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Acta Paulista de Enfermagem

versión impresa ISSN 0103-2100

Acta paul. enferm. vol.25 no.3 São Paulo  2012 



Oropharyngeal colonization, and gastric and tracheal bacterial translocation, in children experiencing mechanical ventilation*



Denise Miyuki KusaharaI; Cristiane Cruz da Silva CanezinII; Maria Angélica Sorgini PeterliniIII; Mavilde da Luz Gonçalves PedreiraIV

IDoctorate in Nursing Philosophy. Professor of Undergraduate and Graduate Nursing, State University of Maringá - UEM, Maringá (PR), Brazil
IIDoctorate in Nursing Philosophy. Professor of Undergraduate and Graduate Nursing, State University of Maringá - UEM, Maringá (PR), Brazil
IIIPost-graduate student (Master's) in Nursing, State University of Maringá - UEM, Maringá (PR), Brazil
IVNurse in the Department of Health of Maringá. Maringá (PR), Brazil, Post-graduate student (PhD) in Nursing, State University of Maringá - UEM, Maringá (PR), Brazil

Corresponding Author




OBJECTIVE: To describe the pattern of oropharyngeal colonization and bacterial translocation, gastric and tracheal, in children experiencing mechanical ventilation.
METHODS: This descriptive study was conducted in a pediatric intensive care unit (PICU). Thirty children were recruited for the study, and 216 serial cultures were analyzed from oropharyngeal, gastric and tracheal secretions. Microbiological characteristics, demographic, clinical and treatment data were evaluated.
RESULTS: Among those who participated in the gastric suctioning, there was a predominance of children with chronic diseases, for which antibiotics, sedatives and gastric protectors were used. There was an increase in the number of children colonized by pathogens during hospitalization, and there was a predominance of several species: Enterobacter spp, K.pneumoniae, P. aeruginosa, A. baumannii and S. aureus. The majority of children (80.0%) experienced oropharyngeal translocation during hospitalization in the PICU.
CONCLUSION: Critically ill children may represent a group of patients at increased risk for colonization and bacterial translocation, predominantly from the oropharyngeal region to the trachea.

Keywords: Bacterial translocation; Pneumonia, ventilator-associated; Pediatric nursing; Intensive care




Healthcare-associated infections are considered important adverse events that compromise the patient's safety and result in considerable morbidity and mortality, increasing the time of hospitalization and attendance costs. In critically ill children, catheter-associated bloodstream infections are the most common, followed by pulmonary and urinary infections.(1)

Ventilator-associated pneumonia (VAP) in Pediatric Intensive Care Units (PICU), is the second most common cause of healthcare-associated infections, accounting for around 20% of the total number of events in this population. Data from the National Nosocomial Infections Surveillance System-NISS, have shown that in spite of the VAP frequency in children having diminished over the last few years, 2.1 episodes of VAP for every 1000 days of mechanical pulmonary ventilation (MPV) continue to be diagnosed in North American children(2,3)

The access of microorganisms to the normally sterile inferior respiratory tract may occur by means of four mechanisms: aspiration of secretions containing pathogens from the oropharynx, gastric cavity or sinus cavities; bacterial dissemination from a contiguous area, such as the pleura; by devices used for respiratory therapy and inhalation of contaminated aerosols, and or hematogenic translocation of microorganisms to the lung, coming from remote sites of infection. (4)

The importance of each potential reservoir of the gastrointestinal tract for tracheal colonization by microorganisms that cause VAP, whether oropharyngeal or gastric, has been cause for discussion among researchers for many years. During the 1980s in the 20th Century, evidence of colonization related to bacteria from the gastric cavity appeared in many researches. Nevertheless, recently, a positive relationship has been shown between bacterial species isolated from the oropharynx of adults and those identified in samples of bronchial secretions collected at the time of making diagnoses of pneumonia. (5)

The association between the oral and gastric micro-biota and VAP has been documented in adult patients, however, investigations about the colonization of these sites and the translocation of microorganisms from the oropharynx or stomach to the lower airways are limited, particularly in the pediatric population. Thus, the aim of this study was to describe the pattern of oropharyngeal, gastric and tracheal bacterial translocation in a group of children exposed to mechanical pulmonary ventilation.



The present investigation is a descriptive study about the colonization and translocation of bacteria from the stomach and oropharynx to the trachea in critically ill children, approved by the Research Ethics Committee of the Institution. The sample was composed of all the children hospitalized in a PICU, whose parents or legal guardians signed the term of free and informed consent, and who were submitted to MPV during the period of February 2007 to February 2008, and who did not have characteristics defined as criteria for exclusion from the main research to which the study is linked, these being: Newborn children, tracheostomized children, PICU length of stay and MPV duration less than 48 hours, respectively, children with diagnosis of pneumonia on admission, and those whose parents or guardians declined to concede free and informed consent. All the children admitted to the study were accompanied during the period of hospitalization in the PICU, and the microbiological, demographic, clinical, hospitalization, intensive therapy characteristics were analyzed.

Children admitted to the study were submitted to the collection of serial cultures of oropharyngeal (OS), gastric (GS) and tracheal (TS) secretions. All collections were performed in the morning period. The first collection occurred within the first 24 hours of tracheal intubation and the following samples for collected at regular intervals of 48 and 96 hours, after intubation. Due to the clinical condition, extubation, discharge and death of some of the children at the third collection, it was possible to analyze a lower number of cultures.

Oropharyngeal secretion cultures were obtained by means of swabbing the tonsil regions and the posterior pharynx, with the swab being introduced directly in a sterile tube containing Stuart Agar. To obtain tracheal secretion, the technique of protected tracheal aspiration was used, in a closed system under vacuum, directly into the collector flask, with dilution in saline solution 1:1. In a similar manner, the gastric aspiration was obtained by means of introducing a gastric tube, aspiration and instillation of the contents in a sterile flask, without dilution.

In the microbiological laboratory the samples were seeded to perform incubated in accordance with the parameters determined for atmosphere, temperature, time and humidity. After incubation the suspect colonies were submitted to biochemical assays for exact identification of the species, and disclosure of the results by professional specialists in microbiology, who provided advisory assistance with conducting this study.

Primary Results: To describe the characteristics of oropharyngeal, gastric and tracheal colonization of the children, the results of the microbiological cultures obtained in the three time intervals of collection were evaluated, and the microorganisms were characterized as species of normal or pathogenic microbiota. Thus, 30 children and 216 cultures were analyzed, with 72 cultures being from each of the sites. Of these, 30 cultures of each of the sites were obtained in time intervals of 24 hours, 30 in 48 hours and 12 in 96 hours. Secondary Results: The study of bacterial translocation, considered the displacement of bacteria from the enteric system to a sterile site, was initially based on the observation of a total number of 30 patients and 90 cultures, in order to identify bacte rial translocation in the first 24 hours of hospitalization in the PICU. Afterwards, a second analysis was made of another 90 cultures, with the purpose of evaluating the occurrence of bacterial translocation that occurred between 24 and 48 hours after the first collection of cultures. Finally, a last analysis was made, including 12 children and 36 cultures to identify the translocation that occurred between 48 and 96 hours of intubation of the children in the PICU. The results of the three serial cultures were analyzed, with oropharyngeal translocation being considered the presence of the same bacteria in the oropharyngeal and tracheal secretion between the time intervals of culture collections; gastric translocation being the presence of the same bacteria in gastric and tracheal secretion between the time intervals of culture collections, gastric and or oropharyngeal translocation, being the presence of the same bacteria in the gastric, oropharyngeal and tracheal secretion between the time intervals of culture collection, and absence of translation being identification of the species of bacteria in the tracheal secretion the one identified in the other secretions, or the absence of microorganism growth. (Figure 1).



Quantitative variables were represented by mean, standard deviation (SD) and median and the qualitative variables by absolute (f) and relative (%) frequency.



The demographic, clinical, hospitalization and therapeutic characteristics of the 30 children included in the stud are presented in Table 1. There was predominance of children with chronic diseases, who made use of antibiotics, central nervous system depressants, and gastric pH modifiers and those submitted to gastric tubes during hospitalization in the PICU. Long periods of use of mechanical pulmonary ventilation, hospitalization in the PICU and in hospital were observed.



A total of 216 samples were obtained, being 72 cultures of each type of secretion, distributed into three collection time intervals. Data with respect to children colonized by microorganisms of the normal and pathogenic microbiota are shown in Table 2.

As regards the presence of microorganisms of the pathogenic microbiota in the serial cultures of oropharyngeal, gastric and tracheal secretion, it may be observed that there was an increase in the number of children colonized by these bacteria as the days passed. Whereas analysis of the normal microbiota revealed a small reduction in the number of colonized children.

With respect to the identification of bacteria typical of normal microbiota, there was predominance of the Gram-positive species Streptococcus viridans and Staphylococcus coagulase-negative species and of the Gram-negative Moraxella spp species. The species of pathogenic microbiota isolated with greater frequency were the enterobacteria such as, Enterobacter spp and Klebsiella pneumoniae; non-glucose-fermenting bacilli such as Pseudomonas aeruginosa and Acinetobacter baumanii and Gram-positive Staphylococcus aureus species. As regards analysis of the gastric secretion, the identification of fungi and enterobacteria is emphasized.

Detailed results of the cultures analyzed may be observed in Chart 1.

It is pointed out that the majority of strains identi fied presented resistance to antimicrobial agents, with high frequency of strains of Klebsiella pneumoniae ESBL; strains of Pseudomonas aeruginosa and Acinetobacter baumanii Carbapenens-resistant and β-lactamase inhibitor resistant; strains of Staphylococcus aureus meticilin-resistant and strains of Enterobacter spp resistant to second and third generations of cephalosporins.

Of the 30 children analyzed, bacterial translocation was observed in 24 children (80.0%). As demonstrated in Table 3, these children suffered from some type of translocation in at least one of the time intervals of observation of the cultures, with oropharyngeal translocation being predominant, followed by absence of translocation. Among the children that presented bacterial translocation, 2 (8.3%) presented translocation identified exclusively before 24 hours, and between 48 and 96 hours; and in 5 (20.8%) patients it was shown that translocation occurred exclusively between 24 and 48 hours.




The physiopathology of respiratory infections involves mainly two processes: Colonization of the respiratory and digestive tracts and microaspiration of secretions from the upper and lower airways. (6)

Bacterial colonization refers to the presence of bacteria in a certain site of the body without causing an active host response to its presence. In the case of the lungs, colonization may occur due to invasion by microorganisms from sites such as the oropharynx, nasal cavities, dental plaque, gastrointestinal tract, the mechanical ventilation appliance circuit and other patients. (4,6)

The presence of a tracheal tube harms the body's natural defense mechanisms, such as reduction in air filtration and humidification, coughing reflex and mucociliary movement, providing a direct route enabling bacteria that colonize the upper airways to reach the lungs. (4,6)

All the children in this study remained intubated for a minimum period of 48 hours and around 30% of them were submitted to a re-intubation process. It was observed that 80% of these patients presented some type of bacterial translocation, and that as from 48 hours of study, there was an increase in the number of children with tracheal colonization by potentially pathogenic bacteria, corroborating the work of researchers who consider the time of tracheal intubation of longer than 48 hours to be a factor of elevated risk for the development of pneumonia.

Aspiration of gastric contents is another potential risk factor for the occurrence of pneumonia, since the stomach serves as a reservoir for bacteria. The majority of critically ill patients are submitted to gastric or post-pyloric intubation for gastric decompression, nutritional or therapeutic support. The insertion of tubes into the nostril has been associated with greater risk for the development of sinusitis, which consequently increases the possibility of alteration in oropharyngeal colonization, since the bacteria present in the paranasal sinuses may migrate to this region.(7) Moreover, when gastric or post-pyloric tubes are used, occlusion of the esophageal sphincter is harmed, generating a potential risk for gastric reflux. Once reflux occurs, the upper airways are exposed to a high number of bacteria that may still migrate to the oropharynx by means of the external wall of the tubes.(7) In the present study, only two children were not submitted to gastric or postpyloric intubation.

Around 90.0% of the children included in this investigation received medications that alter gastric pH. The elevation of gastric pH, as occurs in patients submitted to stress ulcer prophylaxis, may favor an increase in the concentration of gram-negative bacilli in the gastric secretion, causing retrograde colonization from the stomach to the oropharynx and trachea, thus making these patients more susceptible to respiratory infections.(4)

Nevertheless, in spite of this fact, recent researches have suggested that although the stomach is frequently colonized by enteric gram-negative bacilli, it is not the primary source for colonization of the lower respiratory tract by nosocomial pathogens. Microorganisms responsible for the occurrence of pneumonia in adult patients submitted to intensive therapy have been commonly identified, primarily in the oropharyngeal region.(8,9) In a similar matter, a study conducted in a Brazilian PICU revealed that around 41.8% of the 55 studied children presented potentially pathogenic species of microorganisms colonizing the oropharynx at the time of admission to the unit.(10)

All the children included in this study presented oropharyngeal colonization within the first 24 hours of tracheal intubation, either by bacteria of the normal oropharyngeal microbiota or by potentially pathogenic bacteria, whereas gastric colonization in this period was identified in 14 of the 30 children. Of these 14 children, 7 presented enterobacteria in the gastric secretion.

A study conducted in critically ill adult patients without infection on admission to an ICU, demonstrated a 90% rate of colonization, with predominance of gram-negative bacilli, such as K. pneumoniae, P. aeruginosa, E. coli and Enterobacter spp in addition to gram-positive microorganisms such as S.aureus and S. bovis. It was verified that the oropharynx was the first site to be colonized, within approximately 36 hours of hospitalization, followed by the gastric region, and finally the lower respiratory tract.(11) Similar results were found by other researchers who verified that the main source of microorganisms for secondary colonization of the trachea in critically ill adult patients was the oropharynx, and the oropharynx and stomach concomitantly. (12,13)

In a similar manner, it was verified that up to the time interval of 48 hours of study, there was a rise in the number of children who presented oropharyngeal colonization, consequently, translocation of microorganisms from the oropharynx to the trachea was also more frequent, followed by absence of translocation. Gastric translocation was shown to be less frequent as it occurred in only 3.3% of the children.

These data suggest that although the stomach may represent a source of microorganisms that colonized the tracheobronchial tree, in the pediatric population also, it is not the most significant source of bacteria causing respiratory infections. Thus the importance is emphasized, of the oropharyngeal area as a reservoir of microorganisms that cause tracheal colonization.

The normal microbiota of the oropharynx in non intubated patients is predominantly composed of gram-positive species and anaerobic microorganisms. During the period of hospitalization in the ICU the oral micro-biota is replaced by gram-negative and gram-positive pathogenic aerobic bacilli.(14) Research conducted in adults has shown that on admission to an ICU, patients were mainly colonized by species of microorganisms such as S. aureus, H. influenzae and S. pneumoniae, and that during the course of hospitalization there was rapid replacement of the normal oropharyngeal microbiota by gram-negative bacilli, such as P. aeruginosa.(15)

The predominance of the species of normal micro-biota such as, coagulase-negative Staphylococcus, viridans Streptococcus and Moraxella spp, in the oropharynx and trachea cultures of the children included in this study was similar to the results shown by an epidemiological study developed in populations of children at risk for the acquisition of gram-negative aerobic bacilli. (16)

There was also predominance of pathogenic bacteria such as Enterobacter spp, K. pneumoniae and P. aeruginosa, in the cultures of oropharyngeal and tracheal secretions, a result similar to that found in other studies that demonstrated that colonization of the oropharynx by gram-negative pathogens is an almost universal occurrence in critical patients submitted to MPV. (8,13,17)

Risk factors for the development of pneumonia may be divided into three categories: those related to the host, equipment and devices, and to the professionals. Host-related risk factors include: pre-existent conditions such as immunosuppression and chronic diseases, acute respiratory diseases, position in the bed, level of consciousness, number of tracheal intubations, and use of medications such as antibiotics and sedative.(17)

The children included in this study consisted of a group of patients with varied characteristics, which may be considered risk factors for the increase in oropharyngeal, gastric and later tracheal colonization. Among these factors, the use of drugs that may alter the pattern of colonization may be pointed out, such as antibiotics, central nervous system depressants, and gastric protectors, gastric tubing and the process of tracheal intubation itself.

Preventive measures must be implemented to diminish bacterial translocation to the trachea, particularly in groups of patients who have diverse risk factors for the occurrence of this event, such as the children who participated in this study. Moreover, extra-careful attention must be paid to populations that are known to present oropharyngeal and gastric colonization by potentially pathogenic bacteria at the time of admission to intensive care units.

In this context, nurses have been considered the first line of defense in the prevention of bacterial colonization of the oropharynx and gastrointestinal tract and translocation of bacteria to the lungs, with the exception of interventions that must be implemented by these professionals, such as: meticulous hand hygiene, oral hygiene, tracheal aspiration without the instillation of saline solution, aspiration of oral cavity secretions, maintenance of adequate pressure of the tracheal cuff, evaluation of the need for changing the circuits of MPV apparatuses, changes of the patient's decubitus position in the bed, maintenance of the decubitus position elevated to 30º, monitoring the distension and residual gastric volume and the careful use of sedative drugs.

Knowledge of the characteristics of the population attended, of the prevailing bacterial colonization pattern and the risks for the occurrence of bacterial translocation, which expose the child to elevated risk for developing health-care related infections, provide the nurse with scientific knowledge that contributes to improvement of the assistance rendered and a reduction in adverse events arising from a practice without foundation.

Limitation of the study

It was not possible to attain a larger sample of children with data collection in the PICU of a single hospital in a reasonable period of time.



Critically ill children may present factors for an increase in bacterial colonization and translocation from the gastrointestinal region to the trachea. In a sample of 30 children hospitalized in a Pediatric Intensive Care Unit, a high frequency of oropharyngeal colonization by pathogenic microorganisms and translocation of these bacteria to the trachea was found in around half of the children admitted to this study.

Acknowledgements: The authors thank the Fundação de Amparo à Pesquisa do Estado de São Paulo - FAPESP, Dr. Antonia Maria Machado and professionals of the microbiology laboratory, Prof. Dr. Werther Brunow de Carvalho, and the Nursing Team of the PICU for their help with the study.



1. Foglia E, Meier MD, Elward E. Ventilator-associated pneumonia in neonatal and pediatric intensive care unit patients. Clin Microbiol Rev. 2007;20(3):409-25.         [ Links ]

2. National Nosocomial Infections Surveillance (NNIS) System report, data summary from January 1992 through June 2004, issued october 2004. Am J Infect Control. 2004;32(8):470-85.         [ Links ]

3. Edwards JR, Peterson KD, Andrus ML, Dudeck MA, Pollock DA, Horan TC; National Healthcare Safety Network Facilities. National Healthcare Safety Network (NHSN) Report, data summary for 2006 through 2007, issued November 2008. Am J Infect Control. 2008;36(9):609-26; discussion 739-41.         [ Links ]

4. Safdar N, Crnish CJ, Maki DG. The pathogenesis of ventilator - associated pneumonia: its relevance to developing effective strategies for prevention. Respir Care. 2005;50(6):725-39; discussion 739-41.         [ Links ]

5. Robert R, Grollier G, Frat JP, Godet C, Adoun M, Fauchère JL, Doré P. Colonization of lower respiratory tract with anaerobic bacteria in mechanically ventilated patients. Intensive Care Med. 2003;29(7):1062-8.         [ Links ]

6. Augustyn B. Ventilator-associated pneumonia: risk factors and prevention. Crit Care Nurse. 2007;27(4):32-6;38-9; quiz 40.         [ Links ]

7. Grap MJ, Munro CL, Unoki T, Hamilton VA, Ward KR. Ventilator-associated pneumonia: the potential critical role of emergency medicine in prevention. J Emerg Med. 2012 Mar;42(3):353-62.         [ Links ]

8. Garrouste-Orgeas M, Chevret S, Arlet G, Marie O, Rouveau M, Popoff N, et al. Oropharyngeal or gastric colonization and nosocomial pneumonia in adult intensive care unit patients. A prospective study based on genomic DNA analysis. Am J Respir Crit Care Med. 1997;156(5):1647-55.         [ Links ]

9. Chen YC. Critical analysis of the factors enteral feeding in preventing VAP: a systematic review. J Chin Med Assoc. 2009;72(4):171-8.         [ Links ]

10. Kusahara DM, Peterlini MAS, Pedreira MLG. Children's oropharyngeal colonization upon admission at a pediatric intensive care unit. Acta Paul Enferm. 2007;20(4):421-7.         [ Links ]

11. Pneumatikos IA, Dragoumanis CK, Bouros DE. Ventilator-associated pneumonia or endotracheal tube-associated pneumonia? An approach to the pathogenesis and preventive strategies emphasizing the importance of endotracheal tube. Anesthesiology. 2009;110(3):673-80.         [ Links ]

12. de Latorre FJ, Pont T, Ferrer A, Rosselló J, Palomar M, Planas M. Pattern of tracheal colonization during mechanical ventilation. Am J Respir Crit Care Med. 1995;152(3):1028-33.         [ Links ]

13. Cardeñosa Cendrero JA, Solé-Violán J, Bordes Benitez A, Noguera Catalán J, Arroyo Fernández J, Saavedra Santana P, et al. Role of different routes of tracheal colonization in the development of pneumonia in patients receiving mechanical ventilation. Chest. 1999;116(2):462-70.         [ Links ]

14. Scannapieco FA, Stewart EM, Mylotte JM. Colonization of dental plaque by respiratory pathogens in medical intensive care patients. Crit Care Med. 1992;20(6):740-5.         [ Links ]

15. Ewig S, Torres A, El-Ebiary M, Fábregas N, Hernández C, González J, et al. Bacterial colonization patterns in mechanically ventilated patients with traumatic and medical head injury. Incidence, risk factors, and association with ventilator-associated pneumonia. Am J Respir Crit Care Med 1999;159(1):188-98.         [ Links ]

16. Donowitz LG, Page MC, Mileur BL, Guenthner SH. Alteration of normal gastric flora in critical care patients receiving antacid and cimetidine therapy. Infect Control. 1986;7(1):23-6.         [ Links ]

17. Rotstein C, Evans G, Born A, Grossman R, Light RB, Magder S, et al. Clinical practice guidelines for hospital-acquired pneumonia and ventilator-associated pneumonia in adults. Can J Infect Dis Med Microbiol. 2008;19(1):19-53.         [ Links ]



Corresponding Author:
Denise Miyuki Kusahara
Escola Paulista de Enfermagem
Rua Napoleão de Barros, 754, S113. Vila Clementino
São Paulo - CEP: 04024-002

Received article 31/05/2011 and accepted 27/09/2011



* Part of the institutional project, "Mental Health in primary care: perspectives and intervention", linked to the Post-graduate Program (Master's) in Nursing, State University of Maringá - UEM, Maringá (PR), Brazil.

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