Review of Respiratory Medicine - Volumen 25, N�mero 2 - June 2025

Original Articles

Comparison of Microorganisms Found Using Different Sampling Techniques for Bronchial Secretions (mini BAL versus endotracheal aspirate) in Patients Requiring Invasive Mechanical Ventilation: a Retrospective Study

Comparación de los microorganismos encontrados en las diferentes técnicas de toma de muestra de secreciones bronquiales (minibal versus aspirado endotraqueal) en pacientes con requerimiento de ventilación mecánica invasiva: estudio retrospectivo

ABSTRACT

Background: Numerous techniques for obtaining microbiological samples have emerged to improve the diagnosis of nosocomial infections in patients requiring invasive ventila­tion. These include endotracheal aspirate and mini-bronchoalveolar lavage.

Objective: To compare microorganisms found with different sampling techniques (mini-bronchoalveolar lavage versus endotracheal aspirate) in a hospital in the suburbs of the Province of Buenos Aires (Argentina), during the periods 2018-2019 (pre-COVID-19) and 2020-2021 (during COVID-19).

Materials and methods: A retrospective study of mini-bronchoalveolar lavage and en­dotracheal aspirate samples taken from January 2018 to December 2021 in a hospital in the suburbs of Buenos Aires. The technique used with each patient was determined by the medical staff, independently of the present study.

Results: A total of 336 microorganism results were included. 119 of them corresponded to the pre-COVID-19 period, with a predominance of the mini-bronchoalveolar lavage technique, and 217 results corresponded to the COVID-19 period, from samples taken by endotracheal aspirate. Regardless of the technique, gram-negative bacilli predomi­nated in all results, and the most frequently found microorganism was Pseudomonas aeruginosa.

Conclusion: In the pre-COVID-19 period, the mini-bronchoalveolar lavage technique was the most prevalent, and in the COVID-19 period, endotracheal aspirate was more frequently used. This suggests that the endotracheal aspirate technique is optimal for routine analysis, given that it is more economical and safer.

Key words: Bronchoalveolar lavage, Nosocomial infection, Ventilator-associated pneumonia, COVID-19, SARS-CoV-2, Critical care

RESUMEN

Introducción: Para mejorar el diagnóstico de las infecciones nosocomiales en pacien­tes con requerimiento de ventilación invasiva han surgido numerosas técnicas para obtener muestras microbiológicas, entre ellas el aspirado endotraqueal y minilavado broncoalveolar.

Objetivo: Comparar los microorganismos encontrados en las diferentes técnicas de la toma de muestras (minilavado broncoalveolar versus aspirado endotraqueal) en un hospital del conurbano de la Provincia de Buenos Aires (Argentina), en los períodos 2018-2019 (pre-COVID-19) y 2020-2021 (durante COVID-19).

Materiales y métodos: Estudio retrospectivo de las muestras de minilavado broncoal­veolar y aspirado endotraqueal tomadas en el período enero 2018 a diciembre 2021, en un hospital del conurbano de Buenos Aires. La técnica utilizada con cada paciente fue determinada por el personal médico, independiente del presente estudio.

Resultados: Se incluyeron 336 resultados de microorganismos. De estos, 119 co­rrespondieron al período pre-COVID-19, con predominio de la técnica de minilavado broncoalveolar y 217 resultados correspondieron al período COVID-19, de muestras tomadas por medio de aspirado endotraqueal. Independientemente de la técnica, en todos los resultados, predominaron los bacilos gram negativos y el microorganismo más frecuente fue Pseudomonas aeruginosa.

Conclusión: En el período pre-COVID-19 estuvo más presente la técnica de minilavado broncoalveolar y en el período COVID-19, la del aspirado endotraqueal. Esto sugiere que la técnica aspirado endotraqueal es óptima para análisis de rutina, dado que es más económica y segura.

Palabras clave: Lavado broncoalveolar, Infección hospitalaria, Neumonía asociada al ventilador, COVID-19, SARS-CoV-2, Cuidados críticos

Received: 09/27/2024

Accepted: 04/10/2025

INTRODUCTION

Nosocomial infections are a significant public health problem due to their impact on morbid­ity and mortality. The use of an artificial airway significantly increases the risk of developing pneu­monia (estimated to be 6-21 times higher), one of the main causes of death from hospital-acquired infections, along with primary bacteremia. These infectious complications prolong hospital stays (by approximately 7-9 days) and increase healthcare costs. In the context of diagnostic optimization of nosocomial infections, various microbiologi­cal methods have been investigated in the adult population.^{1- 3}

In this study, we will focus on two of these techniques: endotracheal aspirate (EA) and mini-bronchoalveolar lavage (mini-BAL) or protected telescoping catheter. The differences between these techniques are related to their limitations in sensitivity/specificity and the search for non-inva­sive methods over invasive ones. The COVID-19 pandemic exacerbated infectious complications in critically ill patients in the ICU (Intensive Care Unit), with a higher incidence of hospital-acquired bacterial and fungal infections and a consequent increase in mortality. In addition, diagnosis was hindered by adaptations in clinical practice and the precautions necessary to ensure the biosafety of healthcare personnel during sample collection and processing.^{4- 6}

So, the objective of this study is to compare microorganisms found with different sampling techniques (mini-bronchoalveolar lavage versus endotracheal aspirate) in a hospital in the suburbs of the Province of Buenos Aires (Argentina), dur­ing the periods 2018-2019 (pre-COVID-19) and 2020-2021 (during COVID-19). As a secondary objective: to identify the hospital’s most common colonizing microorganisms during the same period.

MATERIALS AND METHODS

Design and ethical aspects

The study design was observational, descriptive, cross-sectional, and retrospective, based on mini-BAL and EA samples taken between January 2018 and December 2021, in a general acute-care hospital in the southern area of the suburbs of Buenos Aires (Dr. O.). The study was ap­proved by the institutional research ethics committee of H.Z.G.A.D. Evita Pueblo, Berazategui, according to Refer­ence Document IF-2021-30624965-GDEBA-CECMSAL. All international ethical standards for research in humans, as set forth in the Declaration of Helsinki, and national regula­tions for patient protection⁷ and personal data protection⁸, were observed.

Population and eligibility criteria

Mini-BAL and EA samples were included using non-proba­bilistic convenience sampling. Exclusion criteria included: samples reported by the hospital’s laboratory service as insufficient, erroneous, or undetectable.

For sample characterization, the variables used were: age (completed years), sex (male/female), sample type (mini- BAL, EA), microorganism found (gram-negative bacillus, gram-positive bacillus, gram-negative coccus, gram-positive coccus, polymicrobial flora, fungi).

Endotracheal aspirate

The tracheal aspirate technique is considered minimally invasive, cost-effective, and easy to perform. Qualitative analyses of the samples show a wide range of sensitivity (38% to 100%) and specificity (14% to 100%), which is why the sample is considered nonspecific.9 Sensitivity improves when the sample contains a concentration of 106 colony-forming units per milliliter (CFU/mL).^9,10

Samples collected for this study had the following characteristics:

1. Collection of secretion samples through a polyvinyl chloride (PVC) suction catheter after passing beyond the artificial airway.

2. Suction vacuum was obtained from the hospital’s central suction system, connected via BT-63 tubing to the suc­tion set.

3. The catheter contents were directed straight into a sterile polypropylene collection container^11,12 attached to the catheter by a lid, which was then replaced so as to seal the container and send the labeled jar with the patient’s name and bed number to the laboratory.

4. Samples were handled according to specific protocols, they were treated as sputum, and sent to the labora­tory without refrigeration to ensure preservation of integrity.¹¹

Samples were considered positive^9,10 when they had less than ten epithelial cells per field, macrophages as indicators of sample depth, and more than twenty-five leukocytes per 100-field (a sign of inflammatory process).

Mini-bronchoalveolar lavage

This method, used to obtain samples from the lower respi­ratory tract, is performed blindly and is considered mildly invasive.^13-15 When the mini-BAL technique is carried out with the appropriate catheter and proper procedure, it shows sensitivity ranges from 63% to 100%, while specificity falls within 66% to 96%.^9,16

The mini-BAL technique was performed as follows:

1. Patient sedated to RASS scale –5.

2. Upper airway secretions were suctioned.

3. Entry into the respiratory system was achieved using a protected telescoping catheter (PTC), consisting of an inner catheter contained within a larger outer catheter. This specific design of the inner catheter prevented con­tamination from the flora present in the upper airway.¹³

4. Once slight resistance was encountered, the inner cath­eter was advanced, followed by the instillation of saline solution, in volumes ranging from 20 mL to 150 mL.^{9 ,15-18}

5. Finally, manual vacuum was applied with the same syringe to collect the respiratory secretion sample, which was transferred to a sterile jar labeled with the patient’s name and bed number, then sent to the laboratory.¹⁵

A sample was considered representative if it met the following criteria:^9,14,19 more than twenty-five polymorpho­nuclear cells, less than ten squamous epithelial cells per field, a concentration of more than 104 colony-forming units per milliliter (CFU/mL), and absence of prior antibiotic administration.

Biosafety measures used in both techniques included: handwashing before and after the procedure; operator protection with goggles, face mask, cap, and gown; use of sterile gloves to handle the equipment; and, only in the case of mini-BAL, the use of a sterile drape.

Data collection

The collection of secretion samples was carried out by physiotherapists from the intensive care unit who were trained and experienced in both techniques (mini-BAL and EA). The technique used was determined according to the medical request and the department’s routine. Some patients required multiple collections during their hospital stay due to suspected new pneumonia, superinfections, or to evaluate the effectiveness of the treatment. Data on the microorganisms identified were gathered from the hospital laboratory records.

Statistical analysis

A nominal variable was used for the measurement of the categorical variable of the microorganism found, and a nominal dichotomous scale was used for the measurement of the remaining variables, while for their description, absolute and relative frequencies were employed. Con­tinuous variables that assumed a normal distribution were reported as mean and standard deviation. The data were documented in a Microsoft Excel database created specifi­cally for the study.

RESULTS

Secretions were collected from 280 patients, 65% of whom were male, aged between 14 and 100 years, with a mean age of 57 (±19) years.

A total of 408 secretion samples were analyzed, of which 137 were excluded (the laboratory report­ed 118 as “undetectable” and 19 as “insufficient or erroneous”; these categories were assigned for not meeting the representativeness criteria speci­fied according to the sample type). A total of 336 microorganism results were included. 119 of them corresponded to the 2018-2019 period, and 217 to the 2020-2021 period. (Figure 1)

Table 1 describes the types of microorganisms found in each period according to each tech­nique. Pseudomonas aeruginosa was the most predominant microorganism in both periods, however, during the pre-COVID-19 period, the mini-BAL technique was more prevalent, and during the COVID-19 period, the more com­monly used was EA. Gram-negative bacilli were predominant.

In both periods, the same four types of microor­ganisms predominated, in different orders. Figure 2 shows the four main microorganisms found in the pre-COVID-19 period, and Figure 3 those from the COVID-19 period. Regardless of the period or the technique, gram-negative bacilli and gram-positive cocci predominated.

DISCUSSION

The analysis of microbiological samples showed that, before the SARS-CoV-2 pandemic, the mini- BAL technique was more frequently used, whereas during the pandemic years studied, the AE tech­nique predominated. This did not change the fact that the predominant microorganism in the critical care areas of H.Z.G.A. Dr. A. O. was Pseudomonas aeruginosa

The Infectious Diseases Society of America and the American Thoracic Society²⁰ clinical practice guidelines recommend that each hospi­tal periodically generate a specific antibiogram. Indeed, identifying the microorganism affecting the patient early facilitates the correct medica­tion,^{17, 21-23} thereby reducing hospitalization days and associated costs, which greatly benefits the patient’s health.^{20, 21, 24}

Due to the lack of direct studies comparing mini- BAL with EA, we included in this discussion some studies that compare mini-BAL with BAL. We em­phasize that there are major differences between these two techniques: BAL is an invasive procedure performed by physicians, involving direct visual­ization of the airway to obtain targeted samples, whereas mini-BAL is a blind technique that in­volves inserting a telescoping catheter through the endotracheal tube and can be performed by trained non-physician staff members –features that make it similar to the EA technique.^{13, 14, 19}

Mini-BAL is supported by studies that conclude that its specificity and sensitivity are acceptable for diagnosing mechanical ventilation-associated pneumonia,^14,19 as in the study by Ahmad et al, in which no significant differences were found be­tween mini-BAL and BAL methods for obtaining secretions or analyzing bacterial and mycological pathogens. For this reason, they propose using mini-BAL, since it is less invasive and, in their study yielded the same results as BAL.¹⁶ Villanueva et al carried out the same comparison and found that mini-BAL could be an effective method for ga­lactomannan antigen testing (a heteropolysaccha­ride in the cell wall of Aspergillus spp.), although a negative result would not rule out COVID-19–as­sociated invasive pulmonary aspergillosis.²⁵

In the hospital where this research was con­ducted, that analysis was routinely performed within the first hours of initiating mechanical respiratory assistance; however, because BAL requires instilling saline solution and retrieving all of the introduced fluid¹⁸ –something not always possible– it is not as harmless⁶ as EA. For this reason, EA samples were more commonly collected during the COVID-19 pandemic. In fact, the guide­lines of the Infectious Diseases Society of America and the American Thoracic Society recommend using EA to diagnose VAP (ventilator-associated pneumonia), as it is less invasive than mini-BAL, causes fewer complications, uses fewer resources, and is faster for the operator, who may have less experience in collecting samples.²⁰ Furthermore, the consensus statement of the Spanish Society of Pulmonology and Thoracic Surgery (SEPAR) and the Spanish Association for Respiratory Endoscopy (AEER) on the use of bronchoscopy and sampling of the respiratory tract in patients with suspected or confirmed COVID-19 infection recommend prioritizing the safety of healthcare personnel and patients against possible contagion from virus exposure during secretion sampling.^{24, 26}

Several studies mention the EA as one of the most widely used blind techniques, due to its ease of performance, low cost, and safe profile for both the operator and the patient, highlighting the speed with which results are obtained –even before patients present symptoms of pneumonia.^{19, 20, 21, 27, 28} Frota et al also carried out this type of analysis, compar­ing the EA technique with a protected catheter technique (10 Fr tracheal tube inside another ²⁰ Fr nasogastric tube, similar to the mini-BAL system) and concluded that both techniques are statistically equivalent in terms of quantity and quality of microorganisms collected.¹² Ranzani et al analyzed samples using EA and concluded that it is a useful tool to improve the specificity of VAP diagnosis, emphasizing its cost-effectiveness and the potential to avoid false positives and overmedi­cation of patients.¹⁰

Regarding the microorganisms found with each technique, there were no differences. In both pe­riods we found a result similar to other studies,²¹ such as that of MacVane et al, where Pseudomonas aeruginosa and Staphylococcus aureus were main­ly identified, followed consistently by Klebsiella in both EA and BAL.²⁷

Studies such as that of Carvalho et al compared the pathogens identified with gram stain from tracheal aspirate and those from bronchoalveolar lavage cultures, and observed a moderate concor­dance. They concluded that the combination of gram staining with quantitative culture of tracheal aspirates may contribute to the diagnostic evalu­ation of VAP.²⁸ This observation is supported by several studies and literature reviews, which agree that we are normally colonized by gram-positive cocci, but in hospitalized patients the number of gram-negative bacilli found in samples^{22, 29, 30} increases significantly –an observation consistent with the data found in this work.

Although there is still no reference method (gold standard) for the diagnosis of VAP,^{19, 27, 31, 32} this analysis allows us to infer that both techniques can identify the pathogenic agents, corroborating the conclusion of previous stud­ies that suggest that the quantitative culture of EA may have the same diagnostic value as other invasive techniques.^{20, 28}

In their study, Mauro et al used a significant cut-off point for EA counts of 105 CFU/mL.²² However, they agree that cut-off points between 106 CFU/ mL and 107 CFU/mL could have greater clinical relevance, as noted in the work of Arango et al, which confirmed that a cut-off point of 106 CFU/ mL or higher in EA provides specificity percent­ages similar to those obtained with the mini-BAL method in the diagnosis of VAP.³³ It is important to note that the hospital laboratory where the present study was conducted also used this same cut-off point. It should be clarified that, in cases where fungal pneumonia is being suspected, mini-BAL is more specific because, in EA, common fungi¹⁹ are considered part of the flora of the mouth or upper airways.^{16, 18, 22, 34, 35}

This work has some limitations. One is that laboratory records did not show patient diagno­ses or if they were receiving antibiotics. Another thing is that the number of mini-BAL analyses during COVID-19 was lower than that of EA, due to the conditions of the pandemic, as previously mentioned. Finally, the number of patients was different in the two samples. Despite this, the study sets a precedent for future research and for updating the data on the predominance of microorganisms not only in the hospital where it was carried out, but also in others from dif­ferent regions of the country, thereby contrib­uting to take measures for infection control in hospitals. Moreover, it offers the most efficient, economical, and safe technique for collecting secretion samples, which facilitates precise drug administration and reduces the length of hospital stay and associated costs, ultimately benefiting patient health.

Since the COVID-19 pandemic, clinical practice guidelines suggest using a smaller volume of fluid for mini-BAL instillation,³⁶ or opting for the EA technique (invasive diagnostic techniques, such as bronchoscopy, do not offer greater benefit than blind tracheal suction using an inline catheter), given that they achieve similar results while being less risky for healthcare personnel in terms of con­tagion.³⁷ In fact, the proper protocol for performing the mini-BAL procedure requires a sequence of meticulous steps to maintain sample sterility, for which it is recommended that two operators be involved, and additional professionals should be available in the intensive care setting-something that is not always feasible. Additionally, in EA it is not necessary to instill saline solution to obtain the sample; it uses fewer resources and is quicker for the operator, who can have less experience and still adequately perform sample collection.²⁰ Fur­thermore, it can be performed by a single operator. For all these reasons, it turns out to be the most economical method.

CONCLUSION

The results of this study indicated that during the pre-COVID-19 periods, the mini-BAL technique was more prevalent, and during the COVID-19 period, the EA was more frequently used. Re­gardless of the technique, gram-negative bacilli predominated in all results, and the most frequent microorganism was Pseudomonas aeruginosa. This suggests that the EA technique is optimal for routine analysis, given that it is more economical and safer.

Conflict of interest

Authors have no conflicts of interest to declare.

Acknowledgment

The authors acknowledge and thank the H.Z.G.A. Dr. A. Oñativia for its support for this study, particularly its labo­ratory department, the Kinesiology service, and its head of service, Lic. Patricia Engardt

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