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(Chest. 1999;116:462-470.)
© 1999 American College of Chest Physicians

Role of Different Routes of Tracheal Colonization in the Development of Pneumonia in Patients Receiving Mechanical Ventilation*

José Antonio Cardeñosa Cendrero, MD; Jorge Solé-Violán, MD; Ana Bordes Benítez, MD; Javier Noguera Catalán, MD; Javier Arroyo Fernández, MD; Pedro Saavedra Santana, PhD and Felipe Rodríguez de Castro, MD, FCCP

* From the Servicio de Medicina Intensiva (Drs. Cendrero, Solé-Violán, and Fernández), Servicio de Microbiología (Drs. Benítez and Catalán), Catedrático de Estadística, Unidad de Investigación (Dr. Santana), and Sección de Neumología (Dr. de Castro), Hospital Ntra Sra del Pino, Las Palmas de Gran Canaria, Spain.

Correspondence to: J. Solé-Violán, MD, Servicio de Medicina Intensiva, Hospital Ntra Sra del Pino, C/Angel Guimerá, 93, 35010 Las Palmas de Gran Canaria, Spain; e-mail: jsole{at}correo.hpino.rcanaria.es


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objective: To evaluate the importance of the different pathogenic pathways involved in the development of ventilator-associated pneumonia (VAP).

Design: Prospective study.

Setting: An 18-bed medical and surgical ICU.

Patients: One hundred twenty-three patients receiving mechanical ventilation (MV).

Interventions: Tracheal, pharyngeal, and gastric samples were obtained simultaneously every 24 h. In cases where VAP was suspected clinically, bronchoscopy with protected specimen brush and BAL were performed. Semiquantitative cultures of pharyngeal samples and quantitative cultures for the remaining samples were obtained.

Results: Tracheal colonization at some time during MV was observed in 110 patients (89%). Eighty patients had initial colonization, 34 patients had primary colonization, and 50 patients had secondary colonization. Nineteen patients had VAP, and 25 organisms were isolated. For none of these organisms was the stomach the initial site of colonization. Gram-positive organisms colonized mainly in the trachea during the first 24 h of MV (p < 0.001). On the contrary, enteric Gram-negative bacilli (p < 0.001) and yeasts (p < 0.002) colonized the trachea secondarily. Previous endotracheal intubation (p < 0.005) and acute renal failure before admission to the ICU (p < 0.001) were associated with colonization by Pseudomonas aeruginosa; prior antibiotics were associated with colonization by Acinetobacter baumanii (p < 0.05) and yeasts (p < 0.006); and cranial trauma was associated with Staphylococcus aureus colonization (p < 0.035).

Conclusions: Although the stomach can be a source of organisms that colonize the tracheobronchial tree, it is a much less common source of the bacteria that cause VAP. The pattern of colonization and risk factors may be different according to the type of organisms involved.

Key Words: BAL • oropharyngeal colonization • protected specimen brush • stomach colonization • tracheal colonization • ventilator-associated pneumonia


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Nosocomial pneumonia (NP) is a common complication in patients receiving mechanical ventilation (MV), and NP is considered to be one of the most common causes of morbidity and mortality. The incidence in this population has ranged from 9 to 70%, depending on the severity of illness and the procedures and criteria that are used to establish the diagnosis.1 The overall mortality is considered to be 20 to 25%,2 although it remains uncertain whether the mortality results from the infection itself or from the severe underlying illness.3 4 5 6 7

Ventilator-associated pneumonia (VAP) develops when the aspiration or inoculation of microorganisms occurs in patients with impaired defense mechanisms. Although microorganisms may reach the distal airway after colonization of the trachea, oropharynx, or stomach, the importance of the different routes of colonization in the development of VAP remains uncertain. Some authors have suggested that the gastric reservoir may play an important role in the pathogenesis of VAP,8 9 10 11 12 but the role of the gastropulmonary route has not been assessed.13 14 15 16 Although many studies have been undertaken to clarify the pathogenesis of VAP, only a few studies have simultaneously monitored the colonization of the stomach and upper respiratory tract over time,13 15 16 17 18 19 20 21 thus establishing the diagnosis of pneumonia by acceptable reliable methods.15 16 20 21

The goals of this study were to evaluate the importance of the different pathogenic pathways by monitoring the colonization at these sites every 24 h and to establish the diagnosis of VAP by isolation of the pathogen from the distal airways.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Patients
From June 1996 to July 1997, we studied 136 patients admitted to our ICU who were expected to receive MV > 48 h and were without pulmonary infection. At the time of entry, the following data were recorded: age; gender; duration of hospital stay; location before ICU admission (emergency department, hospital ward, operating room, or transfer from another hospital); primary reason for ICU admission; and whether the surgery was elective or emergency (defined as an operation for an immediate life-threatening condition). We also recorded the history of COPD and other comorbid conditions; indication for ventilatory support; presence of coma (Glasgow Coma Score <= 8); acute renal failure (serum creatinine > 1.6 mg/dL and serum urea > 50 mg/dL); and APACHE II (acute physiology and chronic health evaluation) score.22 Body temperature, WBC count, PaO2/fraction of inspired oxygen ratio, and chest radiographs were also obtained on a daily basis. A total of 13 patients were excluded: 7 patients because of the impossibility of obtaining tracheal or oropharyngeal samples on some occasion, and 6 patients because of extubation before 48 h.

Sample Collection
Tracheal, pharyngeal, and stomach samples were obtained simultaneously during the first 24 h of tracheal intubation and every 24 h thereafter until a total of 14 days had expired or extubation had taken place. Tracheal samples were obtained using aseptic suction with a mucus collector. Pharyngeal samples were obtained from the posterior pharynx using a sterile cotton swab. Gastric samples were obtained by aspiration through the nasogastric tube, and the first 10 mL was discarded.

A fiberoptic bronchoscopy was performed and respiratory samples were obtained using a protected specimen brush (PSB) and BAL when the patients showed at least three of the following criteria: (1) fever > 38.5°C; (2) purulent tracheobronchial secretions; (3) leukocytosis (WBC count > 12 x 103 /µL); (4) leukopenia (WBC count < 4 x 103 /µL); and (5) new, progressive, or persistent (> 24 h) infiltrate on chest radiograph, the latter criterion being always present. When the clinical diagnosis of pneumonia appeared between 12:00 PM and 8:00 AM, the respiratory samples were obtained using nonbronchoscopic protected BAL (PBAL).

The bronchoscopic techniques of PSB and BAL in intubated patients have been described previously.23 No suction was applied before taking the specimens, and no local anesthetic agents were used. The sequence of sampling was always PSB followed by BAL. PBAL was performed by means of a special catheter (Combicath; Plastimed; Saint Leu La Foret Cedex, France).

Processing of Specimens
Pharyngeal samples were cultured and quantified in terms of none, 1+, 2+, and 3+. Quantitative bacterial and fungal cultures were obtained for the remaining specimens by means of calibrated loops. All the samples were inoculated onto blood agar, chocolate agar, and MacConkey agar and incubated (35°C for 48 h) in a CO2-enriched atmosphere. Samples obtained by PSB, BAL, and PBAL were also inoculated into Brucella agar with vitamin K and hemin, and incubated under anaerobic conditions for 48 h.

Bacterial counts >= 103 cfu/mL for PSB, >= 104 cfu/mL for BAL, and >= 103 for PBAL were used as the cutoff points to establish a positive result. Recovery of > 1% of squamous epithelial cells in the BAL specimen was considered an accurate predictor of heavy oropharyngeal contamination, ie, an unsatisfactory specimen.

Definitions
Tracheal colonization was defined as the presence of microorganisms in cultures of tracheal samples in the absence of clinical signs of respiratory infection. Tracheal colonization that occurred during the first 24 h of MV was defined as "initial tracheal colonization." Tracheal colonization that appeared after 24 h of MV without having been found previously in the other two sites was defined as "primary colonization." Isolation of the same microorganisms at the same time in the trachea and stomach or in the trachea and oropharynx was considered "concurrent." "Secondary colonization" was considered when the microorganisms isolated in the trachea were previously isolated in the stomach or oropharynx. Microorganisms that had the same antibiotype were considered to be the same. Microorganisms were grouped as follows: Gram-positive microorganisms (Staphylococcus aureus, Staphylococcus epidermidis, Streptococcus pneumoniae, Streptococcus agalactiae, Enterococcus spp, Streptococcus viridans, Corynebacterium spp); enteric Gram-negative bacilli (Enterobacter aerogenes, Escherichia coli, Serratia marcescens, Klebsiella pneumoniae, Proteus mirabilis, Citrobacter diversus); other Gram-negative bacilli (Haemophilus influenzae, Neisseria spp, Moraxella (Branhamella) catarrhalis); Pseudomonas aeruginosa; Acinetobacter baumanii; and yeasts.

Outcome and Diagnostic Categories
Subsequent changes in clinical outcome and radiographic findings were recorded, and alternative explanations for the findings, such as atelectasis or pulmonary edema, were always excluded. Atelectasis was diagnosed when a complete resolution of the infiltrates occurred during the first 48 h after their appearance. Cardiogenic and noncardiogenic pulmonary edema were diagnosed using pulmonary arterial catheterization and the response to appropriate therapy.

The diagnosis of pneumonia was established if one or more of the following criteria were fulfilled:

1. Consolidated foci and polymorphonuclear leukocyte accumulation in bronchi and adjacent alveoli at autopsy study, performed within 5 days after sampling procedures;

2. Positive results from blood or pleural fluid cultures;

3. Rapid cavitation of the lung infiltrate;

4. Appropriate clinical response while receiving specific antibiotic therapy for the organisms cultured from PSB or BAL in significant growth.

Pneumonia was considered excluded if at least one of the following criteria was fulfilled:

1. Full recovery without appropriate antimicrobial therapy or without changes in the antibiotic therapy initiated at least 72 h before the appearance of infiltrates;

2. No signs of bacterial pneumonia at autopsy when available within 5 days after sampling procedures;

The presence or absence of each of the following factors were recorded: prior antimicrobial therapy; presence of bacteremia; development of pneumonia-related complications; radiographic spread of the infiltrates; and APACHE II score at the time when pneumonia was diagnosed.

Thirty-two of 123 patients had received broad-spectrum antibiotics 5.12 ± 4.83 days before MV was initiated, and 79 patients received antibiotics at some time during the study. Of those patients who received antibiotics before inclusion in the study, 29 patients (90%) were receiving antibiotics with Gram-negative activity (59% antipseudomonal activity), and in 32 patients (100%), the antibiotics were effective against Gram-positive microorganisms.

No regimen for NP prophylaxis or selective decontamination of the digestive tract was used. When patients received enteral feeding (n = 41), it was performed with the patients in a semierect position. Nutrition was administered ideally into the jejunum (n = 8). When gastric nutrition was required (n = 34), it was administered in a continuous way, by turning the feeding off for 7 h and monitoring the volume of gastric content.

The study protocol was approved by the ethics committee of Hospital Ntra Sra del Pino.

Statistical Analysis
Data are expressed as mean ± SD. Univariate analysis was performed using {chi}2 for categorical variables, Student's t test for normally distributed variables, and Mann-Whitney U test for nonnormally distributed variables. The multivariate analysis was performed using a logistic regression technique. All categorical variables were entered with two categories (0 = absent; 1 = present). For those variables with more than two categories, a cutoff point was selected according to the results of univariate analysis. A p value < 0.05 was considered significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
A total of 123 patients were evaluated (mean age, 58.8 ± 16.9 years; range, 15 to 86 years). Ninety-four patients (76%) were men. The average duration of MV was 6.5 ± 4.2 days. The mean APACHE II score of the entire study population was 14.2 ± 5.13 (range, 3 to 26). The patients had been admitted to the ICU because of postoperative respiratory failure (n = 33); multiple trauma (n = 27); heart failure (n = 15); acute respiratory failure (n = 13); impaired consciousness as a result of neurologic disorders (n = 12); COPD (n = 5); and miscellaneous conditions (n = 18).

Patient characteristics are shown in Table 1 . Eighty-five of 123 patients (69.1%) were receiving MV in the subsequent 48 h after admission to the hospital. Thirty-two of 123 patients had received broad-spectrum antibiotics for 5.12 ± 4.83 days before MV was initiated, and 79 patients received antibiotics at some time during the study.


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  		Table 1. Clinical Characteristics of Patients According to the Presence of Tracheal Colonization*

 
A total of 2,316 microbiological samples were obtained from the 123 patients (772 gastric samples, 772 pharyngeal samples, and 772 tracheal samples). During the study, there were only three patients (2.43%) who did not have colonization from any of the three sites. Thirteen patients (10.5%) did not have tracheal colonization, 8 patients (6.5%) did not have pharyngeal colonization, and 20 patients (16.2%) did not have gastric colonization.

A total of 110 patients had tracheal colonization at some time during the study. In these patients, 545 tracheal samples showed bacterial growth, and 790 microorganisms were isolated. Two hundred fifteen tracheal samples (39.4%) were polymicrobial.

Univariate analysis showed a significant association between the presence of coma on admission and tracheal colonization (p < 0.05; Table 1 ). However, the stepwise logistic regression analysis did not identify any clinical characteristic as a predictor of tracheal colonization.

A total of 255 colonizations occurred in the 110 patients. Eighty patients (115 episodes) had tracheal colonization during the first day of MV. Univariate analysis showed a significant difference among patients with and without initial tracheal colonization (Table 2 ). Multivariate analysis selected the presence of coma on admission (p < 0.001; odds ratio [OR], 14.2) and smoking history (p < 0.002; OR, 4.8) as significant predictors of initial tracheal colonization. The regression analysis did not identify any clinical characteristic as a predictor of initial tracheal colonization by specific microorganisms.


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  		Table 2. Clinical Characteristics of Patients According to the Presence of Initial Tracheal Colonization*

 
Previous antibiotics with activity against Gram-positive cocci or microorganisms grouped as other Gram-negative significantly decreased initial tracheal colonization by these microorganisms (Table 2) .

In our study, 47 of 115 microorganisms that initially colonized the trachea had disappeared in < 48 h, either spontaneously (n = 22) or because of the effect of antibiotics (n = 25).

There were 70 primary tracheal colonizations (34 patients), 43 exclusive tracheal colonizations, and 27 concurrent colonizations (in which microorganisms appeared at the same time in the trachea and pharynx or in the trachea and stomach). Multivariate analysis selected the presence of previous cardiomyopathy (p < 0.05; OR, 3.72) and neurosurgical admission as significant predictors of primary tracheal colonization (p < 0.03; OR, 3.56).

Secondary colonization was observed in 70 cases (50 patients). In 26 colonizations, the source of the microorganisms was the oropharynx; in 15 colonizations, the source of the microorganisms was the stomach; whereas in 29 colonizations, the source was both the oropharynx and the stomach. The microorganisms responsible for secondary tracheal colonizations (grouped according to the time and type of colonization) are listed in Table 3 . Previous chronic corticosteroid treatment (p < 0.02; OR, 12.5) and diabetes (p < 0.01; OR, 4.8) were the factors that were predisposed to gastric secondary tracheal colonization.


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  		Table 3. Microorganisms Isolated in Tracheal Samples and Sources of Colonization*

 
Although 26 patients fulfilled the clinical criteria for pneumonia, the diagnosis of pneumonia was finally established in only 19 of the 123 patients, with a total of 21 episodes of pneumonia (17%). Diagnosis was obtained by means of PSB or BAL in 9 cases and PBAL in 11 cases; in the remaining 1 case, the diagnosis of pneumonia was finally established at autopsy. Twenty-five microorganisms were isolated (Table 4 ). There were five episodes of early-onset pneumonia (< 4 days of MV). Gram-negative bacilli were the most frequently isolated microorganisms in early-onset pneumonia, and S aureus was the most common microorganism in late-onset pneumonia (Table 4) .


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  		Table 4. Microorganisms Isolated in Patients With Pneumonia

 
Of the 25 microorganisms responsible for VAP, 22 had previously colonized the trachea, oropharynx, or stomach; in one case, previous colonization was not observed, and two cases were second episodes of VAP. Moreover, 22 microorganisms were colonizing the trachea an average of 3.63 ± 2.40 days before a definite diagnosis of pneumonia was obtained. Seventeen of the 25 microorganisms isolated at the time of VAP diagnosis had previously colonized the pharynx. Seven of the 25 microorganisms colonized the stomach before or at the time of VAP diagnosis (Table 4) .

For 11 microorganisms, the initial site of colonization was the trachea; for 4 microorganisms, the initial site was the oropharynx; and for 7 microorganisms, the initial site was either the oropharynx or the trachea. In no case was the stomach the initial site of colonization.

During the first day of MV, the most frequent organisms isolated were Gram-positive cocci and H influenzae. The colonization pattern was different according to the different microorganisms (Table 5 ). Gram-positive microorganisms colonized mainly the trachea during the first 24 h of MV (p < 0.001). On the contrary, enteric Gram-negative bacilli (p < 0.001) and yeasts (p < 0.002) colonized the trachea secondarily. The microorganisms grouped as other Gram-negative bacteria colonized the trachea both initially (p < 0.001) and primarily (p < 0.005). P aeruginosa and S aureus colonized mainly the trachea secondarily from the oropharynx (p < 0.05).


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  		Table 5. Microorganisms Isolated in Tracheal Samples According to Pattern of Colonization

 
There were certain factors in the multivariate analysis that predisposed to tracheal colonization with specific pathogens. Endotracheal intubation in the previous 2 weeks (p < 0.005; OR, 9.9) and the presence of acute renal failure before admission to the ICU (p < 0.001; OR, 9.0) were associated with colonization by P aeruginosa. The prior administration of antibiotics was a risk factor for colonization by A baumanii (p < 0.05; OR, 4.6) and yeasts (p < 0.006; OR, 3.4). Cranial trauma was strongly associated with S aureus colonization (p < 0.035; OR, 5.0). No relationship between mortality and the different patterns of colonization was observed.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Although there are several routes by which microorganisms may enter the lung and cause pneumonia, the aspiration of contaminated secretions from the oropharynx or stomach is considered to be the most common route.24 Given that aspiration of oropharyngeal contents is known to occur even in normal healthy individuals, it has been postulated that pathogens colonizing the oropharynx or stomach may reach the distal airways and eventually cause pneumonia. In patients receiving MV, the cuff of the endotracheal tube likely increases the probability of contamination of the airway, because the secretions are pooled in the subglottic region above the inflated cuff and leak around it, being too voluminous for removal by the mucociliary system.25 This process may be exacerbated in patients receiving enteral feeding or by the practice of maintaining patients in the supine position.4

In our study, 18 of 110 patients with tracheal colonization had pneumonia, compared to 1 of 13 patients who did not have tracheal colonization. These data support those of other authors who have found that tracheal colonization precedes pulmonary infection.26 On the other hand, the presence of tracheal colonization by itself does not appear to be a unique condition for VAP to occur, inasmuch as only a minority of patients with colonization have pulmonary infections. Factors other than tracheal colonization must be involved in the development of VAP.27

Although some studies have reported that tracheal colonization increased in patients receiving MV according to the duration of ventilation,28 most patients have evidence of tracheal colonization in the first 24 h of MV. In our study, 65% of the patients showed tracheal colonization during the first 24 h of MV, a finding that is similar to that reported by De La Torre et al16 in a recent article. It is also noteworthy that 77.3% of initial tracheal colonization was produced by Gram-positive cocci, H influenzae, or yeast, which might be explained by taking into account that 85 of 123 patients (69.1%) were receiving MV in the subsequent 48 h after admission to the hospital. Initial tracheal colonization in severely ill patients has not been well defined, and it is difficult to ascertain whether this situation reflects the aspiration of previously colonized secretions in critically ill patients or just the contamination of the trachea during the intubation procedure. In our study, 47 of 115 microorganisms had disappeared from the trachea in < 48 h, both spontaneously (n = 22) or because of the effect of antibiotic treatment (n = 25). This observation supports the hypothesis that initial tracheal colonization is in most cases a transient phenomenon that is related to the passage of microorganisms from the oropharynx to the trachea on intubation.19 29

Forty-three episodes of primary tracheal colonization were observed (34 patients) without previous colonization in any other site, suggesting an exogenous source that is difficult to identify because of the design of our study.

Although several studies have found a variety of risk factors associated with colonization of the upper respiratory tract,30 31 32 we have not found any difference between patients who experienced tracheal colonization at any time and patients who did not. The fact that there were few patients in our study who did not have tracheal colonization may explain these results because of the limited power of the sample.

As it has been reported in other studies, there were certain factors that predispose to colonization with specific pathogens.33 34 35 Prior endotracheal intubation and the presence of acute renal failure before admission to the ICU were associated with colonization by P aeruginosa. In the same way, the prior administration of antibiotics was a predictor of colonization by A baumanii and yeasts. Finally, the presence of trauma was a risk factor for colonization by S aureus.

The colonization pattern was different according to the different microorganisms. Gram-positive cocci show avidity for colonizing the trachea initially in comparison with both primary and secondary colonization. By contrast, enteric Gram-negative bacilli and yeasts colonize the trachea secondarily. The microorganisms grouped as other Gram-negative bacteria colonize the trachea both initially and primarily. P aeruginosa and S aureus show a tendency to colonize the trachea mainly from the oropharynx. Although some authors have found a different pattern of colonization for P aeruginosa less frequently in the stomach and oropharynx before being isolated in the trachea,16 35 we have not been able to confirm these data. Our study, on the other hand, would seem to confirm the hypothesis that different microorganisms have different colonization patterns.

The role of the stomach as a reservoir of microorganisms causing pneumonia is controversial. Although several studies have been undertaken to clarify whether or not gastric overgrowth increases oropharyngeal colonization and the risk for contamination of the tracheobronchial tree, definitive conclusions have not been achieved. Although some authors think that the stomach is a very important pathogenic route,8 9 10 11 12 other investigators do not.13 14 15 16 20 The relationship between gastric colonization and pneumonia comes from different studies that have observed previous or simultaneous gastric colonization before the development of pneumonia.8 9 10 However, only in a few studies have gastric and upper airway colonization been monitored simultaneously13 15 16 17 18 19 20 21 ; in even fewer studies have specific diagnostic methods been used.15 16 20 21

The incidence of NP observed in our study was 17.07%, which is close to that reported by other authors who have studied similar populations and used highly specific criteria to define pneumonia.36 Although our criteria for pneumonia are probably somewhat arbitrary, and most episodes might better be classified as probable pneumonia according to the guidelines of the American College of Chest Physicians,37 it is unlikely that many cases of true pneumonia would have been missed by these criteria. In our study, only 7 of the 25 microorganisms colonized the stomach at the same time as the oropharynx before or at the time of VAP diagnosis. In none of them was the trachea colonized secondarily from the stomach by the microorganism responsible for the pneumonia. These data support the findings reported by other researchers13 14 15 16 20 21 and seem to confirm that the stomach plays a limited role as a source of microorganisms causing VAP.

Although the duration of hospitalization is often used as a guide to predicting likely pathogens and, therefore, appropriate antimicrobial therapy, we have observed a considerable overlap between nosocomial flora and community-acquired flora in patients with early- and late-onset pneumonia, which may have implications for the empiric prescription of antibiotics.

Our study has the limitation of not having been able to explore a variety of other routes for bacterial entry into the lung, such as exogenous penetration or direct inoculation from hospital personnel into the airway of intubated patients. Moreover, most patients had received broad-spectrum antibiotics before inclusion in the study, which may have eradicated sensitive organisms. This might explain the lower risk of colonization observed in patients who had received antibiotics and the pattern of the colonizing flora in our patients.

In summary, the data show that although the stomach can be a source of organisms that colonize the tracheobronchial tree, the stomach is a much less common source of the bacteria that cause pneumonia. By contrast, our data emphasize the importance of the oropharynx as a reservoir of microorganisms that cause tracheal colonization and VAP. Our study also supports the hypothesis that the pattern of colonization may be different according to the type of microorganisms.


   Footnotes
 
Supported by grant FIS No. 98/0980.

Abbreviations: APACHE = acute physiology and chronic health evaluation; MV = mechanical ventilation; NP = nosocomial pneumonia; OR = odds ratio; PBAL = nonbronchoscopic protected BAL; PSB = protected specimen brush; VAP = ventilator-associated pneumonia

Received for publication July 23, 1998. Accepted for publication March 10, 1999.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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