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Nicholas McManus

Nicholas McManus

Chest Tube Management Pearls

Chest tubes…most providers can put them in. You learn the skills in residency, but there are some significant gaps in knowledge of what needs to happen after the tube. If your skills on management are lacking, here are some pearls to catch you back up to speed.
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First...some necessary basic review

The pleural space is the cavity between the membrane lining of the lung (visceral pleura) and the inner lining of the chest cavity (parietal pleura). It’s function is to prevent friction between the outer lining of the lung and the inner lining of the thoracic cavity during respiration and to hold the two pleural surfaces together, creating negative pressure (a vacuum) that keeps the lungs expanded.

The lungs are elastic and naturally tend to collapse or recoil, but in normal conditions, the pleural space causes the outer lining of the lung to adhere to the lining of the chest cavity. This keeps the lungs expanded to proper position during inspiration and expiration. 

The pleural space is normally filled with approximately 50 mL of fluid, only enough to essentially provide a thin coating of fluid for the lubrication. Small increases in volumes of air and/or fluid can be absorbed by the body, whereas larger volumes prevent the lung from expanding to the full potential. Breathing is obviously compromised when this excess air and/or fluid enter the pleural space.

Chest Tube Purpose

The chest cavity is normally under negative pressure. When there is an accumulation of positive pressure, a chest tube is needed to drain body fluids or facilitate the re-expansion of a lung. A chest tube can also be used to provide intrinsic rewarming in a hypothermic patient.

Indications

Indications

Pneumothorax, Hemothorax, Hemopneumothorax, Plaural effusions, Chylothorax, Penetrating chest trauma, Pleural empyem, Post cardiac surgery drainage, Hypothermia, Need for pleurodesis, Chemotherapy administration

Contraindications

Contraindications

*No absolute contraindications* Multiple adhesions, Giant blebs, Coagulopathies, Risks outweigh the benefits

Selecting Chest Tube Size

ATLS 10th Edition Update

    • Prospective analysis has shown 28–32 F to effectively drain hemothorax (not 36-40, like it used to be). 

Patient Positioning

Adults:

    • Place in the supine position with ipsilateral arm abducted and elbow flexed with patients hand above head.
    • If not traumatic (concerned about spinal injury or time), slightly raise the head of the bed to 30 degrees for comfort.

Children:

    • Pediatric patients should have the head of the bed elevated to 30 degrees and consider NG tube to decompress the stomach if the child is suspected of having a high diaphragm on chest x-ray (if time permits).

Insertion Site

Depends on indication for tube…

Traditional Approach: 

      • Used for most everything but a simple spontaneous pneumothorax
      • 4th-5th intercostal space in anterior axillary or mid-axillary line.
      • Landmarks in trauma are nipple line in males sand inframammary crease in females.

Anterior approach:

    • 2nd intercostal space in the midclavicular line.
    • Requires tube to go through pectoralis muscle.
    • Only use with simple uncomplicated pneumothorax with a 10-14 Fr pigtail catheter.
    • In a prospective randomized trial of 40 patients with diagnosis of an uncomplicated post-traumatic pneumothorax aa 14-Fr pigtail catheter inserted in the 2nd intercostal space, midclavicular line vs 29 Fr catheter in the standard 5th intercostal space was associated with reduced pain at insertion site with no other clinically important differences compared with chest tubes (Kulvatunyou, 2014)

The position of the chest tube placement is determined by the intended function of the tube:

    • If used to drain air: the tube may be placed anteriorly near the apex of the lung.
    • If used to drain fluid: it may be positioned posteriorly near the base of the lung.
    • If used for Hemothorax: it may be positioned at apex as well as the lung base. More than one tube may be necessary. 

Indications for Open Thoracotomy after chest tube placement in Trauma

Are Prophylactic Antibiotics needed?

Penetrating Trauma: Prophylactic antibiotics decrease the risk of empyema (RR 0.19) and pneumonia (RR 0.44) and are therefore warranted (Olgac 2006).

Spontaneous Pneumothorax: Prophylactic antibiotics are not warranted for spontaneous pneumothorax as it has not been shown to be necessary with increased risk of medication adverse effects and likely contributes to antibiotic resistance (Olgac 2006).

Applying the dressing

Dressings are not universal, but the concept is the same…

    • Steps to applying a chest tube dressing:
      • Use sterile technique.
      • Surround the chest tube insertion site with Xeroform to create an air-tight seal.
      • Slide a pre-slit 4×4 around the chest tube on the skin around the tube. What the heck, place a second pre-slit 4×4 on top of that (just don’t let the slits line up. 
      • Apply two additional intact 4×4’s over these and covering chest tube.
      • Using foam tape, secure the dressing with an airtight seal.

Basics of the Chest Drainage Unit (CDU)

Chest Drainage Unit

    • A device used to collect chest drainage (air, blood, effusions) and connects to the end of the chest tube.
    • Most commonly, drainage devices use a single unit that has 3 chambers and modeled after the old 3-bottle system.

Bottle #1 (fluid collection)

    • In a traditional water seal operating system, fluids drain from the patient directly into a large collection chamber through a 6-foot tube.

Bottle #2 (underwater seal)

    • One way valve that allows air to exit the chest and prevents air returning to the patient.
    • Air bubbling through the water seal chamber intermittently is normal when the patient coughs or exhales.
    • Continuous air bubbling in the chamber indicates an air leak that should be evaluated.
    • The water seal chamber is connected in series to the collection chamber, and allows air to pass down through a narrow channel and bubble out through the bottom of the water seal.
    • Since air cannot return to the patient, an underwater seal is considered one of the safest ways of protecting the patient, in addition to being a very useful diagnostic tools.
    • In a wet system, the underwater seal column is calibrated and acts as a water manometer for measuring intrathoracic pressure. As changes in intrathoracic pressure occur, fluctuations in the water level can be observed in this calibrated column and may provide clinicians with an indication of how the patient is progressing. More on this later.

Bottle #3 (suction control)

    • Suction helps overcome an air leak by improving the rate of air and fluid flow out of the patient.
    • The simplest and most cost effective means of controlling suction is by using a suction control chamber (wet system setup), which is an atmospherically vented section containing water and is connected in series with the water seal chamber and collection chamber.
    • By adding or removing water in a suction control chamber, the chest drain effectively controls the amount of suction imposed on the patient.
    • The lower the water content, the lower the imposed suction.
    • The higher the water level, the higher the imposed suction.

Types of Chest Drainage Units

Setting up the Chest Drainage Unit

Setting the Level of Suction

Typical initial level of suction is -10 to -20 cm H2O.

Spontaneous pneumothorax:

    • Use the least amount of suction to maintain full lung expansion.
    • Start with water seal, no wall suction.
    • There is no evidence to support routine use of wall suction (Ayed, 2003).

Fluid drainage:

    • -20 cm H2O is a reasonable starting point and increase to pressure necessary to achieve full lung expansion.
    • For very large effusions, initially avoiding suction may decrease the risk of re-expansion pulmonary edema (Sherman, 2003).

Penetrating chest trauma:

    • Surprisingly little data on this topic, and the limited data is mixed.
    • Early literature suggested suction improved expansion of the lung and prevented retained hemothorax.
    • However, a 2014 randomized controlled trial found no benefit to negative pleural suction over water seal without suction in patients with uncomplicated traumatic pneumothorax, hemothorax or hemopneumothorx (Morales, 2014).

Verify Operation


Observe Water Seal Operation

Observe Water Seal Operation

    • Must be filed and maintained at the 2 cm level.
    • Additional sterile water may be added by syringe via the grommet located on the back.


Verify Suction

Wet System:

    • Verity water is filled to -20 cmH20 in the suction control chamber.
    • A continuous gentle bubbling will be appreciated.
    • Adjust suction control stopcock if necessary. 

Dry System:

    • Observe the suction monitoring bellows
    • Bellows must be expanded to the triangular mark or beyond for a -20 cmH20 or higher regulator setting.


Tidaling

  • The water level should fluctuate in the water seal chamber
  • Corresponds to respiration

Patients not on Mechanical Ventilation

    • Inhalation = water level should rise
    • Exhalation = water level should fall

Patients on Mechanical Ventilation

    • The opposite occurs

* If the lung is re-expanded, tidaling may not be present


Assess for Air Leaks

  • It is important to rectify air leaks because an airtight system is necessary to effective lung expansion (develop negative pressure in the thoracic cavity).

Assessing for air leak

    • Clamp off suction for 1 minute
    • Air leak is present if there is constant bubbling in the water-seal chamber.
    • Starting away from the patient, check all connections. work up towards the patient. Finally, assess the dressing.

Intermittent bubbling with respiration is expected if the pleural space is leaking (such as in a pneumothorax). However, this should decrease as the pneumothorax improves.


Check Tubing Connections

  • Keep all tubing patent and free of kinks.
  • Avoid dependent loops as they obstruct drainage and increase positive pressure in the chest cavity.
  • It is acceptable to gently milk the tubing if a visible clot is obstructing drainage (squeezing hand-over-hand).
  • DO NOT STRIP the tubing as it can result in transient high negative pressure in the pleural space.
  • When ambulating the patient, the drainage unit must be carried at a level below the patient’s chest.

Changing the Chest Drainage Unit

  • Instruct the patient to exhale and hold his or her breath (perform the valsalva). 
  • Clamp the chest tube with a padded Kelly clamp 1-2” from the patient.
  • Place a second clamp distally.
  • Aseptically, disconnect tubing from old chest drainage unit and connect to the new chest drainage unit.
  • When completed, remove clamps within one minute and have patient breath normally.
  • Secure all connections with tape.

Monitoring Intrathoracic Pressure (wet systems only)

If the chest tube is not connected to suction, it is utilizing gravity to drain fluid from the chest cavity.

Assessing Intrathoracic pressure while OFF suction

    • Read directly from the water seal
    • A rise in water seal = negative pressure is present = patient is healing (good)
    • Bubbling = positive pressure is present = air leak (not good)

Calculating intrathoracic pressure while ON suction

    • Add the readings of suction control chamber + the level of the water seal chamber.
      • Ex: -20 cm H2O + – 5 cm H2O = -25 cm H2O.

Addressing Complications

Air Leak

    • Using a padded clamp, begin at the dressing and clamp the drainage tubing momentarily. If the bubbling stops, the air leak is at the chest tube insertion site or in the lung.
    • If bubbling continues, check the drainage tubing by moving down the drainage tubing in 20 cm intervals toward the chest drainage unit
    • Check the water-seal/air leak meter chamber for resolution of bubbling each time you clamp
    • When you place the clamp between the source of the air leak and the water-seal/air leak meter chamber, the bubbling will stop.

Chest tube accidentally falls out of chest

    • Instruct the patient to perform the Valsalva maneuver.
    • At end expiration, immediately cover the insertion site with Vaseline gauze, a dry sterile dressing and occlusive tape.

Chest drainage tube becomes disconnected but is NOT contaminated

    • Clean both sides of the connection with alcohol or iodine prior to reconnecting
    • Secure with zip-ties or tape to reinforce connection

Chest drainage tube becomes disconnected and IS contaminated

    • Submerge the tube 1” to 2” (2-4 cm) below the surface of a 250 mL bottle of sterile water or saline solution until a new CDU is set up.
    • This establishes a water seal, allows air to escape, and prevents air re-entry. 

Bleeding at the chest tube insertion site

    • Apply pressure to the site and monitor.

Subcutaneous emphysema

    • Occurs when air or CO2 is trapped in the SubQ tissue.
    • Frequently seen on the face, neck or chest.
    • Appreciated as crepitus (crackling sensation under skin) sometimes described as “Rice Krispies” under skin
    • Usually painless.
    • In most cases, surrounding tissue will absorb the SCE after underlying cause is treated. 

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Malposition of the Tube

    • Most common complication, occurring in 26% of chest tubes (Lim, 2005).
    • 80% not diagnosed until CT scan is obtained (usually missed on plain x-ray).
    • Therefore, obtain a CT scan if concerned about a malpositioned tube
    • Leave the tube in place and consult pulmonology or cardiothoracic surgery prior to making any changes if the patient is stable
    • Intra-parenchymal chest tubes should not be removed until aa second functional chest tube is in place.
    • Prepare to manage bleeding and massive air leak after malpositioned tube is removed. 

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Reexpansion Pulmonary Edema (RPE)

    • Rare (< 1 % incidence)
    • Mortality estimated at 5-20% (Feller-Kopman, 2007)
    • Typically occurs soon after chest tube placement, but can be delayed up to 48 hours. 
    • To prevent RPE, clamp the chest tube if patient starts to develop severe coughing, chest pain, shortness of breath or oxygen desaturation before resuming drainage and limit initial drainage to 1.5 liters in adults, 20 cc/kg in children and waiting at least 1 hour before draining any more fluid.
    • Patients with mediastinal shift may tolerate larger initial volumes of fluid removal because the lung will not re-inflate until the mediastinum is back to midline, and RPE begins when the lung starts to reinflate (American Thoracic Society).
    • RPE is usually self limited and treatment is supportive (fluid restriction, positioning, positive pressure ventilation)
    • No specific treatments have been recommended (Kira, 2014).

Criteria for Discontinuing the chest tube

Remove as soon as possible to decrease risk of infection…

Pneumothorax:

    • The lung is fully expanded.
    • No air leak for at least 24 hours (some experts suggest 48 hours).
    • Air does not accumulate when suction is removed and the tube is clamped for at least 6 hours, although literature is mixed on timing and necessity of this (Baumann, 2001).
    • There are no specific studies on optimal removal in mechanically ventilated patients. Some providers maintain the chest tube until mechanical ventilation is discontinued. However, this has not been studied and removal of the tube should occur as soon as is safe by the same criteria used in a non-vented patient to decrease the risk of infection.
    • One study suggest the removal of a chest tube in a patient on mechanical ventilation, who meet criteria for removal, can safely be done 5-7 days after insertion without increased risk of complications (Paydar, 2015). 
    • Leaving a chest tube in place for longer than 7 days significantly increases the risk of infection (Kao, 2013).

Effusion (Hemothorax, Serous Effusion, Empyema): 

    • The lung is adequately expanded.
    • Daily sero-sanguinous fluid output < 200 mL/day (Paydar, 2015)
      • The timing of chest tube removal based on 24 hour fluid output is not well studied and recommendations vary. One study even suggests safe to remove when output over 24 hours is > 450 mL in post-surgical patients (Zardo, 2015).
    • Empyema should be near completely resolved (< 20 cc/24 hours). There may still be small pockets of fluid remaining with empyema, but as long as patient is clinically improved (afebrile, no leukocytosis, tolerating diet), the tube may be removed and antibiotics continued.

Use of Ultrasound for Chest tube Management

Point-of-care ultrasound has been shown to provide rapid and accurate assessment for pneumothorax and well described in literature. The presence of lung sliding or lung pulse excludes pneumothorax at the point of the probe, with a negative predictive value of 100% (Lichtenstein, 1995, 2005). The most specific sign of pneumothorax is the presence of a lung point, with 100% specificity for pneumothorax (Lichtenstein, 2000). 

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Is Ultrasound better than Chest X-ray in the diagnoses of pneumothorax?

Chest x-ray can miss 30-50% of pneumothoraxes in trauma patients and ultrasound has higher sensitivity than chest x-ray with near equal specificity (Rowan, 2002).

Blaivas, 2005

    • Prospective study of 176 patients comparing bedside ultrasound in the emergency department with supine portable AP chest radiography for the detection of pneumothorax in trauma patients.
    • Standard criterion used was computed tomography.
    • Results:
      • Chest X-ray Sn = 75.5% and Sp = 100%
      • Ultrasound Sn = 98.1% and Sp = 99.2%

Wilkerson, 2010

    • Evidence‐based review of Four prospective observational studies, with a total of 606 patients included.
    • Compared sensitivity of bedside US and AP chest radiographs in identifying pneumothorax after blunt trauma.
    • Results:
      • Chest X-ray Sn = 28-75% and Sp = 100%
      • Ultrasound Sn = 86-98% and Sp = 97-100%

Saucier, 2010

    • Prospective observational comparison study of 50 cardiothoracic patients with surgically placed pleural chest tubes.
    • Assessed the accuracy of bedside ultrasound compared to standard chest radiography to detect pneumothorax.
    • The sample kappa statistic was 1.000, indicating a perfect agreement between bedside ultrasonography and chest radiography in the detection of pneumothorax. 
    • Completion of the bedside ultrasound procedure took significantly less time than chest radiography.

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Can Ultrasound be used to predict success of chest tube removal?

Lavingia, 2014

    • Used resident physicians with only basic knowledge of ultrasound.
    • Goal was to see if chest x-ray for removal of tube thoracostomy when performed by resident physicians with limited US training could predict save chest tube removal. 
    • All residents were provided at least 1 hour of ultrasound training. 
    • 49 patients included in the study.
    • Included pneumothorax in 37 (76%), hemothorax in seven (14%), hemopneumothorax in four (8%), or a pleural effusion in one (2%)
    • Recurrent pneumothorax occurred in 2 patients. This was similar to failure rate described by chest x-ray in prior studies. 
    • Concluded that ultrasound was able to successfully predict safe removal and patient discharge at all residency levels after receiving basic US training.

Patella, 2018

    • 50 patients undergoing lung resections.
    • Inclusion criteria were complete expansion of the lung at postoperative CR, pleural effusion of less than 300 mL/24 h, air leak of 10 to 20 mL/min for 6 hours.
    • Two hours after chest drain removal, LUS was performed at the second and third intercostal spaces to assess pleural sliding.
    • LUS has a negative predictive value of 100% in excluding large PTxs and a positive predictive value of 71%.

M
Criteria for chest tube removal by ultrasound

    • Linear array probe in longitudinal orientation
    • Scan midclavicular line in the first three interspaces
    • If no pneumothorax seen, connect to water seal for at least 6 hours
    • Chest tube could safely be removed if lung sliding, comet tail artifacts in B mode and “seashore sign” in M mode seen at all 3 sites (designated by red circles in figure to the left) after 6 hours.
    • Repeat bedside ultrasound 4-6 hours after chest tube removal

How to remove a chest tube

  1. Stack Xeroform Petrolatum gauze dressing on a nonadhesive dressing.
  2. Tape three sides of the dressing over the tube with foam tape.
  3. While keeping a fourth piece of tape ready, snip the sutures holding the tube in place.
  4. Have the patient take a deep breath.
  5. At the end of inspiration, put gentle pressure on the dressing with one hand and swiftly pull out the chest tube with the other.
  6. Keep the dressing hand in place and apply tape to the remaining side of the gauze.

Can Chest Tubes be managed outpatient?

Ponn, 1997

    • Review of charts from 240 patients over a 7 year period who were discharged from the hospital with chest tubes and Heimlich valves.
    • Diagnostic groups included pneumothorax (176 cases), prolonged postresection air leak (45 cases), and outpatient thoracoscopic pulmonary wedge excision (19 cases).
    • Showed a 4.5% failure rate defined as hospital admission for complication of tube function without any life threatening complications.
    • Cost saving of 1,263 inpatient hospital days
    • Study suggests that select patients with primary spontaneous pneumothorax may be candidates for outpatient treatment.

Heimlich Chest Drainage Valve (aka: flutter valve)

The Heimlich valve is an alternative to larger chest drainage units. It is most commonly used for smaller pneumothorax. It connects directly to the chest tubing and allows air to pass in one direction only and regulated suction can be attached, if necessary.

    • Advantages:
      • Functions in any position
      • Does not need to be clamped
      • The valve drains into a plastic bag which can also be held in any position
    • Disadvantages:
      • More prone to clogging of the tube
      • Fluid commonly leaks from valve (can attach a sputum collection cup to catch).

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References

  1. American Thoracic Society. Management of malignant pleural effusions. Am J Respir Crit Caare Med. 2000 Nov;162(5):1987-2001.
  2. Ayed AK. Suction versus water seal after thoracoscopy for primary spontaneous pneumothorax: prospective randomized study. Ann Thorac Surg.2003;75(5):1593.
  3. Baumann MH, Strange C, et al. Management of spontaneous pneumothorax: an American College of Chest Physicians Delphi consensus statement. Chest. 2001;119(2):590.
  4. Blaivas M, Lyon M, Duggal S. A prospective comparison of supine chest radiography and bedside ultrasound for the diagno- sis of traumatic pneumothorax. Acad Emerg Med. 2005; 12(9): 844-849. doi: 10.1197/j.aem.2005.05.005
  5. Brunelli A, et al. Evaluation of a new chest tube removal protocol using digital air leak monitoring after lobectomy: a prospective randomized trial. Eur J Cardiothorac Surg. 2010 Jan;37(1):56-60.
  6. Feller-Kopman D, Berkowitz D, et al. Large-volume thoracentesis and the risk of reexpansion pulmonary edema. Ann Thorac Surg. 2007. 84(5):1656.
  7. Jensen K, et al. Early chest tube removal after video-assisted thoracic surgery lobectomy with serous fluid production up to 500ml/day. Eur J Cardiothorac Surg. 2014 Feb;45(2):241-6.
  8. Kao JH, Kao HK, Chen YW, et al. Chest tube duration in mechanically ventilated patients with acquired pneumotho- rax. Respir care. 2013; 58(12): 2093-2100. doi: 10.4187/resp- care.02273
  9. Kulvatunyou,N, Erickson L, et al. Randomized clinical trial of pigtail catheter versus chest tube in injured patients with uncomplicated traumatic pneumothorax. Br J Surg. 2014;101(2):17.
  10. Kira S. Reexpansion pulmonary edema: review of pediatric cases. Paediatr Anaesth.2014. 24(3):249.
  11. Lavingia KS, et al. Basic ultrasound training can replace chest radiography for safe tube thoracostomy removal. Am Surg. 2014 Aug; 80 (8):783-6.
  12. Lichtenstein DA, Menu Y. A bedside ultrasound sign rul- ing out pneumothorax in the critically III: Lung sliding. Chest. 1995; 108(5): 1345-1348. doi: 10.1378/chest.108.5.1345
  13. Lichtenstein DA, Mezière G, Lascols N, et al. Ultrasound di- agnosis of occult pneumothorax. Crit Care Med. 2005; 33(6): 1231-1238. doi: 10.1097/01.CCM.0000164542.86954.B4
  14. Lichtenstein D, Mezière G, Biderman P, Gepner A. The “lung point”: An ultrasound sign specific to pneumothorax. Intensive Care Med. 2000; 26(10): 1434-1440. doi: 10.1007/ s001340000627
  15. Lim KE, Tai SC, et al. Diagnosis of malpositioned chest tubes after emergency tube thoracostomy: is computed tomography more accurate than chest radiography? Clin Imaging. 2005. 29(6):401.
  16. Martino K, et al. Prospective randomized trial of thoracostomy removal algorithms. J of Trauma, Injury, Infection and Critical Care. 1999; 46: 369-373.
  17. Morales CH, Mejia C, et al. Negative pleural suction in thoracic trauma patients: A randomized controlled trial. J Trauma Acute Care Surg. 2014 Aug;77(2):251-5.
  18. Olgac G, Aydogmus U, et al. Antibiotics are not needed during tube thoracostomy for spontaneous pneumothorax: an observational case study. J Cardiothoraac Surg. 2006;1:43.
  19. Patella M, Saporito A, et al. Lung ultrasound to detect residual pneumothorax after chest drain removal in lung resections. Ann Thorac Surg. 2018 May;105(5):1537-1542. doi: 10.1016/j.athoracsur.2017.12.008. Epub 2018 Jan 11.
  20. Paydar S, Ghahraamani Z, et al. Tube thoracostomy (chest tube) removal in traumatic patients: What do we know? What can we do? Bull Emerg Trauma.2015. 3(2): 37-40. PMID 27162900.
  21. Ponn RB, Silverman HJ, Federico JA. Outpatient chest tube management. Ann Thoracic Surg.1997;64(5):1437.
  22. Rowan K, Kirkpatrick A, Liu D, Forkheim K, Mayo J, Nicolaou S. Traumatic pneumothorax detection with thoracic US: Correlation with chest radiography and CT-initial experi- ence. Radiology. 2002; 225(1): 210-214. doi: 10.1148/radi- ol.2251011102
  23. Saucier S, Motyka C, Killu K. Ultrasonography versus chest radiography after chest tube removal for the detection of pneumothorax. AACN Adv Crit Care. 2010. Jan-Mar;21(1):34-8. doi: 10.1097/NCI.0b013e3181c8013a.
  24. Sherman SC. Reexpansion pulmonary edema: a case report and review of the current literature. J Emerg Med.2003;24(1):23.
  25. Wilkerson RG, Stone MB. Sensitivity of bedside ultrasound and supine anteroposterior chest radiographs for the identifi- cation of pneumothorax after blunt trauma. Acad Emerg Med. 2010; 17(1): 11-17. doi: 10.1111/j.1553-2712.2009.00628.x
  26. Zardo P, et al. Chest tube management: state of the art. Curr Opin Anaesthesiol. 2015 Feb;28(1):45-9.
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