You are on page 1of 6

Art & science respiratory nursing

Management of patients with empyema


Myatt R (2014) Management of patients with empyema.
Nursing Standard. 28, 30, 42-47. Date of submission: October 15 2013; date of acceptance: January 8 2014.

limited success. Management using intercostal


Abstract chest drains was widely adopted following an
Empyema is the term used to describe an accumulation of pus in a influenza epidemic in the early 20th century
body cavity such as the pleural space as a result of bacterial infection. (Davies et al 2010). This technique, combined
The condition is serious because it is difficult for the immune system with the introduction of antibiotics, helped to
to resolve infection in this area. Empyema can be avoided by the use of improve patient outcomes. Most cases of empyema
appropriate antibiotic therapy and good aseptic technique when dealing result from medical intervention, trauma or
with any situation that breaches the chest wall. Treatment of this pneumonia (Anyanwu et al 2004). The use of
condition may be medical but if the condition does not resolve, surgical prompt antibiotic therapy and aseptic technique
intervention is required. The nursing role involves providing support, when dealing with situations that breach the chest
education and long-term management for patients with empyema. wall can limit the risk of developing the condition.
Occasionally, empyema develops because of
Author oesophageal trauma or as a result of conditions
causing dysphagia, where food is aspirated leading
Rebecca Myatt to infection.
Nurse case manager, thoracic surgery, Guys Hospital, London. Treatment of patients with empyema is
Correspondence to: Rebecca.Myatt@gstt.nhs.uk frequently complex as a result of multiple
comorbidities and the involvement of many
Keywords healthcare professionals, both in hospital and the
Chest drain, clinical nurse specialists, empyema, nurse-led clinic, community. The specialist nurse has a significant
outpatient care, patient education, pleural infection role in the management of this condition,
especially liaising between interdisciplinary
Review teams, communicating with the patient and
family, providing education as well as physical and
All articles are subject to external double-blind peer review and psychological support, preparing the patient for
checked for plagiarism using automated software. discharge and acting as a contact person once the
patient has returned home.
Online
Guidelines on writing for publication are available at
Anatomy and physiology of the lungs
www.nursing-standard.co.uk. For related articles visit the archive
and search using the keywords above. The pleurae are a thin double layered membrane
surrounding the contents of the thoracic cavity.
The parietal pleura covers the inside of the chest
wall, the thoracic side of the diaphragm, the heart
EMPYEMA, the accumulation of pus in the and the area between the lungs, and the visceral
pleural space, may have a slow onset as the result pleura covers the external lung surface (Marieb
of an untreated pneumonic infection or it may be 2011). The parietal and visceral pleurae are in
the result of a medical intervention. The condition close contact and the potential space between them
is usually treated in a specialist environment such contains only a thin layer of fluid, approximately
as respiratory medicine or cardiothoracic surgery, 0.1-0.2mL/kg body weight (Rahman et al 2004,
however initial diagnosis may occur in other Bourke and Burns 2011), that lubricates the pleural
clinical areas because empyema tends to develop surfaces and prevents friction during respiration.
undetected in debilitated patients.
Empyema was first identified by the Egyptian
physician Imhotep around 3,000 BC, and Pathophysiology of empyema
Hippocrates also recognised it 2,500 years later Empyema develops in phases (Figure 1). Initially,
(Davies et al 2010). Before the 20th century, the fluid is a free flowing sterile exudate, referred
treatment involved open drainage of the pleural to commonly as a simple parapneumonic
cavity, which had a high mortality rate and effusion. During this exudative phase, fluid moves

42 march 26 :: vol 28 no 30 :: 2014 NURSING STANDARD / RCN PUBLISHING


Downloaded from RCNi.com by ${individualUser.displayName} on May 27, 2016. For personal use only. No other uses without permission.
Copyright 2016 RCNi Ltd. All rights reserved.
into the pleural space as a result of increased unwell, but attribute his or her symptoms to other
pulmonary vascular permeability and the effect causes and not seek additional help. Common
of proinflammatory cytokines on the mesothelial symptoms of empyema are shown in Box 1. Nurses
cells. Prompt treatment with antibiotics is usually are ideally placed to recognise symptoms, reassure
adequate and chest tube drainage is often not the patient and alert the relevant medical team.
required (Davies et al 2010). A pleural effusion may be apparent on a chest
If appropriate antibiotics are not commenced, X-ray, but the diagnosis of infection is often made
the effusion may progress to the fibrinopurulent following aspiration of the fluid and microscopy,
phase. Increased amounts of fluid accumulate culture and sensitivity examination. Ultrasound
in the pleural space and bacteria invade through scanning is an important diagnostic tool, because
the damaged endothelium (Davies et al 2010). it detects the exact location of any fluid collection
Bacterial invasion accelerates the immune and accurate aspiration can be performed if
response, promoting the migration of neutrophils required (Rosenstengel 2012). Rapid diagnosis and
and depression of fibrinolytic activity as a result intervention are paramount to reduce morbidity,
of the activation of the coagulation cascade (Idell mortality and treatment costs (Davies et al 2010).
et al 1991, Kroegel and Antony 1997). The fibrin Frequently, empyema is not detected until the
deposits form pus-filled pockets (septations). infection is advanced and the patient is unwell.
Neutrophil phagocytosis and bacterial death Estimated mortality is between 14% and 18%, but
stimulate the inflammatory process to release up to 57% of patients diagnosed at an advanced
more proteases and bacterial cell wall-derived stage will die as a direct result of the condition
fragments (Kroegel and Antony 1997). The (Ferguson et al 1996, Davies et al 2010). Because
combination of adhesions, loculations and thick of the high morbidity and the specialised nature of
pus make simple drainage ineffective (Lim 2001). this infection, it is recommended that a respiratory
The fibrinopurulent phase is also known as a physician or thoracic surgeon manage the patient
complicated parapneumonic effusion. (Davies et al 2010). Therefore, a patient may
In the organising phase, fibroblasts proliferate, require transfer to a specialist unit for long-term
creating a solid fibrous peel (Kroegel and Antony management. This can increase anxiety for the
1997). This surrounds the outside of the lung and patient and family and the rationale for the move
prevents re-expansion, impairs lung function should be explained.
and creates a persistent pleural space (Davies
et al 2010). The fibrous peel is difficult to remove FIGURE 1
and often requires surgical thoracotomy and
Phases of empyema development
decortication (Roberts 2003, Anyanwu et al 2004).
The pathogens responsible for pleural infection
vary according to whether it is hospital or Exudative phase simple parapneumonic effusion
community acquired, or iatrogenic (Davies et al
2010). Streptococcal species are responsible for
Fibrinopurulent phase complicated parapneumonic effusion
up to 65% of community-acquired infections
(Maskell et al 2006, Davies et al 2010), whereas
Staphylococcus aureus accounts for up to 50% of Organising phase formation of scar tissue from the fibrin
hospital-acquired cases, with meticillin-resistant deposits that surround the lung, preventing full expansion
S. aureus accounting for up to two thirds of these
cases (Maskell et al 2006, Davies et al 2010). (Davies et al 2010)
The causative organism of pleural infection also
varies between countries. Knowledge of the
microbiological profile and differing bacteriology BOX 1
is important to guide appropriate antibiotic Common symptoms of empyema
therapy (Davies et al 2010).
Fever (night sweats).
Lethargy.
Dyspnoea.
Diagnosis Anorexia.
Empyema often has an insidious clinical onset, Weight loss.
which makes accurate and timely diagnosis Breathlessness (if large effusion is present).
difficult (Davies et al 2010). For the patient, Chest pain.
it represents a chronic infective state, which Cough.
frequently occurs with a malignant disease process Purulent sputum.
(British Medical Journal 2013)
or other long-term condition. A patient may feel

NURSING STANDARD / RCN PUBLISHING march 26 :: vol 28 no 30 :: 2014 43


Downloaded from RCNi.com by ${individualUser.displayName} on May 27, 2016. For personal use only. No other uses without permission.
Copyright 2016 RCNi Ltd. All rights reserved.
Art & science respiratory nursing

Pleural infection leading to empyema can surgery is not imminent, for example in those
develop following illness or intervention. Up to who are not fit for surgery because of other
57% of patients with pneumonia may develop comorbidities (Davies et al 2010).
a pleural effusion, which usually resolves with Concurrent antibiotic therapy is initiated based
appropriate antimicrobial therapy (Davies on local antibiotic policy and resistance patterns.
et al 2010); however, if not treated promptly Amino-penicillins such as amoxicillin and
complications arise. Other risk factors include ampicillin, penicillins combined with
iatrogenic pleural infection following pleural, beta-lactamase inhibitors (co-amoxiclav,
thoracic or oesophageal surgery, diabetes mellitus, piperacillin with tazobactam) and cephalosporins
immunosuppression, gastro-oesophageal reflux, such as cephalexin and cephradine have good
alcohol misuse and intravenous drug use (Davies penetration of the pleural space compared to
et al 2010, British Medical Journal 2013). aminoglycosides (gentamicin, streptomycin,
neomycin) (Davies et al 2010). Duration of
antibiotic therapy is based on a combination of
Management clinical response, radiological improvement,
Management of pleural infection depends on bacteriology and inflammatory marker
severity. Treatment approaches range from improvements, for example C-reactive protein,
antibiotic therapy alone to radical surgical and is usually for at least three weeks (Davies et al
intervention (Rosenstengel 2012). Choice 2010, Rosenstengel 2012).
of antibiotic is guided by underlying Surgical intervention is considered on
microbiology, local prescribing guidelines an individual basis and is based on clinical
and drug resistance patterns (Rosenstengel improvement and residual sepsis in association
2012). Advice regarding management and with persistent pleural collection (Davies et al
antibiotic therapy is available from the British 2010). Video-assisted thoracoscopic surgery
Thoracic Society (Davies et al 2010). involving surgical debridement or decortication is
It is impossible to clinically differentiate between increasingly performed, often with good results,
the presence of a complicated parapneumonic although open thoracic drainage or thoracotomy
effusion requiring chest tube drainage and a simple and decortication are alternative techniques
effusion that may resolve with antibiotic therapy (Zahid et al 2011). Video-assisted surgery does
using a chest X-ray alone (Davies et al 2010). It not necessarily require a general anaesthetic,
is, therefore, recommended that all patients with decortication can be performed in patients who
a pleural effusion have diagnostic pleural fluid are awake using an epidural or para-vertebral
sampling, preferably under ultrasound guidance nerve block, and this is important in patients
(Davies et al 2010). Fluid is analysed for pH, with multiple comorbidities (Zahid et al 2011).
protein, glucose and lactate dehydrogenase to However, thoracic surgery can be high risk for
confirm whether it is a transudate or exudate, a patient debilitated by a chronic disease, and
which can aid with diagnosis, microbiology to guide therefore a full risk and benefit analysis, and
antibiotic prescribing, and cytology to detect the discussion with the patient and family are required
presence of malignant cells and acid fast bacilli if before any procedure. All inpatients need to be
mycobacterial infection is suspected (Davies et al assessed for risk of hospital-acquired complications
2010, Rosenstengel 2012). and treated according to local policy for issues such
Patients with a purulent or cloudy effusion, or as thrombosis prophylaxis and pressure area care.
with pleural fluid with a pH greater than 7.2 In addition, patients with empyema require
should receive prompt pleural space chest tube dietetic support and food supplements to ensure
drainage, to allow the infected fluid to be removed adequate nutrition.
(Davies et al 2010). This reduces sepsis as well as Length of inpatient stay following surgical
reducing the risk of formation of septations. This intervention will vary according to individual
is known as a loculated pleural effusion. Previous recovery rates. Some patients require prolonged
medical management of a loculated effusion has hospitalisation and rehabilitation following this
included the use of intrapleural fibrinolytic drugs procedure and resolution of infection. For others,
such as streptokinase or urokinase to break down when they have overcome the initial surgical episode,
the septations. However, a large double-blind they may be discharged with a long-term chest drain,
randomised controlled trial found this treatment oral antibiotic therapy and regular outpatient follow
was of little benefit (Maskell et al 2005). up. Decisions regarding management are taken in
Therefore, it is only recommended following conjunction with the patient, carers and medical
discussion with a thoracic surgeon for patients staff as well as relevant members of the wider
with symptoms such as dyspnoea and for whom multidisciplinary team (Box 2).

44 march 26 :: vol 28 no 30 :: 2014 NURSING STANDARD / RCN PUBLISHING


Downloaded from RCNi.com by ${individualUser.displayName} on May 27, 2016. For personal use only. No other uses without permission.
Copyright 2016 RCNi Ltd. All rights reserved.
Role of the clinical nurse specialist providing an opportunity for discussion regarding
The clinical nurse specialist has a significant role expectations, management and potential length of
in the management of patients with empyema both time for full resolution of the condition. The nurse
in the ward environment and following discharge can also begin assessment of whether management
because these individuals may receive continued at home would be feasible and the level of support
outpatient care for several months, depending available in the community.
on their progress. Over time, a good rapport Following medical or surgical intervention, there
can be established, which is vital to support the is an initial inpatient period where the patients chest
individual in coping with this chronic condition. drain is connected to a traditional underwater sealed
Since this type of infection is not common, the drainage bottle. When the patient has recovered
terminology may be unfamiliar to the patient and from the acute episode, a period of rehabilitation is
his or her family, and explanation may be required. required to allow him or her to regain confidence
Education with regard to management, treatment and independence. Resolution of the infection
options and long-term prognosis is also necessary. and lung re-expansion is closely observed through
The clinical nurse specialist is ideally placed to haematological and radiological monitoring.
offer physical and psychological support and assist Many patients require a chest drain for a long
long-term care and follow up for these individuals. period of time, often several months. To improve
In some cases, the clinical nurse specialist may mobility, these patients can be fitted with valved
meet the patient before surgery or fluid aspiration, ambulatory bags (Figure 4). These allow the chest
drain to remain in situ, but with a portable bag to
FIGURE 2 collect any drainage. They are also much lighter,
more discreet, and enable increased mobility and
Pre-operative chest X-ray showing left empyema
independence than the drainage bottles. Because
treatment is frequently lengthy, the ambulatory

BOX 2
Case study: an 82-year-old with long-term empyema
John (a pseudonym) was referred with a history of dyspnoea, pyrexia,
lethargy, weight loss and night sweats following a pneumonic infection,
and was diagnosed with left empyema (Figure 2). His condition did not
improve following initial antibiotic therapy and chest tube drainage, and
he was becoming progressively more unwell. He was assessed in the
critical care unit by the surgical team and although high risk because of
his age and infective state, it was determined that he may benefit from
surgery to clear the infected pleural space. The risks and benefits of the
surgery were explained to John and his family, and after considerable
discussion they agreed to proceed.
Following successful decortication and drainage, John faced a lengthy
recovery with a long-term drain. He was initially managed on the ward,
FIGURE 3 however his family was keen that he should return home and felt he
Post-operative chest X-ray showing left empyema would recover more quickly in familiar surroundings. After three weeks,
and chest drain in situ he was discharged with daily visits from the community nursing team,
community dietetic support and weekly outpatient follow up. Over the next
few months, the chest drain was gradually withdrawn (shortened) as his
lung expanded and the residual infection resolved. Weekly appointments
became fortnightly and then monthly.
The clinical nurse specialist supported John and his family by providing
education before discharge, liaison with community teams, practical
assistance with drain management and reassurance regarding the
progress of the condition. Johns family was aware that they could
contact one of the nurse specialists at any time should they have
questions between appointments.
After ten months, significant radiological improvement combined with
Johns vastly improved clinical condition indicated that the drain could
be removed. John was discharged with instructions to contact the team
if there were any signs of recurrence. Figure 3 shows one of the final
X-ray images before removal of the drain and the position of a safety pin
through the drain and against the skin to ensure the drain was secure.

NURSING STANDARD / RCN PUBLISHING march 26 :: vol 28 no 30 :: 2014 45


Downloaded from RCNi.com by ${individualUser.displayName} on May 27, 2016. For personal use only. No other uses without permission.
Copyright 2016 RCNi Ltd. All rights reserved.
Art & science respiratory nursing

bag also enables the patient to be discharged home St Thomas NHS Foundation Trust (unpublished
with a drain in place. data) found that patients fear others becoming aware
Nursing care of the ambulatory chest drain bag of the odour and this can lead them to restrict their
initially involves patient support and education. movements, and become isolated and depressed.
On a practical level, information is required Some patients associated the odour with poor
regarding positioning, emptying and changing hygiene and became preoccupied with trying to
the bag. This frequently requires multiple wash it away or disguise it. In these situations,
demonstrations in hospital before the patient the specialist nurse can reassure the patient and
and family feel confident to complete the task. provide practical and psychological support. The
Troubleshooting common problems such as patient should be encouraged to shower with a
spillages, disconnection of the bag or cessation of drain or stoma bag in situ, as long as the device is
drainage are also discussed in detail and advice is not submerged. Patients should carry out personal
given on what to do if the drain falls out. hygiene, and change the bag and dressing regularly
If chest tube drainage proves ineffective and to reduce the risk of unpleasant odours. Encouraging
long-term drainage is required for residual sepsis, patients to dress in familiar, comfortable clothes and
the patient may require surgical rib resection make regular trips out of the house can help them
(Davies et al 2010), creating an opening in the chest to establish a routine with which they become more
wall known as a pleural window or pleurostomy confident over time. Patients often become adept
(Anyanwu et al 2004). This removes the need for an at disguising the bag, either under clothes or in a
intercostal drain, and any fluid can be drained into particular handbag or shopping bag.
a stoma bag. For many individuals, this is a better Initially, both the patient and family can feel
option because the chest drain can be uncomfortable anxious about leaving the hospital environment
and the drainage device visible. Use of a stoma bag with a chest drain or stoma in place. This is
is considered by patients to be more discreet and overcome by changing to an ambulatory chest
causes fewer lifestyle restrictions. The clinical nurse drain bag before discharge and allowing the
specialist can assist the transition from one device to patient to familiarise him or herself with the
another by providing practical demonstrations and device. Increased mobility and independence are
answering questions regarding management. incentives to self-management of these devices.
Empyema has an offensive odour that is often Psychological and practical support is offered by
distressing to patients and their families. A local audit regular explanations, demonstrations of care and
carried out on the thoracic surgical unit at Guys and reassurance regarding self-management.

FIGURE 4 Long-term management of the chest drain


To meet the psychological and physical needs of
Ambulatory chest drain bag
patients with empyema, a specific outpatient clinic
run by clinical nurse specialists was established
within the thoracic outpatients service at Guys
and St Thomas NHS Foundation Trust. The clinic
is held twice per week alongside consultant-led
outpatient clinics. Hospital visits are combined
with telephone contact at home and regular
communication with the consultant surgeon. In
addition, visits by community nursing teams ensure
careful management of these patients. Audit results
(unpublished data) showed that over a two-year
period, 26% of the patients with empyema who
attended the clinic were managed with a long-term
drain or stoma bag.
The patients are cared for over a prolonged
period, allowing good rapport to develop with the
team. Observing or speaking to the individual on
(Reprinted with permission from Smiths Medical, ASD, Inc. a weekly basis gives nurses the opportunity to see
Refer to the Smiths Medical Portex Ambulatory Bag how patients become confident and empowered
Operators Manual Instructions for use this contains when managing their condition. This provides
specific information including contraindications, warnings, evidence of how nursing input, patience and
precautions and potential complications for the safe and
education can affect an individual during treatment
proper use of the product).
and recovery. The following recommendations

46 march 26 :: vol 28 no 30 :: 2014 NURSING STANDARD / RCN PUBLISHING


Downloaded from RCNi.com by ${individualUser.displayName} on May 27, 2016. For personal use only. No other uses without permission.
Copyright 2016 RCNi Ltd. All rights reserved.
should to be taken into account when considering The patient should be given a supply of drainage
a clinical nurse specialist-led outpatient clinic for equipment to allow for changes between
managing patients with empyema: outpatient visits. Family members often become
Explanations may need to be repeated with adept at changing bags and dressings.
regard to the function of and requirement for Community nursing teams require specific
the chest drain before the patient and family feel instructions for the management of the drain
confident enough to return home with the drain and contact telephone numbers for the ward,
in situ. Reassurance is required before the patient nurse specialist and medical team in the event
is confident to undertake normal activities such that problems arise at the patients home.
as sleeping and showering. The patient should contact his or her medical
Patients should be encouraged to mobilise, and team if signs of infection, increased dyspnoea or
the collection device should be kept below the surgical emphysema are observed, or if the drain
level of the chest drain entry site. This promotes falls out or becomes blocked.
fluid drainage and prevents back-flow into the The selection of clothing can be difficult for
pleural cavity. The patient should be warned not patients, especially for females. Loose tops can
to sit or lie on the tube or bag because this can help disguise the drain and the ambulatory bag,
obstruct drainage or cause the contents to leak. and supportive sports vests or camisoles can be
The chest drain entry site should be covered with worn instead of a brassiere. The patient should
a small non-adherent dressing and secured with be encouraged to experiment with outfits on the
hypo-allergenic tape. Large quantities of tape ward before discharge home to determine what
are not required if the suture holding the chest is comfortable and provides confidence.
drain in place (anchor suture) is secure. The The drain should not be removed without the
removal of large dressings can be uncomfortable knowledge of the medical or surgical consultant
for patients, especially hirsute men, and large who recommended insertion.
dressings can restrict chest expansion.
Dressings should be changed daily if possible,
observing for signs of infection, oozing and Conclusion
surgical emphysema, which is rare. The anchor Empyema is a distressing and uncomfortable
suture should also be assessed because it can condition, and patients may require long-term use
erode through the skin, causing the drain to alter of an intercostal chest drain, which can be managed
position or fall out. effectively in the community. With the help and
The collection device should be changed support of the clinical nurse specialist, medical
according to the amount and type of drainage. team and community nurses, many patients with
A large volume of fluid is heavy for the patient empyema are able to manage their ambulatory drain
to carry and can pull on the anchor suture. or stoma confidently NS

References
Anyanwu A, Jaiswal P, Treasure Ferguson AD, Prescott RJ, Selkon Current Opinion in Pulmonary Rahman N, Chapman S, Davies R
T (2004) Surgical treatment for JB, Watson D, Swinburn CR Medicine. 7, 4, 193-197. (2004) Pleural effusion: a
thoracic empyema. In Treasure T, (1996) The clinical course and structured approach to care. British
Hunt I, Keogh B, Pagano D (Eds) The management of thoracic empyema. Marieb E (2011) Essentials of Medical Bulletin. 72, 1, 31-47.
Evidence for Cardiothoracic Surgery. Quarterly Journal of Medicine. 89, Human Anatomy & Physiology.
TfM Publishing, Shrewsbury, 131-139. 285-289. Tenth edition. Pearson Education, Roberts JR (2003) Minimally
San Francisco CA. invasive surgery in the treatment
Bourke S, Burns G (2011) Lecture Idell S Girard W, Koenig KB, of empyema: intraoperative
Notes: Respiratory Medicine. Eighth McLarty J, Fair DS (1991) Maskell NA, Batt S, Hedley EL, decision making. Annals of
edition. Wiley-Blackwell, Chichester. Abnormalities of pathways of fibrin Davies CW, Gillespie SH, Thoracic Surgery. 76, 1, 225-230.
turnover in the human pleural space. Davies RJ (2006) The bacteriology
British Medical Journal (2013) American Review of Respiratory of pleural infection by genetic Rosenstengel A (2012) Pleural
Empyema. Best Practice Guidelines. Disease. 144, 1, 187-194. and standard methods and its infection: current diagnosis and
bestpractice.bmj.com/best- mortality significance. American management. Journal of Thoracic
practice/monograph/1008/ Kroegel C, Antony VB (1997) Journal of Respiratory and Disease. 4, 2, 186-193.
diagnosis/step-by-step.html (Last Immunobiology of pleural Critical Care Medicine. 174, 7,
accessed: March 4 2014.) inflammation: potential implications 817-823. Zahid I, Nagendran M, Routledge T,
for pathogenesis, diagnosis and Scarci M (2011) Comparison of
Davies HE, Davies RJ, Davies CW therapy. European Respiratory Maskell NA, Davies CW, Nunn AJ video-assisted thoracoscopic
(2010) Management of pleural Journal. 10, 10, 2411- 2418. et al (2005) U.K. controlled trial surgery and open surgery in the
infection in adults: British Thoracic of intrapleural streptokinase for management of primary empyema.
Society Pleural Disease Guideline Lim TK (2001) Management of pleural infection. New England Current Opinion in Pulmonary
2010. Thorax. 65, Suppl 2, ii41-ii53. parapneumonic pleural effusion. Journal of Medicine. 352, 865-874. Medicine. 17, 4, 255-299.

NURSING STANDARD / RCN PUBLISHING march 26 :: vol 28 no 30 :: 2014 47


Downloaded from RCNi.com by ${individualUser.displayName} on May 27, 2016. For personal use only. No other uses without permission.
Copyright 2016 RCNi Ltd. All rights reserved.

You might also like