Chylothorax

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Chylothorax
Chylothorax.jpg
Three bottles of chyle drained from a chylothorax
Specialty Respiratory medicine
Symptoms None, breathlessness
Complications Dehydration, malnutrition, abnormal electrolyte levels, weakened immune system
TypesLow output, high output
CausesComplication of surgery, trauma, cancer, infections, lymph vessel abnormalities
Diagnostic method X-ray, CT scan, thoracic MRI, fluid sampling
TreatmentRemoving fat from the diet, decreasing lymph flow, chest tube, surgery
Medication Octreotide, midodrine, and sirolimus
Prognosis ~10% risk of death

A chylothorax is an abnormal accumulation of chyle, a type of lipid-rich lymph, in the space surrounding the lung. The lymphatics of the digestive system normally returns lipids absorbed from the small bowel via the thoracic duct, which ascends behind the esophagus to drain into the left brachiocephalic vein. If normal thoracic duct drainage is disrupted, either due to obstruction or rupture, chyle can leak and accumulate within the negative-pressured pleural space. In people on a normal diet, this fluid collection can sometimes be identified by its turbid, milky white appearance, since chyle contains emulsified triglycerides.

Contents

Chylothorax is a rare but serious condition, as it signals leakage of the thoracic duct or one of its tributaries. There are many treatments, both surgical and conservative. [1] About 2–3% of all fluid collections surrounding the lungs (pleural effusions) are chylothoraces. [2] It is important to distinguish a chylothorax from a pseudochylothorax (a pleural effusion that happens to be high in cholesterol), which has a similar appearance visually but is caused by more chronic inflammatory processes and requires a different treatment. [3]

Signs and symptoms

The symptoms of a chylothorax depend its size and the underlying cause. A small chylothorax may not cause any symptoms and only be detected on a chest X-ray performed for another reason. A large chylothorax may lead to breathlessness or a feeling of pressure in the chest, caused by fluid restricting the expansion of the lungs, although large chylothoraces may remain asymptomatic if the chylothorax has accumulated slowly, as the lungs may have had time to become used to the pressure. Fever or chest pain are not usually associated with chylothorax, as chyle does not generate inflammation by itself. [4]

On examination, chylothorax may lead to reduced breath sounds on the affected side, associated with a dull sound when the chest is tapped or percussed. In cases of postoperative chylothorax, the first sign may be persistent drainage from intercostal drains. [1] Large chylothoraces may cause signs related to the loss of nutrients, including features of malnutrition or decreased ability to fight infections. [5] Rapidly accumulating chylothoraces can cause a sudden drop in blood volume, leading to low blood pressure. [5]

Causes

There are three main types of chylothorax: traumatic, non-traumatic, and idiopathic. Historically the most common form of chylothorax was non-traumatic, but traumatic chylothoraces now represent the majority of cases, with most arising as postoperative complications of surgery. [6] [7] The most common cause of non-traumatic chylothoraces is cancer. [1] Chylothoraces can also be classified as low- or high-output based on the rate of chyle accumulation: low-output chylothoraces accumulate <500 mL of chyle per 24 hours, while high-output chylothoraces accumulate >1000 mL per 24 hours. [8]

Non-traumatic

Malignancies are the most frequent cause of non-traumatic chylothorax. Cancers like chronic lymphocytic leukemia, lung cancer, lymphoma, Kaposi sarcoma, metastatic carcinoma or esophageal cancer are potential causes of chylothorax. Infectious causes are also observed, most often in developing countries. The most common cause of an infectious chylothorax is a complication of tuberculous lymphadenitis. Other possible causative infections include aortitis, histoplasmosis, and filariasis. Chylothorax can also be congenital, and may co-occur with other lymphatic malformations like lymphangiectasis and lymphangiomatosis. Other conditions like tuberous sclerosis, congenital heart disease, trisomy 21 (Down syndrome), Noonan syndrome, or Turner syndrome (missing X chromosome) are also possible causes of congenital chylothorax. Other, more rare causes of congenital chylothorax include Castleman's disease, yellow nail syndrome, Waldenström's macroglobulinemia, sarcoidosis, venous thrombosis, thoracic radiation, macroglobulinemia, amyloidosis, and a goiter. These diseases cause chylothorax by obstructing or destroying the thoracic duct. Also, parenteral nutrition has been a possible cause; a quick dose of total parenteral nutrition can overwhelm the thoracic duct, causing the chyle to leak into the surrounding pleural space. [1]

Traumatic

Iatrogenic chylothorax after surgery is the most common variety of chylothorax. [1] It is a common and serious complication of a pneumonectomy. [9] It is especially common in surgeries requiring mediastinal dissection. [5] The probability of chylothorax depends on the type of surgery. The surgery with the highest risk of chylothorax is an esophagostomy, with a 5-10% risk of chylothorax. Lung resection and mediastinal node dissection have the second highest risk, with 3-7% risk. Other operations like mediastinal tumor resection, thoracic aneurysm repair, sympathectomy, and any other surgeries that take place in the lower neck or the mediastinum can lead to chylothorax. Chylotharax after trauma but not after surgery has also been described after central line placement, pacemaker implantation, and embolization of a pulmonary arteriovenous malformation. Blunt trauma to the chest region is another cause of chylothorax, which has occurred after blast injuries and even simple injuries from coughing or sneezing. [1]

Mechanism

The main mechanism of chylothorax is the leaking of chyle from the thoracic duct, usually caused by a disturbance affecting the structural integrity of the thoracic duct. [5] For example, placement of a central venous catheter can potentially disrupt drainage of lymph into the subclavian veins, followed by the thoracic duct, resulting in chylothorax. [5] The disturbances cause the pressure in the thoracic duct to increase. Soon, collateral channels form, which eventually drain into the thorax. [10] Trauma affecting the thoracic duct is the most common disturbing mechanism.

Whether a chylothorax occurs in the left or right pleural space is a consequence of the thoracic duct's anatomic location in the body and depends on the level where the duct was injured. If the thoracic duct is injured above the fifth thoracic vertebra, then a left-sided chylothorax results. [5] Conversely, a thoracic duct injury below that level will lead to the formation of a right-sided chylothorax. [5] Chylothoraces most commonly occur in the right pleural space (50% of cases). [5] Left-sided and bilateral chylothoraces are less common and occur in 33% and 17% of cases, respectively. [5]

In the case of cancer, invasion into the thoracic duct or collateral lymph channels can obstruct lymph. In the case of mediastinal lymphadenopathy, the enlarged lymph node causes compression of the lymphatic channels and thoracic duct. This impedes the centripetal drainage of the flow of lymph from the edges of the lung parenchyma and pleural surfaces. This causes the chyle to ooze extensively into the pleural cavity, leading to a chylothorax. In the case of yellow nail syndrome, or lymphedema, chylothorax is caused by hypoplasia or dilation of the lymph vessels. In rare cases, like in hepatic chylothorax, chylous ascites crosses the diaphragm into the pleural cavity. In idiopathic cases like genetic disorders, the mechanism is not known. [5] Up to three liters of chyle can easily drain into the pleural space daily. [10]

Diagnosis

Bilateral chylothorax seen on a thoracic MRI Bilateral chylothorax seen on a thoracic MRI.png
Bilateral chylothorax seen on a thoracic MRI
CT scan showing extensive chylothorax caused by leakage from the thoracic duct Extensive chylothorax caused by leakage from the thoracic duct.png
CT scan showing extensive chylothorax caused by leakage from the thoracic duct

Chest X-rays can detect a chylothorax. It appears as a dense, homogeneous area that obscures the costophrenic and cardiophrenic angles. Ultrasounds can also detect a chylothorax, which appears as an echoic region that is isodense with no septation or loculation. However, neither a normal chest x-ray nor an ultrasound can differentiate a chylothorax from any other type of pleural effusion. [1]

Chest X-ray showing bilateral chylothorax Chest X-ray showing bilateral chylothorax.png
Chest X-ray showing bilateral chylothorax

The cisterna chyli can be found in a thoracic MRI, making it possible to confirm chylothorax. However, MRI is not the ideal method to scan the thorax, and so it is rarely used. Another diagnostic technique is conventional lymphangiography. It is rarely used since there are equally sensitive yet less invasive techniques available to identify a chylothorax. Lymphangiography procedures use the contrast dye agent lipiodol, which is injected into the lymphatic vessels. The chylothorax shows up on the images and identifies the source any leak in the thoracic duct. [1]

Another, more commonly used type of lymphogram is nuclear lymphoscintigraphy; this procedure requires human pentetic acid labeled Tc99m to be injected into the subcutaneous lesions of both sides of the dorsum of the foot. Then two images, anterior and posterior, are obtained using gamma-ray cameras. This test can be used with an integrated low-dose CT-scan with photon emission to get images that are more precise. Once pleural effusion is detected, a thoracentesis is recommended. [1]

The fluid of a chylothorax may appear milky, serous or serosanguineous. If the appearance of the fluid is not milky, that does not exclude a chylothorax from consideration. Since chyle is rich in triglycerides, a pleural effusion that is rich in triglycerides (>110 mg/dL) confirms the presence of a chylothorax; a pleural effusion that is low in triglyceride content (<50 mg/dL) virtually excludes the diagnosis. [11] [12] If a pleural effusion contains triglycerides between 50 and 110 mg/dL, analysis of the lipoprotein content of the pleural effusion to evaluate for chylomicrons is recommended. [11] If that procedure detects chylomicrons in the fluid, that confirms a chylothorax. Chylothoraces are typically exudative and often contain a high number of lymphocytes and have low levels of the enzyme lactate dehydrogenase (LDH). [11] However, atypical chylothoraces can occur and are transudative in 14% of cases. [11] A milky appearance of pleural fluid is insufficient to confirm the diagnosis of chylothorax as pseudochylothoraces and empyemas can mimic this appearance. [11] Conversely, the absence of a milky appearance does not mean a chylothorax is not present as they may instead appear serous or bloody. [11]

Treatment

The treatment for chylothorax depends on the underlying cause but may include dietary modification, medication to prevent chyle formation including somatostatin/octreotide, midodrine and sirolimus, pleurodesis, and surgical treatment including ligation of the thoracic duct, pleurovenous or pleuroperitoneal shunting or thoracic duct embolization. [1]

Initial

The initial treatment of a chylothorax is usually drainage of the fluid from the pleural space. This may be necessary to restore lung function compromised by the pressure exerted by the chyle on the lungs. [1] Those with large chylothoraces may need nutritional support due to the nutrients lost, primarily to correct protein and electrolyte losses. Once the affected person is hemodynamically and nutritionally stable, then specific treatment can begin. [5]

Conservative

A conservative treatment is changing diet to include fewer long-chain fatty acids, in particular free fatty acids. Since chyle is formed from these acids, chyle formation will reduce, allowing the defects to heal spontaneously. However, this can lead to fat deficiency and malnutrition over time. A possible response to this drawback is a venous fat hemorrhage, in which small and medium-chain fatty acids are given by diet, and long-chain fatty acids are given intravenously. Thoracentesis and an indwelling catheter for use at home is generally used to drain the chylothorax. [1] If a malignant neoplastic chylothorax is present, then treatment with radiotherapy and/or chemotherapy is warranted.

Surgical

Surgery is indicated if the case is post-traumatic, iatrogenic, or refractory to other treatments, in which cases surgery reduces mortality by 40%. One invasive surgical intervention called a thoracic duct ligation involves closing off the thoracic ducts. [1] Surgical pleurodesis is another option and can be undertaken if the affected person fails to respond to conservative treatment and is not a candidate for surgical intervention. [13]

Another treatment option is pleuroperitoneal shunting (creating a communication channel between the pleural space and peritoneal cavity). Since surgery to close the leak is not reliable, talc pleurodesis is recommended; in a case study of 19 people with refractory malignant chylothorax due to lymphoma, it resulted in success for all affected individuals. [5] Chemical pleurodesis is an option, since the leaking of lymphatic fluids is stopped by irritating the lungs and chest wall, resulting in a sterile inflammation. This causes the lung and the chest wall to fuse together, thus preventing lymphatic fluids from leaking into the pleural space. [14]

Prognosis

The morbidity and mortality rates associated with chylothorax have declined as treatments have improved. Malignant, bilateral, and chronic chylothoraces have an inferior prognosis to other types. [5] Currently, the mortality and morbidity rates are about 10% if treated surgically. [1] If cases are post-operative and treated conservatively, mortality rates approach 50%. [5]

Complications

Complications of chylothorax include malnutrition, immunosuppression, dehydration, and respiratory distress. [6] The severity of the complications depends on how quickly the chylothorax accumulated, its size, and its chronicity. [13]

Epidemiology

Chylothoraces are rare and usually occur as a complication of surgeries in the neck and mediastinum. It has no gender or age predisposition. A chylothorax occurs in 0.2-1% of cardiothoracic surgeries, 5-10% of esophagostomies, and 3-7% of lung resections. [1]

Other animals

Horses

Chylothorax is uncommon in horses. Clinical signs and symptoms in foals include difficulty breathing, fast breathing, cough, fever, and lethargy. The fluid generally appears opalescent and milky without any odor. A line of fluid is observed on percussion and there are reduced lung sounds. To differentiate between chyle is pseudochyle, which does not clear after centrifugation. There is not much information on the treatment of chylothorax in horses. Supportive care, antimicrobials, drainage of the thorax, and dietary management have been used with success. Surgery has been done in other animals with limited success, but has not yet been reported in horses. Although success has been reported, the prognosis is relatively unknown due to the lack of data. [15]

Related Research Articles

<span class="mw-page-title-main">Pleural cavity</span> Thin fluid-filled space between the two pulmonary pleurae (visceral and parietal) of each lung

The pleural cavity, pleural space, or interpleural space is the potential space between the pleurae of the pleural sac that surrounds each lung. A small amount of serous pleural fluid is maintained in the pleural cavity to enable lubrication between the membranes, and also to create a pressure gradient.

<span class="mw-page-title-main">Pleural effusion</span> Accumulation of excess fluid in the pleural cavity

A pleural effusion is accumulation of excessive fluid in the pleural space, the potential space that surrounds each lung. Under normal conditions, pleural fluid is secreted by the parietal pleural capillaries at a rate of 0.6 millilitre per kilogram weight per hour, and is cleared by lymphatic absorption leaving behind only 5–15 millilitres of fluid, which helps to maintain a functional vacuum between the parietal and visceral pleurae. Excess fluid within the pleural space can impair inspiration by upsetting the functional vacuum and hydrostatically increasing the resistance against lung expansion, resulting in a fully or partially collapsed lung.

<span class="mw-page-title-main">Chyle</span> Milky bodily fluid consisting of lymph and emulsified fats

Chyle is a milky bodily fluid consisting of lymph and emulsified fats, or free fatty acids (FFAs). It is formed in the small intestine during digestion of fatty foods, and taken up by lymph vessels specifically known as lacteals. The lipids in the chyle are colloidally suspended in chylomicrons.

<span class="mw-page-title-main">Pleurodesis</span> Medical procedure on pleural cavity

Pleurodesis is a medical procedure in which part of the pleural space is artificially obliterated. It involves the adhesion of the visceral and the costal pleura. The mediastinal pleura is spared.

<span class="mw-page-title-main">Chest tube</span> Type of surgical drain

A chest tube is a surgical drain that is inserted through the chest wall and into the pleural space or the mediastinum in order to remove clinically undesired substances such as air (pneumothorax), excess fluid, blood (hemothorax), chyle (chylothorax) or pus (empyema) from the intrathoracic space. An intrapleural chest tube is also known as a Bülau drain or an intercostal catheter (ICC), and can either be a thin, flexible silicone tube, or a larger, semi-rigid, fenestrated plastic tube, which often involves a flutter valve or underwater seal.

<span class="mw-page-title-main">Thoracotomy</span> Surgical procedure

A thoracotomy is a surgical procedure to gain access into the pleural space of the chest. It is performed by surgeons to gain access to the thoracic organs, most commonly the heart, the lungs, or the esophagus, or for access to the thoracic aorta or the anterior spine. A thoracotomy is the first step in thoracic surgeries including lobectomy or pneumonectomy for lung cancer or to gain thoracic access in major trauma.

<span class="mw-page-title-main">Hemothorax</span> Blood accumulation in the pleural cavity

A hemothorax is an accumulation of blood within the pleural cavity. The symptoms of a hemothorax may include chest pain and difficulty breathing, while the clinical signs may include reduced breath sounds on the affected side and a rapid heart rate. Hemothoraces are usually caused by an injury, but they may occur spontaneously due to cancer invading the pleural cavity, as a result of a blood clotting disorder, as an unusual manifestation of endometriosis, in response to Pneumothorax, or rarely in association with other conditions.

<span class="mw-page-title-main">Hydrothorax</span> Medical condition

Hydrothorax is a type of pleural effusion in which transudate accumulates in the pleural cavity. This condition is most likely to develop secondary to congestive heart failure, following an increase in hydrostatic pressure within the lungs. More rarely, hydrothorax can develop in 10% of patients with ascites which is called hepatic hydrothorax. It is often difficult to manage in end-stage liver failure and often fails to respond to therapy.

<span class="mw-page-title-main">Thoracentesis</span> Removal of fluids/air from the pleural cavity of the lungs

Thoracentesis, also known as thoracocentesis, pleural tap, needle thoracostomy, or needle decompression, is an invasive medical procedure to remove fluid or air from the pleural space for diagnostic or therapeutic purposes. A cannula, or hollow needle, is carefully introduced into the thorax, generally after administration of local anesthesia. The procedure was first performed by Morrill Wyman in 1850 and then described by Henry Ingersoll Bowditch in 1852.

<span class="mw-page-title-main">Pancreatic fistula</span> Medical condition

A pancreatic fistula is an abnormal communication between the pancreas and other organs due to leakage of pancreatic secretions from damaged pancreatic ducts. An external pancreatic fistula is one that communicates with the skin, and is also known as a pancreaticocutaneous fistula, whereas an internal pancreatic fistula communicates with other internal organs or spaces. Pancreatic fistulas can be caused by pancreatic disease, trauma, or surgery.

<span class="mw-page-title-main">Yellow nail syndrome</span> Medical condition

Yellow nail syndrome, also known as "primary lymphedema associated with yellow nails and pleural effusion", is a very rare medical syndrome that includes pleural effusions, lymphedema and yellow dystrophic nails. Approximately 40% will also have bronchiectasis. It is also associated with chronic sinusitis and persistent coughing. It usually affects adults.

<span class="mw-page-title-main">Gorham's disease</span> Syndrome characterized by bone loss

Gorham's disease, also known as Gorham vanishing bone disease and phantom bone disease, is a very rare skeletal condition of unknown cause, characterized by the uncontrolled proliferation of distended, thin-walled vascular or lymphatic channels within bone, which leads to resorption and replacement of bone with angiomas and/or fibrosis.

<span class="mw-page-title-main">Catamenial pneumothorax</span> Medical condition

Catamenial pneumothorax is a spontaneous pneumothorax that recurs during menstruation, within 72 hours before or after the onset of a cycle. It usually involves the right side of the chest and right lung, and is associated with thoracic endometriosis. A third to a half of patients have pelvic endometriosis as well. Despite this association, CP is still considered to be misunderstood as is endometriosis considered to be underdiagnosed. The lack of a clear cause means that diagnosis and treatment is difficult. The disease is believed to be largely undiagnosed or misdiagnosed, leaving the true frequency unknown in the general population.

<span class="mw-page-title-main">Lymphangiomatosis</span> Medical condition

Lymphangiomatosis is a condition where a lymphangioma is not present in a single localised mass, but in a widespread or multifocal manner. It is a rare type of tumor which results from an abnormal development of the lymphatic system.

<span class="mw-page-title-main">Fibrothorax</span> Medical condition involving fibrosis of the pleural space

Fibrothorax is a medical condition characterised by severe scarring (fibrosis) and fusion of the layers of the pleural space surrounding the lungs resulting in decreased movement of the lung and ribcage. The main symptom of fibrothorax is shortness of breath. There also may be recurrent fluid collections surrounding the lungs. Fibrothorax may occur as a complication of many diseases, including infection of the pleural space known as an empyema or bleeding into the pleural space known as a haemothorax.

<span class="mw-page-title-main">Tracheal deviation</span>

Tracheal deviation is a clinical sign that results from unequal intrathoracic pressure within the chest cavity. It is most commonly associated with traumatic pneumothorax, but can be caused by a number of both acute and chronic health issues, such as pneumonectomy, atelectasis, pleural effusion, fibrothorax, or some cancers and certain lymphomas associated with the mediastinal lymph nodes.

<span class="mw-page-title-main">Urinothorax</span> Presence of urine in the fluid-filled cavity that surrounds the lungs

Urinothorax is defined as urine in the fluid-filled cavity that surrounds the lungs. It is usually caused by obstructive uropathy. It is mainly diagnosed by analyzing the pleural fluid. Treatment involves treating the underlying condition, which typically results in resolution of the urinothorax. It is an extremely rare cause of pleural effusion.

<span class="mw-page-title-main">Pulmonary pleurae</span> Serous membrane that lines the wall of the thoracic cavity and the surface of the lung

The pulmonary pleurae are the two opposing layers of serous membrane overlying the lungs and the inside of the surrounding chest walls.

Thoracic endometriosis is a rare form of endometriosis where endometrial-like tissue is found in the lung parenchyma and/or the pleura. It can be classified as either pulmonary, or pleural, respectively. Endometriosis is characterized by the presence of tissue similar to the lining of the uterus forming abnormal growths elsewhere in the body. Usually these growths are found in the pelvis, between the rectum and the uterus, the ligaments of the pelvis, the bladder, the ovaries, and the sigmoid colon. The cause is not known. The most common symptom of thoracic endometriosis is chest pain occurring right before or during menstruation. Diagnosis is based on clinical history and examination, augmented with X-ray, CT scan, and magnetic resonance imaging of the chest. Treatment options include surgery and hormones.

<span class="mw-page-title-main">Lung surgery</span>

Lung surgery is a type of thoracic surgery involving the repair or removal of lung tissue, and can be used to treat a variety of conditions ranging from lung cancer to pulmonary hypertension. Common operations include anatomic and nonanatomic resections, pleurodesis and lung transplants. Though records of lung surgery date back to the Classical Age, new techniques such as VATS continue to be developed.

References

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  2. ↑ "Chylothorax and Cholesterol Effusion". Pulmonology Advisor. 2019-01-23. Retrieved 2019-03-24.
  3. ↑ Heffner J. "Clinical presentation, diagnosis and management of cholesterol effusions". 8.0. UpToDate. Retrieved 30 October 2014.
  4. ↑ Schild, Hans H; Strassburg, Christian P; Welz, Armin; Kalff, Jörg (2013–2014). "Treatment Options in Patients With Chylothorax". Deutsches Ärzteblatt International. 110 (48): 819–826. doi:10.3238/arztebl.2013.0819. ISSN   1866-0452. PMC   3865492 . PMID   24333368.
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  7. ↑ Pillay, TG; Singh, B (March 2016). "A review of traumatic chylothorax". Injury. 47 (3): 545–50. doi:10.1016/j.injury.2015.12.015. PMID   26776461.
  8. ↑ Lyon, S; Mott, N; Koukounaras, J; Shoobridge, J; Hudson, PV (June 2013). "Role of interventional radiology in the management of chylothorax: a review of the current management of high output chylothorax". CardioVascular and Interventional Radiology. 36 (3): 599–607. doi:10.1007/s00270-013-0605-3. PMID   23580112. S2CID   22158968.
  9. ↑ Vallières, E.; Karmy-Jones, R.; Wood, D. E. (1999). "Early complications. Chylothorax". Chest Surgery Clinics of North America. 9 (3): 609–616, ix. ISSN   1052-3359. PMID   10459431.
  10. 1 2 Talwar, Arunbh, and Hans J Lee. “A Contemporary Review of Chylothorax.” A Contemporary Review of Chylothorax, 2007, medind.nic.in/iae/t08/i4/iaet08i4p343.pdf Archived 2016-09-10 at the Wayback Machine .
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  12. ↑ Nadolski, G (December 2016). "Nontraumatic Chylothorax: Diagnostic Algorithm and Treatment Options". Techniques in Vascular and Interventional Radiology. 19 (4): 286–90. doi:10.1053/j.tvir.2016.10.008. PMID   27993324.
  13. 1 2 Kumar, Abhishek; Harris, Kassem; Roche, Charles; Dhillon, Samjot Singh (2014-11-01). "A 69-Year-Old Woman with Lymphoma and Chylothorax. Looking Beyond the Usual Suspect". Annals of the American Thoracic Society. 11 (9): 1490–1493. doi:10.1513/AnnalsATS.201406-251CC. ISSN   2329-6933. PMID   25423001.
  14. ↑ Sonoda, A; Jeudy, J; White, CS; Kligerman, SJ; Nitta, N; Lempel, J; Frazier, AA (May 2015). "Pleurodesis: indications and radiologic appearance". Japanese Journal of Radiology. 33 (5): 241–5. doi:10.1007/s11604-015-0412-7. PMID   25791777. S2CID   22780289.
  15. ↑ Weese, Scott; Munroe, Graham; Munroe, Graham (2011-03-15). Equine Clinical Medicine, Surgery and Reproduction. CRC Press. p. 476. ISBN   978-1-84076-608-0.
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