David J Fox, Rajdeep S Khattar
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1 1224 Valve disease CARCINOID HEART DISEASE: PRESENTATION, DIAGNOSIS, AND MANAGEMENT David J Fox, Rajdeep S Khattar AETIOLOGY See end of artile for authors affiliations Correspondene to: Dr Rajdeep S Khattar, Manhester Heart Centre, Manhester Royal Infirmary, Oxford Road, Manhester M13 9WL, UK; rskhattar@ hotmail.om T Heart 2004; 90: doi: /hrt riuspid and pulmonary valve regurgitation usually ours as a seondary phenomenon aused by dilatation of the valve ring seondary to right ventriular failure or pulmonary hypertension, respetively. Primary diseases of the triuspid or pulmonary valves are unommon, but the more likely auses might inlude ongenital abnormalities, rheumati heart disease, or infetive endoarditis. Carinoid heart disease is a rare, but interesting and important ause of intrinsi triuspid and pulmonary valve disease leading to signifiant morbidity and mortality aused by right heart failure. When treated medially, and in appropriate ases surgially, signifiant benefits in overall quality of life and long term survival an be ahieved. We review the urrent literature regarding the pathophysiologial basis of the disease, the ardiovasular ompliations, and the urrently available treatment strategies. AND PATHOPHYSIOLOGY Carinoid tumours are rare neuroendorine malignanies arising from neural rest amine preursor uptake dearboxylation ells. Approximately 90% of all arinoid tumours are loated in the gastrointestinal system of whih the most ommon sites are the appendix and terminal ileum. Other less ommon sites inlude the bronhus and gonads. The most malignant of the arinoid tumours tend to arise from the ileum and must be invasive or metastasise to produe the arinoid syndrome whih is haraterised by faial flushing, intratable seretory diarrhoea, and bronhoonstrition. The inidene of arinoid tumours is approximately 1 in of the population 1 of whom about 50% develop arinoid syndrome. One the arinoid syndrome has developed, approximately 50% of these patients develop arinoid heart disease whih typially auses abnormalities of the right side of the heart. Usually, only arinoid tumours that invade the liver result in pathologial hanges to the heart. The ardia manifestations are aused by the paraneoplasti effets of vasoative substanes suh as 5-hydroxytryptamine (5-HT or serotonin), histamine, tahykinins, and prostaglandins released by the malignant ells rather than any diret metastati involvement of the heart. Ordinarily, the vasoative tumour produts are inativated by the liver, lungs, and brain, but the presene of hepati metastases may allow large quantities of these substanes to reah the right side of the heart without being inativated by the liver. The harateristi pathologial findings are endoardial plaques of fibrous tissue that may involve the triuspid valve, pulmonary valve, ardia hambers, venae avae, pulmonary artery, and oronary sinus. The fibrous reation may involve not only the valve leaflets, but also the subvalvar apparatus inluding the tendinous hords and papillary musles of the triuspid valve, and more rarely the mitral valve in ases with left sided involvement. The fibrous tissue in the plaques results in distortion of the valves leading to either stenosis, regurgitation, or both. The preferential right heart involvement is most likely related to inativation of the vasoative substanes by the lungs. In the 5 10% of ases with left sided valvar pathology, one should suspet either extensive liver metastases, bronhial arinoid, or a patent foramen ovale. 2 3 Although the preise ause for the plaque formation is not entirely lear, the diret ations of serotonin and bradykinin have been impliated by animal studies. 4 This finding is orroborated by the observation that the appetite suppressant drug fenfluramine, whih releases serotonin, has been noted to ause valvar distortion similar to that seen in arinoid heart disease. 5 NATURAL HISTORY Many arinoid tumours are slow growing and follow a prolonged ourse of up to 20 or more years from the development of the arinoid symptoms. However, the development of ardia pathology in the arinoid patient heralds a deline in linial outome. Three year mortality data for patients with arinoid heart disease shows a 31% survival rate, whereas arinoid patients without ardia involvement have approximately twie the survival rate. One study showed mean survival in those with arinoid heart disease to be redued to 1.6 years ompared to 4.6 years in those without ardia involvement. 6 Nevertheless, there is good evidene to suggest that
2 EDUCATION IN HEART treatment of the ardia aspets of arinoid not only improves symptoms but inreases longevity. 7 TRYPTOPHAN CLINICAL PRESENTATION There needs to be a high index of linial suspiion to diagnose arinoid heart disease. Carinoid symptoms typially our between the fifth and seventh deades of life with a mean age of years The time period between onset of symptoms and diagnosis of arinoid heart disease usually approximates to months but may be as long as five years The mean time lag to surgery, depending on ardia symptoms and valvar disease severity, is approximately 24 months. 9 Obvious features of flushing, diarrhoea, and bronhospasm should draw attention to the possibility of the arinoid syndrome and, as disussed previously, patients with florid arinoid symptoms have a 50% hane of ardia involvement. In suh patients, physial examination usually reveals a systoli murmur along the left sternal edge, produed by triuspid regurgitation; onomitant murmurs of pulmonary stenosis or regurgitation may also be present. Pellagra with dermatitis of sun-exposed areas may also be seen seondary to the high turnover of niotini aid metabolised by the tumour. The vast majority of patients with ardia involvement present with signs of right heart failure seondary to severe dysfuntion of the triuspid and pulmonary valves. In a large US ase series, 97% of the 74 patients with ardia involvement had triuspid valve disease, of whom 90% displayed moderate or severe triuspid regurgitation; smaller numbers had oexistent triuspid stenosis. Pulmonary valve pathology was noted in 88% of patients, of whom 81% had pulmonary regurgitation and 53% had pulmonary stenosis. 6 In the same series, only 7% had left sided involvement, in whom the most typial feature was mild to moderate mitral regurgitation; left ventriular systoli funtion was not usually affeted. Two unusual ases reported arinoid heart disease presenting as pure right heart failure in the absene of the typial features of arinoid syndrome. 12 A further unique ase presented with the arinoid syndrome and right heart failure seondary to onstritive periarditis rather than triuspid or pulmonary valve dysfuntion. 13 Cardia metastases of arinoid tumours are extremely rare. In the largest series of 11 patients derived from the Mayo lini, arinoid syndrome was present in all patients and all metastases were intramyoardial in loation. 14 It is noteworthy that patients with arinoid heart disease may have labile blood pressure with either pronouned hypotension or hypertension, depending on the relative quantities of the individual vasoative substanes in the irulation. Serotonin, for example, an lead to tahyardia and hypertensive risis refratory to onventional treatment. DIAGNOSIS Basi sreening with a 12 lead ECG and hest x ray is of limited value. Between 30 50% of ECGs are normal; nonspeifi ST segment hanges and sinus tahyardia are the most ommon abnormal findings and p pulmonale or right bundle branh blok may also be seen on oasion. 6 8 The hest x ray is also largely unhelpful as around 50% are normal and the remainder have non-speifi hanges suh as inreased ardiothorai ratio, blunting of the ostophreni angles, or small pulmonary nodules Hydroxylase 5-HYDROXYTRYPTOPHAN Dearboxylase 5-HYDROXYTRYPTAMINE Monoamine oxidase 5-HYDROXYINDOLE ACETALDEHYDE 5-HYDROXYINDOLE ACETIC ACID Aldehyde dehydrogenase Figure 1 Biohemial pathway for the synthesis and degradation of serotonin (5-hydroxytryptamine). The two key investigations for the diagnosis of arinoid heart disease are 24 hour urinary exretion of 5-hydroxyindole aeti aid (5-HIAA) and transthorai ehoardiography. Biohemial sreening Metastati arinoid tumours take up the amino aid tryptophan and onvert it to serotonin (fig 1). The latter is the biologially ative moleule of the metaboli pathway and appears to play a role in the pathogenesis of some arinoid symptoms inluding diarrhoea and bronhoonstrition. Serotonin is ultimately broken down into 5-HIAA whih aounts for more than 95% of the urinary exretion. Patients with arinoid syndrome therefore have raised onentrations of 24 hour urinary 5-HIAA. In a large series of patients with arinoid syndrome and ardia involvement the mean 24 hour urinary exretion of 5-HIAA was up to 10-fold higher than the referene value (referene value, 50 mmol/l per 24 hours). Some studies suggest that a positive orrelation exists between urinary onentrations of 5-HIAA, disease progression, and worsening prognosis. 8 9 This has been attributed to the fat that higher irulating onentrations of vasoative substanes produed by the tumour (espeially 5-HT ausing fibroblast proliferation) are likely to indue more ardia damage. 8 9 In patients with both right and left sided arinoid heart disease, urinary values of 5-HIAA appear to be higher in patients without interatrial shunts ompared to those with interatrial shunts, suggesting greater disease ativity in the former group. 10 It should be noted that diets rih in bananas, nuts, pineapple, kiwi, and avoado an ause modest rises in
3 1226 urinary exretion of 5-HIAA and thereby lead to false positive results. Conversely the anti-parkinson s disease drug levodopa an falsely lower urinary 5-HIAA onentrations. Notably, arinoid tumours may also be assoiated with raised plasma onentrations of gastrin, gluagon, insulin, adrenoortiotropi hormone (ACTH), parathyroid hormone, and alitonin. Transthorai ehoardiography The main preditor of linial outome in patients with arinoid syndrome is the extent and severity of ardia involvement. Therefore ehoardiography plays a entral role in the diagnosti and prognosti evaluation of this ondition. In patients with arinoid heart disease, right atrial and right ventriular enlargement is present in up to 90% of ases and ventriular septal wall motion abnormalities are seen in almost half of the ases. 6 The triuspid valve leaflets and subvalvar strutures are often thikened, shortened and retrated, leading to inomplete oaptation and usually moderate or severe triuspid regurgitation (fig 2). The ontinuous wave Doppler profile of triuspid regurgitation shows a harateristi dagger shaped spetrum with an early peak pressure and rapid deline (fig 3). The pulmonary valve may also be thikened and retrated, leading to pulmonary regurgitation and less ommonly, pulmonary stenosis. The ombination of severe triuspid regurgitation and pulmonary stenosis is partiularly problemati as this further exaerbates the triuspid regurgitation and worsens right heart failure. Interestingly, alifiation of affeted valves is rare and may be onsidered a notable negative ehoardiographi feature of arinoid heart disease. TREATMENT In the early non-metastati phase, surgial resetion of the arinoid tumour tends to be urative. In those with the arinoid syndrome, treatment tends to be palliative as metastati spread has already ourred. Relief of symptoms an be ahieved surgially by debulking the tumour, and sometimes, in those with hepati metastases, by hepati artery ligation or embolisation. Patients with ardia involvement tend to have higher irulating onentrations of 5-HIAA and more advaned disease. The priniples of management of patients with arinoid heart disease an be divided into the treatment of right heart failure, pharmaotherapy to redue the seretion of tumour produts, and surgial/interventional treatment of valvar pathology. Heart failure management General measures for the treatment of heart failure inlude salt and water restrition, and monitoring of fluid balane and weight. General mobility and ompression stokings an help to prevent the development of deep venous thrombosis and epithelial breakdown from gross peripheral oedema. Right heart failure an be suessfully treated with a ombination of loop diuretis and digoxin. Often, loop diuretis alone are enough to ahieve suffiient fluid loss, but if additional diuresis is required, the judiious oadministration of a thiazide diureti usually produes the desired effet. 15 Digoxin is believed to help with right ventriular ontratility although the data on pure right sided heart failure (without onomitant lung disease or pulmonary hypertension) are limited. 7 Pharmaotherapy The use of somatostatin analogues has been noted to provide symptomati improvement and improved survival in patients with arinoid heart disease. Otreotide is an eight amino aid peptide that, by binding to somatostatin reeptors, has Figure 2 (A) Transthorai ehoardiogram in a modified apial four hamber view showing thikened and rigid triuspid valve (TV) leaflets in an abnormal, fixed open position during systole. Endoardial plaque formation of the subvalvar apparatus is also notable. (B) Colour flow Doppler imaging in the same view shows severe triuspid regurgitation through a wide regurgitant orifie. MV, mitral valve; RA, right atrium; RV, right ventrile. Figure 3 Continuous wave Doppler profile of severe triuspid regurgitation showing the harateristi dagger shaped spetrum with an early peak pressure and rapid deline.
4 the diret effet of reduing the vasoative peptides that provoke the arinoid syndrome. Treatment with otreotide gives rise to both diretly observable linial benefit and measurable biohemial improvement. About 70% of patients obtain symptomati relief from diarrhoea and flushing, showing a derease in measurable 5-HIAA urinary seretion and serum 5-HT onentrations. 16 Otreotide is usually administered subutaneously in 2 4 divided doses varying between mg/day. 17 Both blood pressure and blood gluose should be arefully monitored when administering the drug. A newer somatostatin analogue, lanreotide (or BIM23014, angiopeptin and somatuline), may be used as an alternative to otreotide with the advantage of less frequent administration. 18 There is some evidene that the use of leuoyte interferonalpha ontrols the seretion of tumour produts. It stimulates T lymphoytes and an produe a notable redution in tumour size with evidene of survival benefit. Interferonalpha an be used in onjuntion with somatostatin antagonists. Unfortunately, however, there are no data to suggest that either interferon or otreotide an ause any regression of the ardia damage aused by arinoid disease. Surgial and interventional treatment In seleted ases, balloon valvoplasty of the right sided valves has produed symptomati improvement in patients with stenoti triuspid or pulmonary valves, although reurrent symptoms have been observed. In suitable andidates, valve surgery is the only definitive treatment for severe right heart failure, as the arinoid syndrome may produe pronouned morphologial defets of the right sided valves. Patients with arinoid heart disease usually die as a result of severe triuspid regurgitation 7 rather than arinomatosis. Therefore, onsideration should be given to the suitability of a patient for valve surgery even in metastati disease, unless the metastati proess is likely to lead to imminent demise. It is usually onsidered preferable to operate early or soon after the onset of ardia symptoms, as delay an result in worsening right ventriular failure and inrease the risk of surgery. Perioperative management may involve the use of an intravenous bolus or infusion of otreotide to redue the risk of intraoperative hypotension. Ketanserin given orally for the week leading up to surgery helps to redue the risk of a hypertensive risis, but an ause QT prolongation and should therefore be given autiously to prevent the risk of ventriular arrhythmias. Antihistamines are also used before surgery to prevent flushing and bronhospasm; ortiosteroids an be used to redue bradykinin prodution. In the triuspid position, mehanial valvar prostheses are believed to be adequately durable and relatively unaffeted by the vasoative substanes ausing the original valve pathology. However, their use is disadvantaged by the fat that arinoid patients often have extensive liver metastases and therefore are at very high risk from bleeding as a result of the mandatory use of antioagulant treatment. Bioprostheti valves might, on balane, be preferable as antioagulation an be avoided, and the life expetany of the patient is likely to be shorter than that of the valve. 7 Unfortunately, triuspid valve repair is not usually feasible as the leaflets are so restrited that there is a strong possibility of residual postrepair stenosis. There is some debate regarding the optimal surgial management of the pulmonary valve; the two options inlude valvetomy or valve replaement. Although the data are sparse, a reent small study of 22 patients Carinoid heart disease: key points Carinoid tumours are rare neuroendorine malignanies mostly arising within the gastrointestinal system, partiularly the ileum and appendix The arinoid syndrome, haraterised by utaneous flushing, seretory diarrhoea, and bronhospasm, ours seondary to the paraneoplasti effets of vasoative tumour produts suh as serotonin and only ours in the presene of metastati spread Raised mean 24 hour urinary exretion of 5-hydroxyindole aeti aid (5-HIAA), an end produt of serotonin metabolism, is a key diagnosti finding Carinoid heart disease ours in approximately 50% of patients with the arinoid syndrome and usually heralds a worsening prognosis The vast majority of patients with arinoid heart disease develop right heart failure aused by severe dysfuntion of the triuspid and pulmonary valves Palliation of symptoms and prolonged survival an be ahieved with appropriate medial treatment and valvar surgery in seleted patients with arinoid heart disease suggested that pulmonary valve replaement redued the risk of right heart dilatation postoperatively. 21 In general, there is evidene to support an inrease in both longevity and quality of life in patients suessfully treated by surgery. However, those over the age of 60 years are onsidered to have a high surgial mortality, with one study quoting a 63% death rate, 23 possibly even higher in patients with signifiant o-morbidity. More reassuringly, a reent small study suggests that preoperative ontrol of arinoid ativity with drug treatment, followed by metiulous perioperative anaestheti and surgial are, may lead to a more aeptable mortality rate of approximately 20%, even in patients with left sided involvement. 10 ACKNOWLEDGEMENTS The authors state that they have read the above artile and agree with its ontent. They also onfirm that it has not been published elsewhere, nor is it for onsideration in any other journal for publiation. There is no onflit of interest from any party.... Authors affiliations D J Fox, R S Khattar, Manhester Heart Centre, Manhester Royal Infirmary, Oxford Road, Manhester, UK REFERENCES 1 Bassan MD, Ahlman H, Wangberg B, et al. Biology and management of the midgut arinoid syndrome. Am J Surg 1993;165: Shweizer W, Gloor F, Von Bertrab R, et al. Carinoid heart disease with left sided lesions. Cirulation 1964;29: Strikman NE, Rossi PA, Massumkhani GA, et al. Carinoid heart disease: a linial, pathologi and therapeuti update. Curr Prob Cardiol 1982;6: Spatz M. Pathogeneti studies of experimentally indued heart lesions and their relation to arinoid syndrome. Laboratory Investigation 1964;13: Khan MA, Herzog CA, St Peter JV, et al. The prevalene of ardia valvular insuffiieny assessed by transthorai ehoardiography in obese patients treated with appetite suppression drugs. N Engl J Med 1998;339: Important study demonstrating the toxi effets of inreased irulatory 5-HT onentrations aused by appetite suppression drugs, mimiking arinoid and ausing endoardial fibrosis. 6 Pellikka PA, Tajik AJ, Khandheria BK, et al. Carinoid heart disease. Clinial and ehoardiographi spetrum in 74 patients. Cirulation 1993;87: Largest series of arinoid patients with omprehensive ehoardiographi data demonstrating the spetrum of strutural valvar and ardia abnormalities, linial presentations, and therapeuti options
5 Connolly HM, Nishimura RA, Smith HC, et al. Outome of ardia surgery for arinoid heart disease. J Am Coll Cardiol 1995;25: Westberg G, Wangberg H, Ahlman C, et al. Predition of prognosis by ehoardiography in patients with midgut arinoid syndrome. Br J Surg 2001;88: Moller JE, Connolly HM, Rubin J, et al. Fators assoiated with the progression of arinoid heart disease. N Engl J Med 2003;348: Most reent large study, examining in partiular key diagnosti features to look for in patients whih may herald an adverse or poorer outome. 10 Connolly HM, Shaff HV, Mullany CJ, et al. Surgial management of left sided arinoid heart disease. Cirulation 2001;104:I Case series of 11 patients with left sided arinoid heart disease showing improved long term outome in operative survivors. The authors onlude that ardia surgery should be onsidered early in appropriate patients 11 Zuetenhorst JM, Bonfrer JMGM, Korse CM, et al. The role of urinary 5- hydroxyindoleaeti aid exretion and plasma levels of atrial natriureti peptide, transforming growth fator beta and fibroblast growth fator. Caner 2003;97: Sirois I, Pothier J, Couture C, et al. Atypial presentation of arinoid syndrome. Can J Cardiol 1999;15: Johnson SD, Johnson PW, O Rourke D. Carinoid onstritive periarditis. Heart 1999;82: Pandya U, Pellikka P, Enriquez-Sarano M, et al. Metastati arinoid tumour to the heart: ehoardiographi-pathologi study of 11 patients. J Am Coll Cardiol 2002;40: Warrell DA, Cox TM, Firth JD, Benz EJ, eds. Oxford textbook of mediine, 4th ed. Oxford: Oxford University Press, Matthew HK, Robert JM. Carinoid tumours. N Engl J Med 1999;340: Anderson AS, Krauss D, Lang R. Cardiovasular ompliations of malignant arinoid disease. Am Heart J 1997;66: General review of arinoid heart disease inluding historial bakground of the ondition and in-depth disussion of treatment options. The artile is supplemented by lear diagrams and high quality ehoardiographi images. 18 Janmohamed S, Bloom SR. Carinoid tumours. Postgrad Med J 1997;73: Casthely PA, Jablons M, Griepp RB, et al. Ketanserin in the preoperative and intraoperative management of patients with arinoid tumour undergoing triuspid valve replaement. Anesth Analg 1986;65: Houghton K, Carter JA. Perioperative management of arinoid syndrome using Ketanserin. Anaesthesia 1986;41: Connolly HM, Shaff HV, Mullany HJ, et al. Carinoid heart disease: impat of pulmonary valve replaement on right ventriular funtion and remodelling. Cirulation 2002;106(12 suppl I): Observational study showing that pulmonary valve replaement appears to be better than simple pulmonary valvetomy with a redution in right heart size and improved linial outome. 22 Defraigne JO, Jerusalem O, Soyeur D, et al. Suessful triuspid valve replaement and pulmonary valvotomy for arinoid heart disease. Ata Chiurge Belg 1996;96: Robiolio PA, Rigolin VH, Harrison JK. Preditors of outome of triuspid valve replaement in arinoid heart disease. Am J Cardiol 1995;75: LEARNING ON THE WEB... Case 7: Reurrent pleural effusions, resistant atrial arrhythmias, and abnormal liver funtion tests: general mediine or ardiology? N Melikian, J Anderson*, D Lefroy, Departments of Cardiology and Cardiothorai Surgery*, Hammersmith Hospital, London, UK A 65 year old man presented with reurrent pleural effusions. Repeated pleural fluid examination and pleural biopsy were unremarkable. Periardial alifiation was noted on admission and attributed to an unompliated episode of periarditis 30 years previously. His symptoms and signs were not thought not to be assoiated with the heart. While awaiting an open pleural biopsy the patient was admitted with a further pleural effusion, jaundie, resistant atrial arrhythmias, and dyspnoea. Hepati investigations inluding autoantibody sreen and transjugular liver biopsy were normal. The signifiane of these signs and symptoms, the diagnosis, and the management of these problems are disussed in an interative ase presentation. To aess the interative ase visit BMJ Online Learning (free aess; registration required) Correspondene to: Dr N Melikian; drnarbeh@hotmail.om
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