific authority that has shaped our current understanding of pneumonia etiology. Oval diplococci, presumably pneumococci, were identified in lung juice separately in 1882 by Leyden²⁶ and Günther²⁷ in Germany. In France, Netter⁴⁹ established that Hemophilus influenzae was responsible for many bronchopneumonias in children, using lung aspirates during the influenza epidemic of 1918. Staphylococcus aureus was defined as a pneumonia pathogen by lung aspirate studies performed shortly after death,⁵⁰ and Neisseria meningitidis by both postmortem⁵¹ and antemortem lung aspirates.⁵² Mycobacterium tuberculosis,⁵² respiratory syncytial virus,⁵³ Pneumocystis carinii,⁵⁴ and Nocardia⁵⁵ have all been defined as pneumonia pathogens by antemortem lung aspirate studies. Idiopathic pulmonary hemosiderosis of children, previously only found at postmortem, was also first described in life by lung puncture.⁵⁶

Postmortem lung aspiration was thought to provide uncontaminated lung material without introducing the risk of adverse events during life and was practiced widely in the early part of the 20th century.^{28 57 58 59 60} Axton and Giles⁶¹ used this technique to investigate the etiology of pneumonia in malnourished Rhodesian children. Specimens were taken within 10 min of death and were dominated by Gram-negative cultures. Overgrowth of the lungs by Gram-negative organisms is a potential hazard of postmortem material, but subsequent antemortem lung aspirate studies of malnourished African children have revealed a similar shift in the spectrum of pathogens.^{62 63} The value of postmortem cultures has diminished in the antibiotic era, where the causative organism may be obliterated by treatment, leaving only postmortem opportunistic organisms,⁶⁴ but specimens taken after death have been successfully used recently to implicate a viral etiology in children with acute respiratory infection.⁶⁵ The practical difficulty is in obtaining consent in a tactful and timely manner.

After the introduction of antibiotics, interest in lung aspiration waned. However, two factors led to its revival in recent decades: the development of antibiotic resistance and the recognition of the wide spectrum of potential respiratory pathogens. The additional diagnostic yield of lung aspiration has been used to enhance sensitivity in etiologic studies of pneumonia and to obtain live organisms for susceptibility testing.^{66 67} It has also evolved a role in the evaluation of individual patients with unresponsive or complex pneumonias,^{16 19 25 68 69} and in the detection of disease-specific end points in vaccine efficacy trials for adults⁷⁰ and children.⁷¹

	Specificity: Bacteriology of the Normal Lung

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The advantage of lung aspirate samples is that neither the instrument nor the specimen has to pass through the upper respiratory tract, trachea, or bronchi, all of which may be colonized by potential respiratory pathogens. For example, while a single pathogen is normally obtained from lung aspirate cultures, sputum specimens from the same patient frequently culture a mixture of organisms with an excess of Gram-negative bacilli.^{5 72} In healthy individuals, bacteria are detected with decreasing frequency and concentration as the respiratory tract is descended.^{73 74} Using a transtracheal approach to avoid upper respiratory tract contamination, Kalinske et al⁷⁵ were unable to culture bacteria from the tracheas of 13 healthy volunteers; Berman et al⁷⁶ found only scanty cultures in 4 of 15 tracheal aspirates from 12 normal volunteers.

Lung aspirates in 25 healthy anesthetized dogs yielded positive bacterial cultures in 3 animals, despite shaving and sterilizing the skin, giving a specificity estimate of 0.88.⁷⁷ In humans, lung tissue excised at pulmonary lobectomy has been shown to be sterile, unless the indication for surgery was an abscess.⁷⁸ Aspirates of the lung in normal healthy control subjects support this conclusion. Bacteria were cultured from none of 13 lung aspirates from normal healthy Chilean infants, but from 228 of 505 aspirates (45%) from infants with pneumonia.⁷⁹ In 10 healthy South African adults subjected to lung puncture, respiratory pathogens were absent from all cultures, although 4 yielded scanty "contaminants."²⁵

Patients with other diseases provide additional evidence. Of 16 aspirates from Spanish adults with suspected pneumonia who later received diagnoses of pulmonary embolism, pulmonary edema, or malignancy, only 1 specimen cultured a microorganism, Candida parapsilosis, a likely opportunistic pathogen in an immunocompromised patient.⁸⁰ Cultures of 10 lung aspirates from children with suspected tuberculosis (TB) were negative for conventional respiratory pathogens.⁸¹ Taken together, the evidence suggests that the normal lung rarely contains sufficient organisms to produce a significant culture in lung aspirates, and the specificity of the technique in pneumonia is likely to be very high.

	Causes of False-Positive Results

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A false-positive result implies culture of an organism in a lung aspirate that is not responsible for the episode of pneumonia being investigated. There are three obvious sources of false-positive results: (1) contamination of the aspirate cultures; (2) detection of infection confined to the blood stream; and (3) culture of bacteria that are not primarily responsible for the pneumonia. In lung aspirates, the frequency of skin or laboratory contamination should be similar to that of blood cultures, which is normally 1 to 3%. In the context of a radiographic pneumonia, differentiating whether an aspirate culture is derived from lung tissue or merely from the blood of a punctured vessel⁹ may seem an unnecessary distinction. However, several studies have documented different organisms in blood and lung simultaneously, and bacteremia may be a secondary consequence of severe illness rather than the primary cause of the pneumonia.^{23 31 66 82}

Secondary infection may also be established in the lung tissue itself, eg, S aureus pneumonia may be superimposed on an episode of influenza.^{83 84} The viral disease may compromise the mechanical defenses of the larynx and the clearing action of the mucociliary escalator, allowing inhalation, stasis, and growth of organisms normally confined to the pharynx. In the same manner, one bacterial infection may facilitate infection with another, and the finding of dual infection in lung aspirates may occur in as many as 25 to 40% of children with pneumonia.^{24 66} Case fatality rates in patients with dual infections are higher.¹² Although two pathogens may lead to a worse prognosis than one, it is more likely that dual infection is simply a marker of advanced disease; as the patient approaches death, more colonizing bacteria may gain a foothold in the normally sterile lung tissue. Secondary infecting pathogens are not "false-positives" because they all contribute to the condition of the patient; however, if the objective is to define the pathogen initiating the pneumonia, as it would be in evaluating the potential impact of a pathogen-specific vaccine, then cultures of secondary organisms are misleading.

	Sensitivity and Diagnostic Yield

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There is no superior "gold standard" by which the sensitivity of lung aspiration can be assessed. Therefore, the appropriate measure of the value of the procedure is its diagnostic yield, or the percentage of positive diagnoses. A summary of etiologic series using lung aspirates is presented for children, in Table 1 , and for adults, in Table 2 . The mean diagnostic yield for culture of a single respiratory pathogen is 41% in children and 47% in adults. For any culture, single or multiple, the mean yield is 48 to 49% in both groups. A summary yield must be interpreted with caution as there is significant variation in the estimates of individual studies within both children and adults (², p < 0.0005), which probably reflects the different age structures and geographic locations of the populations studied and the differential access to antibiotics.

Lung aspirate studies may also reveal additional or discordant isolates when compared with results of blood cultures.^{5 23 31 66 82} Among 100 children in the Gambia, different species of pathogen were isolated in blood and lung aspirate cultures from four patients; for a child with S pneumoniae in blood cultures and S aureus in the lung aspirate, the latter investigation may have provided life-saving information.²³

Sensitivity to Multiple Etiologies
When two organisms are implicated in pneumonia, the possibility of a false-positive test should be considered seriously. When both organisms are isolated from lung aspirate cultures, however, the evidence implicating dual etiology is relatively strong. H influenzae and S pneumoniae were first co-isolated in lung aspirates 80 years ago^{31 58} and have been found repeatedly throughout the century.^{12 21 23 24 37 44 66 87 103} Dual etiology appears to be more common among children. For example, H influenzae and S pneumoniae were isolated in 18 of 83 lung aspirates (22%) in children from the Papua New Guinea (PNG) Highlands⁶⁶ but in only 2 of 90 aspirates (2%) from adults in coastal PNG.²¹ Other pairs of pathogens have been cultured together,^{31 79 100} and three and four organisms have been found in the same lung aspirate,^{24 66} although higher orders of co-isolation frequently include one or more probable skin contaminants. It is notable how frequently Branhamella catarrhalis appears as a co-culture in lung juice, yet how infrequently it is isolated alone,^{24 66} suggesting that its role in pneumonia is rarely that of the initiating cause.

Dual infection can occur within one species. Two different serotypes of pneumococci were isolated from 7 of 1,255 aspirations performed by Bullowa⁴⁵ on adults with pneumonia. Two serotypes have also been isolated from postmortem lung cultures in a United States adult and from an antemortem lung aspirate in a Gambian child.^{23 112} In the PNG study, two different populations of H influenzae were isolated from lung aspirates in eight children, with each culture comprising one encapsulated strain and one unencapsulated.^{12 66} As the encapsulated strain was also more likely to be isolated from blood, the authors argue that lung aspirates may reveal a pattern of serotypes that is more representative of those causing pneumonia and is more relevant for the selection of antigens in polyvalent vaccines.⁶⁶ Among adults with pneumonia in Kenya, serotypes 1, 4, and 14 accounted for 11 of 17 pneumococci (65%) found in lung aspirates alone, but for only 6 of 25 isolates (24%) found in blood alone (authors’ unpublished observations).

Diagnostic Yield in TB
TB was first diagnosed by lung tap in 1923,⁵² and mycobacteria have been isolated from lung juice in numerous subsequent aspirate studies.^{62 81 82 94 101 103 113 114 115 116} Schuster et al⁸¹ were the first to propose aspiration as a specific diagnostic technique for pulmonary TB and argued their case by reporting aspirates from 10 Chilean infants with an appropriate clinical syndrome; in eight, M tuberculosis was cultured on Lowenstein-Jensen medium, and in seven, acid-fast bacilli were seen on lung juice smears, providing a rapid diagnosis. From the eight infants who received TB diagnoses, culture of gastric washings proved negative in six. In a similar study from Udaipur, India, 16 of 30 infants with a compatible clinical illness had positive lung juice cultures, five of which were positive on lung aspirate smears.¹¹³

From a series of 1,255 lung aspirates in Sweden, Dahlgren and Ekstrom¹¹⁴ performed a retrospective audit of 212 cases in which a diagnosis of TB had been suspected. The patients were investigated using fine-needle aspiration under fluoroscopic control with Ziehl-Neelsen stains, Lowenstein-Jensen cultures, and guinea pig inoculation. Based on 5-year follow-up figures, TB was missed by lung aspirate in only 26 of 197 true-positive patients, and false-positive diagnoses were encountered in 15 patients. This gives a sensitivity of 87% and positive predictive value of 92%. The case definition in all these studies is subjective and ill-defined, so it is difficult to relate these very successful results to an unselected population of patients with chronic respiratory illness. Nonetheless, in patients with a strong clinical suspicion of TB and negative gastric lavage and sputum smears, lung aspiration may lead to a diagnosis, particularly if the needle is radiologically guided to the center of the diseased area.¹¹⁵ Furthermore, in etiologic studies of acute pneumonia, particularly in developing countries, M tuberculosis has been found either alone or in combination with other respiratory pathogens in 2 to 9% of lung aspirate cultures, indicating that all aspirate samples should be cultured for Mycobacteria.^{62 82 101}

Diagnostic Yield in Bronchopneumonia
The patchy nature of bronchopneumonia suggests that it might lend itself less readily to lung aspirate diagnosis.^{42 43} Only three studies have directly contrasted the diagnostic yield in comparable populations with lobar pneumonia and bronchopneumonia. In Lyon’s study,³¹ the yield from 20 children with lobar pneumonia and 18 with bronchopneumonia was 50% in each group. Glynn and Digby⁵² studied 31 adults and 13 children and obtained positive cultures in 4 of 6 bronchopneumonia patients (67%) and in 18 of 38 lobar pneumonia patients (47%). In Kenyan adults, respiratory pathogens were cultured in 7 of 28 patients with bronchopneumonia (25%) and in 57 of 231 patients with lobar pneumonia (25% [authors’ unpublished observations]). In the latter two studies, there was an excess of S aureus in cultures from bronchopneumonia patients. The largest experience of bronchopneumonia comes from a population of 505 Chilean infants in whom the diagnostic yield was a very adequate 45%.⁷⁹ There is no evidence to support the idea that lung aspirate cultures are less sensitive in patients with bronchopneumonia.

	Causes of False-Negative Results

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One of the commonest causes of a negative result in a lung aspiration study is failure to perform the test! Physicians have an understandable reluctance to puncture the thorax, particularly in children,^{31 117} and patients have an understandable anxiety. Diak-paromre and Obi¹⁰⁰ limited their punctures to the posterior thorax "in order to reduce anxiety." Lyon³¹ wrote in 1922, "At best, it is a somewhat painful procedure, and often excites in the child patient a terror which for several days to come reawakens with every appearance of the physician." Shortening the needle from 15 cm to 3 cm will reduce much of this anxiety, but there are other obstacles to puncture. In many African cultures, consent to invasive procedures can only be given by the father of a pediatric patient, but it is usually the mother who takes the child to the hospital. This may have been a factor in a study of 90 Gambian infants with acute respiratory infection, in which lung aspirates were obtained in only 2 patients.¹¹⁸ A second limitation is the timing of presentation. Lung puncture studies usually require radiographic evidence of consolidation, but patients presenting early in the disease may not yet have developed radiologic changes. A good example is given by Douglas and Devitt,¹⁰⁶ who performed lung aspiration in a patient with clinical signs of bronchial breathing before the radiograph was formally reviewed. The aspirate grew S pneumoniae, and the radiograph was reported as normal.

Occlusion of the needle by a skin plug⁴⁵ will yield a false-negative result, but this can be avoided by using a stylet or by injecting a small volume of sterile broth.¹¹⁹ The consolidation may be missed if it is small or if the operator is inexperienced. The changes on the radiograph may represent malignancy, pulmonary edema, pulmonary eosinophilia, or other noninfectious etiology.¹²⁰ Because the number of organisms cultured from patients with pneumococcal pneumonia increases as the disease progresses and falls as a patient recovers naturally, punctures performed too early or too late may fail to detect the infection.^{13 22 121}

In seven studies with appropriate data, prior use of antibiotics reduced the diagnostic yield in all but one, with a mean reduction of 32% (Table 4 ). Antibiotics given after hospital admission have also been associated with a 57% reduction in diagnostic yield, although patients selected for aspiration after failure of initial therapy are not representative of newly presenting patients.¹²² Because of the large antibiotic effect, some authors have specifically excluded patients with a prior history of antibiotics.¹⁰⁶ While this will lead to higher diagnostic yields, it excludes a group who differ on a number of potentially important variables, including severity of illness, and may produce an unrepresentative description of pneumonia etiology. If the presence of antibiotic is measured in urine, these patients do not need to be excluded and compensation can be made for the calculated antibiotic effect; furthermore, the history of antibiotic use correlates poorly with biological measures of antibiotic use.⁶⁶ A separate approach to the problem of antibiotics is to use nonculture-based methods. Polymerase chain reaction for penicillin-binding protein genes PBP 2x and PBP 2b have been positive in lung aspirate specimens from 75% (9/12) and 89% (16/18) respectively, of adult patients with pneumonia whose blood or lung aspirate cultures were positive.^{11 123} Antigen detection in lung aspirate specimens using pneumococcal omniserum has been reported in several studies,^{11 104 109 123 124 125} with sensitivities ranging from 12 to 92%.

Lung aspirate cultures may also be defined as "negative" if the organism isolated does not fit with our current concept of pneumonia etiology: an example is given by the isolation of poliovirus type 1 from the lungs of an Indian child.¹²⁷ We have isolated Staphylococcus epidermidis from a Kenyan adult in lung aspirate cultures and two separate blood cultures, but dismissed the organism as a contaminant; against such prejudice, it would be difficult to detect a case of S epidermidis pneumonia should one ever arise.

	Complications

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Death
Rapidly popularized after its introduction, lung puncture was widely practiced at the turn of the 20th century but quickly became associated with fatal complications. Horder’s Lancet report²⁹ of the technique in 1909 did not mention serious side effects, but contemporary medical publications referred to at least 11 deaths after thoracic puncture.^{128 129} In 1905, an editorial in the British Journal of Childhood Diseases opined, "exploratory puncture of the chest is looked on by the younger members of the profession as a harmless proceeding, and on a par with the use of the stethoscope for the examination of children’s lungs, indeed there are some who give precedence to the needle."¹³⁰

We have been able to find 17 reports of death in patients who have undergone lung puncture (Table 5 ). There is no denominator for the 10 reports published between 1898 and 1920. Most of these cases had empyema or unresolved pneumonia; investigation of acute pneumonia was the indication in only one case. Three patients died of pulmonary hemorrhage, one of air embolism, and another of pneumothorax. The cause of death is unclear in the remainder; most patients died suddenly, and two deaths were preceded by neurologic symptoms suggestive of air embolism.

Pneumothorax
Pneumothorax is the major nonfatal complication of lung aspiration. From a summary of > 3,000 reported procedures, pneumothorax occurred in 3.3%, or 1 in 30 (Table 6) . Among the studies summarized, some included routine postprocedure radiographs while others did not; many authors do not report whether radiographs were evaluated routinely. A small laminar pneumothorax is clearly a minor problem; pneumothorax requiring the insertion of a chest drainage tube is much more serious. Chest drainage was required following only 0.5%, or 1 in 200 procedures, among the series summarized in Table 6 . By comparison, chest tube insertion is required in approximately 12%¹³⁸ of aspiration lung biopsies, indicating the higher risk associated with a larger needle.

The risk of significant pneumothorax can be reduced by puncturing the lung only once⁴⁰ and by avoiding inexperienced operators.^{25 40 93} Chronic obstructive airways disease and Pneumocystis carinii pneumonia (PCP) are particular risks for pneumothorax after thoracentesis,^{14 139} and patients with less respiratory reserve are more likely to require drainage should a small pneumothorax develop.

In patchy bronchopneumonia, the consolidation may not abut against the pleura, and the risk of pneumothorax is theoretically higher than in lobar pneumonia. What little evidence exists tends to contradict this idea. In a series of 505 Chilean infants with bronchopneumonia, pneumothorax requiring chest drainage occurred in only 2 patients (0.4%)⁷⁹ ; among 30 Indian children with suspected TB followed up with fluoroscopic examination, none developed pneumothoraces.¹¹³

Other Complications
Empyema, air embolism, and pulmonary hemorrhage were greatly feared by the pioneers of lung aspiration, but they are mentioned only rarely in the series collected in Table 6 . There is not a single report of empyema thoracis, and numerous investigators in the preantibiotic era argued that the risk of empyema after pneumonia was not increased by the introduction of lung aspiration.^{15 40 85} Bullowa⁹ attributes five adverse events among > 2,500 aspirates to air embolism, but otherwise the complication is confined to patients undergoing aspiration lung biopsy.^{25 140} In closed lung aspiration, with the syringe firmly attached to the needle, the risk of introducing air to a vessel is minimal, but it increases significantly if a technique is used in which a stylet must be removed after a large needle is introduced.¹⁴¹

Although minor hemoptysis is relatively common, prolonged or serious pulmonary hemorrhage after lung puncture was reported after only 2 of > 3,000 procedures, and neither case was fatal. In studies that have directly compared fine-needle aspiration with larger-gauge biopsy cutting needles, the risk of pulmonary hemorrhage is considerably higher following lung biopsy.^{142 143} In fact, in recent decades, major hemorrhage appears to be confined to patients undergoing trephine biopsy with large-bore needles.¹⁴⁴ In the biopsy of pulmonary nodules, aerated lung along the needle track does not provide any compression in the event of a vessel puncture.¹⁴⁵

Pleuritic pain is rarely reported but occurs with a consistent frequency of approximately 2% in studies that do report it.^{80 101 113} Among Kenyan adults, 6 of 259 patients complained of pain requiring anal-gesia and one developed protracted hiccups (au-thors’ unpublished observations). Surgical emphysema^{62 96 113 146} and hematoma²¹ are infrequent local complications.

	Investigation of Pneumonia in Complex Patients

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In addition to community-acquired pneumonia, lung aspiration has been used to investigate lung cancer, pulmonary nodules, diffuse lung disease, granulomata, lung abscess, cavitating lung disease, and chronic and unresponsive pneumonias.¹⁴⁵ These aspirates are usually conducted under fluoroscopic or ultrasound control, using longer and wider-gauge needles. There is considerable heterogeneity in the conditions investigated, although the principal use of the technique is to diagnose primary lung neoplasms. Table 7 summarizes 19 investigations in which, by contrast, the objective of the study was to define an infective etiology in patients who did not have simple, acute, community-acquired pneumonia.

What is clear is that the frequency of serious, nonfatal complications in complex patients is considerably higher than in simple pneumonia patients, with 18% of all aspirates leading to pneumothorax and 8% leading to insertion of a chest drain. Pulmonary hemorrhage is also more common, with serious events occurring in about 1% of patients. Air embolism was reported in only 1 of 1,018 patients. Wider reviews of > 8,000 lung aspiration procedures in patients with abnormal radiologic lung lesions have documented similar complication rates with only one fatality, no cases of air embolus, and only three cases of major hemorrhage; pneumothorax requiring chest drainage occurred in 8%.^{144 152 153} Occasional case reports have drawn attention to fatal hemorrhage¹⁵⁴ or air embolism.¹⁴⁰

In patients with HIV, bedside lung aspiration with an ultrathin needle has succeeded in identifying an infective pulmonary pathogen in 29 of 47 procedures undertaken in Spanish adults¹⁵⁰ ; half of these had PCP. Induced sputum specimens were positive in only 3 of 15 patients with PCP, suggesting that lung aspiration was targeted at patients whose early induced sputum specimens were known to be negative. Wallace et al¹⁴⁷ diagnosed PCP using lung aspirates in 10 of 16 patients with AIDS or suspected AIDS, but 7 of these patients developed pneumothoraces and 3 required drainage. The risk of pneumothorax is increased in patients with previous or concurrent PCP or with a history of nebulized pentamidine use,^{155 156} which constrains the use of lung aspiration in HIV-infected patients. In sub-Saharan Africa, where PCP is an uncommon cause of pneumonia in HIV, lung aspiration has been successful in the diagnosis of bacterial pneumonia.⁸²

	Safe Conduct of Lung Aspiration

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Guidance for the safe conduct of lung aspiration in 1904 advised premedication with brandy and the following emergency action: "Should the heart cease beating or the breathing become suspended during or after the puncture immediate resort by the medical attendant to artificial respiration and the injection hypodermically of ether and strychnine."¹³³ Although the procedure has remained unchanged in over 100 years, the preparation for the procedure and resuscitation techniques have evolved consid-erably.

The equipment required to support the procedure consists of a supply of oxygen, a chest drain insertion kit,¹⁵⁷ and smaller cannulae for the rapid relief of smaller pneumothoraces. The success of the procedure is critically dependent on localization of disease; chest radiographs in two planes,⁸² CT scans,^{17 148} or ultrasonography^{19 126 151} can all enhance localization based on clinical signs. They may also reveal unexpected contraindications such as bullae or Echinococcus cysts.¹³¹ The prothrombin time, partial thromboplastin time, and platelet count should be checked when possible, and lung aspiration should be avoided in patients with significant derangements, eg, a prolongation of the prothrombin time by > 50% or a thrombocytopenia of < 70,000/mL.

A knowledge of the surface anatomy of the thorax is essential, especially in the child, to avoid striking the heart and great vessels; the illustrations in the cadaver study of Abdel-Khalik et al²⁴ may be a useful aid. Targeting only peripheral consolidation, and therefore using a short needle (< 5 cm), will avoid puncture of a major vessel. Similarly, use of a finer needle (21- or even 25-gauge) will decrease the likelihood of pneumothorax without compromising the search for infectious etiologic agents.¹⁶ The aspirate system should be properly sealed throughout the procedure and use of a stylet should be avoided, if possible, to eliminate the possibility of air embolism during transfer to the syringe. Multiple stabs within the lung parenchyma may increase the risk of hemorrhage and have not been demonstrated to increase the diagnostic yield.²¹ Avoidance of normal lung will reduce the risk of pneumothorax, and lung puncture should never be done bilaterally.⁹ Patients who are too hypoxemic to suspend respiration for 1 to 2 s (Gherman and Simon¹¹⁹ ) and those who are unable to tolerate a pneumothorax briefly should not be investigated. In adults, COPD and lung bullae are relative contraindications, depending on severity and location; similarly, puncture should be avoided in children with hyperinflation. Pulmonary hypertension is also a contraindication,¹⁵⁸ but the pressure in the pulmonary circulation is rarely known in the acute investigation of pneumonia.

The vital signs of the patient should be monitored closely for 24 to 48 h and a chest radiograph taken 1 h after the procedure. Of 160 pneumothoraces that developed in patients undergoing aspiration biopsy, 89% were evident on the radiograph performed immediately after the procedure, and 9% were first seen 1 h later. Pneumothoraces that appeared after the 1-h radiograph were never sufficiently important to require chest drainage.¹³⁸ Patients requiring mechanical ventilation have been avoided by most investigators, although successful aspirations have been performed with suspension of assisted ventilation in eight patients.¹⁸

	Uses of Lung Aspiration

TOP Introduction Materials and Methods The Technique Historical Perspective Specificity: Bacteriology of the... Causes of False-Positive Results Sensitivity and Diagnostic Yield Causes of False-Negative Results Complications Investigation of Pneumonia in... Safe Conduct of Lung... Uses of Lung Aspiration References

 
Lung aspiration has an undoubted role in etiologic studies of pneumonia. It provides considerable additional information over blood cultures on the species and serotypes causing disease, and their antibiotic susceptibilities, with high specificity. It is usually acceptable to the patient and carries a minimal risk of serious adverse effects, and the individual undergoing aspiration stands to benefit personally from the microbiologic information obtained. It has been so successful in some tropical environments that it is now commonly used as an adjunct to routine clinical management.⁶²

Outside scientific studies lung aspiration may be considered on an individual basis for patients who have not responded to initial therapy, who may have nosocomial superinfection, who are immunocompromised, or in whom TB is suspected but has not been confirmed by examination of the sputum or gastric lavage.⁹¹ The more complex the patient’s clinical course, the more valuable the information obtained directly from the lung; at the same time, the more likely the procedure is to be complicated by coagulopathy, thrombocytopenia, pleural infection, or mechanical ventilation. There are no studies directly comparing lung puncture with blind therapy or other diagnostic procedures in these cases, but it seems likely, extrapolating from epidemiologic studies of pneumonia, that early use of the procedure in appropriately selected patients may improve patient outcomes. If lung aspiration is reserved as a diagnostic measure of last resort for the ICU patient with fever, diffuse lung disease, mechanical ventilation, multiorgan failure, and nosocomial flora in sputum, it will not provide timely diagnostic information and may well contribute to death. However, in the presence of dense peripheral consolidation, percutaneous transthoracic lung puncture can provide life-saving etiologic information with minimal risk in experienced hands; it can be performed quickly at the bedside, it requires no sedation, and it is likely to be more acceptable to the patient and less traumatic than the major alternative, bronchoscopic lavage, performed a few days later.

	Acknowledgements

 
We are very grateful to Dr. Nicola Strnad for translation from German.

	Footnotes

 
Abbreviations: PCP = Pneumocystis carinii pneumonia; PNG = Papua New Guinea; TB = tuberculosis

Supported by the Wellcome Trust of Great Britain through a Wellcome Trust research training fellowship in clinical epidemiology, No. 035375 (Dr. Scott).

Received for publication March 17, 1999. Accepted for publication May 5, 1999.

	References

TOP Introduction Materials and Methods The Technique Historical Perspective Specificity: Bacteriology of the... Causes of False-Positive Results Sensitivity and Diagnostic Yield Causes of False-Negative Results Complications Investigation of Pneumonia in... Safe Conduct of Lung... Uses of Lung Aspiration References

 

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