Lymphangitis carcinomatosis is the malignant infiltration and inflammation of lymphatic vessels secondary to the metastatic spread of malignancy from a primary site. The carcinomatous infiltration of the lymphatic vessels almost always occurs in the pulmonary interstitial lymphatics (pulmonary lymphangitic carcinomatosis) though rare reports of lymphangitic carcinomatosis of skin, duodenum & kidney(non-pulmonary lymphangitic carcinomatosis) have been described in the literature.
Our focus of attention in this review is about pulmonary lymphangitic carcinomatosis, which almost always represents the clinical form of lymphangitic carcinomatosis. The terms pulmonary lymphangitic carcinomatosis & pulmonary tumor embolism represent end-stage manifestations of malignancies and have been used synonymously in the literature given highly similar clinical & radiological features though the former represents a pathology predominantly restricted to the interstitium with absent tumor cells in pulmonary arteries and or capillaries, whereas the latter demonstrates the presence of tumor cells inside the pulmonary vessels.
Dr. Gabriel Andral was the first to describe pulmonary lymphangitic carcinomatosis in 1829 in a case of uterine malignancy. Subsequently, Troissier & Reynaud made a detailed description of the gross anatomy & histopathology in 1874. Although pulmonary lymphangitic carcinomatosis usually represents an end-stage malignancy with poor life expectancy, reports of increased survival have been observed in recent literature. The commonest causes for lymphangitic carcinomatosis include breast, lung, stomach, prostate, pancreas, colon, cervix, & uterine malignancies.
Only about 6 -8 % of pulmonary metastasis is caused by lymphangitic carcinomatosis. 80 % of pulmonary lymphangitic carcinomatosis is caused by adenocarcinomas. The commonest primaries include carcinoma of breast, lung, stomach, colon, prostate, pancreas, cervix, uterus, thyroid, and larynx. Other reported sites of primary include lip, tonsil, pharynx, hypopharynx, mandible, choriocarcinoma, hepatocellular carcinoma, malignant melanoma, malignant pleural mesothelioma and carcinoma of unknown primary.
Interesting reports of hepatic carcinoma manifesting as pulmonary lymphangitic carcinomatosis eight weeks after a liver transplant, and renal cell carcinoma presenting as pulmonary lymphangitis carcinomatosis barely two weeks after resection of the primary renal tumor is available in the literature. Though pulmonary lymphangitic carcinomatosis is rare in children, cases have been reported in renal cell carcinoma, chondrosarcoma, skin, colon, and cancer of unknown primary.
Determination of true clinical incidence & prevalence of pulmonary lymphangitic carcinomatosis is challenging, given subtle symptoms & delayed diagnostic consideration often resulting in post mortem confirmation. Pulmonary lymphangitic carcinomatosis represents only 6 to 8% of pulmonary metastasis.
Lymphangitic carcinomatosis seems to occur in the age of 40 to 49 years. A recent meta-analysis of case reports published over 48 years showed the mean age of 49.21 years. There was no difference between sexes. The commonest primary site was breast (17.3%), followed by lung & stomach (10.8 % each). Two different studies by Bruce et al. and Ikezoe et al. also found carcinoma breast as the commonest cause of pulmonary lymphangitic carcinomatosis.
Pulmonary lymphangitic carcinomatosis & pulmonary tumor embolism represents end-stage manifestations of malignancies and has been used interchangeably in the literature although the former represents a pathology predominantly restricted to the interstitium with absent tumor cells in pulmonary arteries and or capillaries, whereas the latter demonstrates the presence of tumor cells inside the pulmonary vessels. Pulmonary hypertension & right heart strain are much more common in pulmonary tumor embolism when compared to lymphangitic carcinomatosis.
The distribution of pulmonary lymphatics is in the peribronchovascular, centrilobular, interlobular & subpleural locations. There are many theories regarding the metastatic tumor spread predominantly confined to lymphatics though the exact mechanism is still unclear. One theory proposes the initial hematogenous spread of tumor cells, which causes obliterative endarteritis and subsequently pierce the vascular endothelium to reach the perivascular lymphatics to be stationed there. Direct entry into lymphatic circulation is feasible once a nearby lymph vessel (e.g., thoracic duct) is invaded.
Widespread retrograde permeation & embolization can occur once the hilar lymph nodes are involved. Trans diaphragmatic spread has also been proposed to explain lymphangitic carcinomatosis caused by infra diaphragmatic neoplasms. Local obstruction and fluid accumulation ensue soon after the tumor cells are trapped in the lymphatic vessels. Thickening of bronchovascular bundles and alveolar septa follows due to tissue edema,& the presence of nodular thickening suggests the possibility of the tumor cells growing locally.
Macroscopically lungs might appear normal or show white streaks representing distended lymphatic vessels on the pleural or the cut surfaces. The above streaks might also be seen from lung hila to the periphery. Obstruction & distension of the lymphatics by the tumor cells without invasion of the vessel is classically described in lymphangitic carcinomatosis.
Unexplained progressive dyspnea, which evolves over days to weeks, is the commonest presentation in almost 60 % of patients. Although a history of underlying malignancy is noted in most cases, lymphangitic carcinomatosis could rarely be the initial presentation of an occult malignancy. Pleuritic chest pain will be present if the neoplasm obstructs the subpleural lymphatics. Cough, hemoptysis, weight loss, and lethargy are usually uncommon though a report of pulmonary lymphangitic carcinomatosis presenting with isolated chronic cough is reported in the literature. Asymptomatic presentations do exist where the diagnosis is incidentally made during radiologic surveillance of a preexisting malignancy.
Physical examination may reveal a low-grade fever, tachypnoea, and tachycardia. The respiratory evaluation usually reveals a clear chest, with the rare occurrence of adventitious sounds. The clinical signs &symptoms of pulmonary lymphangitic carcinomatosis and pulmonary tumor embolism could often overlap. Features of cor pulmonale and pulmonary hypertension, such as prominent pulmonary second heart sound, right ventricular heave, elevated jugular venous pressure, and cyanosis are less commonly noticed in pulmonary lymphangitic carcinomatosis when compared to pulmonary tumor embolism.
Diagnostic suspicion of pulmonary lymphangitic carcinomatosis is often arrived based on clinical background, the history & clinical features supported by characteristic imaging findings. The definite confirmation of diagnosis needs cytology and/or biopsy & histopathology, which is usually performed only on patients who are safe to undergo the procedure. The closest differential diagnosis for pulmonary lymphangitic carcinomatosis is pulmonary tumor embolism. Other pulmonary interstitial pathologies also need to be ruled out.
Imaging is an insensitive modality for the detection of pulmonary lymphangitic carcinomatosis as well as pulmonary tumor embolism and often normal in initial stages. However, imaging is often performed to diagnose or rule out other causes for dyspnoea & cardio-respiratory symptoms rather than to diagnose lymphangitic carcinomatosis.
X-ray chest: Often normal (in 30 to 50 %), especially in the initial stages. Reticular, nodular, or reticulonodular patterns with coarse bronchovascular features are often noted as the disease advances. The abnormalities are often bilateral &predominantly seen in lower lobes, although unilateral & asymmetric changes are also seen. Kerley A &B lines typically represent interstitial lymphangitic edema. Hilar/mediastinal adenopathy (in 20 to 40% of cases & are usually asymmetric) with associated pleural effusions (in one third to half of the patients) are observed. Signs of pulmonary hypertension is much more commonly seen in tumor embolism rather than lymphangitic carcinomatosis.
CT thorax: Interlobular septa & peribronchovascular interstitium exhibits smooth (early stage), or nodular thickening(late development).Thickened interlobular septa form polygonal arcades(tessellating polygons) with thickened limbs. Interstitial edema or parenchymal extension of tumors often results in ground-glass opacities. The abnormalities could be on one or both sides, focal or widespread, symmetrical, or asymmetrical. Smooth or irregularly thickened interlobular septa are more in favor of lymphangitic carcinomatosis rather than tumor embolism. Although nodular thickening of septa is believed to differentiate lymphangitic carcinomatosis from other interstitial lung patterns, certain pathologies like sarcoidosis & asbestosis can closely mimic the same. Another differentiating feature in pulmonary lymphangitic carcinomatosis pathology is the preservation of the general as well as the lobular architecture of the lung.
V/Q scans: V/Q scan is of limited help in the diagnosis of pulmonary lymphangitic carcinomatosis since they are often normal. However, a study on 32 patients has shown that pulmonary lymphangitic pattern in perfusion scan has been associated with extremely poor prognosis, which helps attending physicians in making crucial treatment decisions.
F-18 FDG PET/CT is found to be 86% sensitivity and 100% specificity in detecting pulmonary lymphangitic carcinomatosis by subjective analysis. The mean, standard uptake value(SUV) was 1.37 +/- 0.64 in the lymphangitic area in comparison with 0.51 +/- 0.29 in the normal lung. The standard uptake ratio (SUR) of mediastinal blood pool to the lymphangitic lung was 1.26 +/- 0.45, whereas the ratio between the blood pool to the normal lung was 3.78 +/-1.37. Another study showed that enhanced diffuse uptake of FDG is consistent with the pulmonary lymphangitic pattern, & total lesion glycolysis(TLG) of the primary lung tumor was a strong predictor of progression-free survival(PFS) in non-small cell carcinomas. Diagnosis of lymphangitic carcinomatosis using gallium-68 prostate-specific membrane antigen in a 53-year-old man with prostatic malignancy has been reported.
Conventional pulmonary arteriography & EBUS are unhelpful in making a diagnosis of pulmonary lymphangitic carcinomatosis but might be able to suggest a diagnosis of pulmonary tumor embolism, which is the close differential diagnosis of pulmonary lymphangitic carcinomatosis.
Laboratory evaluation: findings are often non-specific. A small increase in leucocytes may be noted secondary to stress response.D-dimer values are non-specific. Arterial blood gas typically shows hypoxemia, respiratory alkalosis with a widened A-a gradient. Pulmonary function tests done in stable patients could show a restrictive pattern with decreased diffusion capacity. ECG and ECHO could be normal & may reveal signs of right ventricular strain & pulmonary hypertension, which is more commonly seen in pulmonary tumor embolism. A mean pulmonary artery pressure more than 40 mmHg rules out acute pulmonary embolism in most patients, though mean pulmonary artery pressure more than 40 mmHg could also be seen in any chronic pulmonary hypertension apart from pulmonary tumor embolism.
Histopathological diagnosis: Histopathology is an accurate measure to diagnose pulmonary lymphangitic carcinomatosis though it is not feasible in many clinical circumstances. In real practice, many authors have observed that by the time a dyspnoeic patient with suspected pulmonary lymphangitic carcinomatosis gets evaluated with varying imaging modalities, she/he might have already progressed to severe respiratory distress, making him or her unfit for any invasive diagnostic procedure. Most often, the postmortem evaluation provides a retrospective diagnosis in such cases.
The decision regarding the utilization and the choice of intervention to achieve a definite histologic/cytologic diagnosis in a given patient with suspected pulmonary lymphangitic carcinomatosis is made after a complete consideration of the general condition of the patient with the safety of the proposed procedure, the stage & expected prognosis of the underlying malignancy, availability of effective anti-cancer therapy for the underlying tumor & finally the choice and decision of the patient. The expected yield by the particular intervention & the procedural risks is always taken into account. Sincere assessment of risks versus potential benefits from the intervention is mandatory. It is not surprising that many clinicians & patients often opt for management plans based on radiologic findings rather than an invasive diagnostic procedure, especially in advanced malignancies with poor expected prognosis.
Bronchoscopy and bronchoalveolar lavage (BAL) may show malignant cytology in lymphangitic carcinomatosis though a negative report can not rule out malignancy. Lung biopsies are usually attempted only in patients with an adequate cardiopulmonary reserve and who are stable enough to undergo the procedure. Transbronchial lung biopsy is expected to provide a high yield in diffuse lung diseases like lymphangitis carcinomatosis with insignificant procedural complications. Few centers have started using transbronchial lung biopsy using cryoprobes, which is expected to improve the diagnostic yield by providing more tissue volume without distortion of architecture. If transbronchial lung biopsy is negative, surgical lung biopsy(open lung biopsy) is often considered for a definite diagnosis in a suitable patient. Although surgical biopsy has the highest yield, it has higher procedural risks too. A video-assisted thoracoscopic biopsy is also considered to be a safe intervention in stable patients & provides good yield in expert hands.
Right heart catheterization is usually performed in patients who are unfit for an invasive diagnostic procedure and do not help in diagnosing pulmonary lymphangitic carcinomatosis. Positive aspiration cytology for malignant cells from a wedged pulmonary artery catheter may give a clue for pulmonary tumor embolism. A mean pulmonary artery pressure value of more than 40 mm Hg practically rules out acute pulmonary embolism.
Presumptive diagnosis: In unstable patients whose histologic/cytology diagnosis could not be achieved with non-invasive or semi-invasive interventions, the invasive interventions are also often deferred & a presumptive diagnosis is made on the basis background history, clinical symptoms & signs, and imaging. This approach is commonly considered in patients who are having an advanced underlying malignancy with poor functional status with a poor response documented or expected to anti-cancer therapy. The possible life-threatening risks involved in such invasive diagnostic measures are unacceptably high in such patients when compared to potential benefits. Patient & family need to be adequately involved & counseled in such decisions.
The management is discussed under the headings of definitive and supportive. The prognosis remains poor with both the above measures once a diagnosis of pulmonary lymphangitic carcinomatosis is established. If pulmonary lymphangitic carcinomatosis is the initial mode of presentation of underlying malignancy & underlying malignancy has subsequently been confirmed, attempts at definitive therapy involve consideration for surgical resection/chemotherapy /radiotherapy after a definite diagnosis & staging of the underlying tumor is made.
Only tumors with effective anti-tumor agents will respond to chemotherapy (e.g., Wilms tumor/trophoblastic tumors). There are isolated reports of considerable remission of pulmonary lymphangitic carcinomatosis in various malignancies with hormonal therapy, chemotherapy, tyrosine kinase inhibitors(eg.apatinib), and certain monoclonal antibodies(e.g., bevacizumab, cetuximab). A report of intravenous eribulin successfully achieving rapid symptom control and partial remission with the disappearance of pulmonary lymphangitic carcinomatosis in a case of metastatic breast carcinoma in visceral crisis has also been published.
Supportive care involves the organ support measures (e.g., oxygen, non-invasive ventilation/mechanical ventilation, or inotropes) provided during attempts at diagnosis or definitive therapy is made. Many patients with a history of advanced underlying malignancy and poor quality of life who present with signs and symptoms of pulmonary lymphangitic carcinomatosis often opt for non-invasive radiology based presumptive diagnosis and end up receiving a course of empiric antibiotics along with oxygen supplementation.
Intravenous steroids are prescribed by many physicians for symptomatic relief of symptoms, although there is no scientific evidence for this traditional practice. Opiates & benzodiazepines could be used judiciously for control of dyspnoea & anxiety. Diuresis and pulmonary vasodilators are considered if there is evidence of heart failure. Focus on palliative measures are initiated once comfort care decision is finalized in a given patient with advanced progressive non-responsive malignancy.
The nearest differential diagnosis to pulmonary lymphangitic carcinomatosis is pulmonary tumor embolism. Signs and symptoms of pulmonary hypertension and cor pulmonale are much more common in the latter. Although clinical and radiological overlaps are common, both conditions represent end-stage malignancy and are evaluated and managed similarly. Pulmonary lymphangitic sarcomatosis is a rare but closely resembling entity with similar clinical and imaging features.
Pulmonary embolism(thrombotic as well as non-thrombotic), obstructive airway disease, community-acquired pneumonia, especially viral, atypical, or fungal pneumonia with an interstitial pattern(eg.pneumocysis jirovecii), ARDS, pulmonary hypertension, and heart failure could easily mimic lymphangitis carcinomatosis clinically and radiologically.
Interstitial lung diseases to be considered include acute idiopathic interstitial pneumonitis, cryptogenic organizing pneumonia, severe eosinophilic pneumonia, sarcoidosis, hypersensitivity pneumonitis, alveolar hemorrhage syndrome, connective tissue disorder associated interstitial lung diseases,drug-induced lung disease, radiation pneumonitis, lymphomas, and vasculitis.
Erdheim-Chester disease, a rare proliferating form of non-Langerhans histiocytosis presenting with respiratory symptoms with radiology closely mimicking lymphangitic carcinomatosis, has been described in the literature.
Diagnosis of pulmonary lymphangitic carcinomatosis is considered to represent end-stage malignancy, with the life expectancy being about six months. However, reports of survival up to 3 years and more have also been reported with currently available management.
Bruce et al. observed death within three months of presentation of respiratory symptoms in half of the patients, and Zhang et al. noted that almost 72% of the patients died within seven months of presentation. A recent systematic review has observed an increased survival of patients between the years 2000 to 2018 when compared to years between1970 to 1999. Survival is noted to cut short considerably after an event of hospital admission. Improved survival has been reported in lymphangitic carcinomatosis with hormonal therapy (e.g., prostate), chemotherapy (e.g., breast, ovary, cervix, stomach), tyrosine kinase inhibitors (apatinib), and monoclonal antibodies (e.g., colon cancer).
The immediate complication of an advanced pulmonary lymphangitic carcinomatosis could be severe hypoxemia and respiratory failure, which will ideally require intubation & mechanical ventilation. The severe hypoxemia is due to the extensive interstitial involvement with impairment of gas transfer. Complications are also attributable to the complications of underlying malignancy and also to the side effects of chemotherapeutic agents. An acute thrombotic pulmonary embolism aggravating the pre-existing respiratory failure is quite possible in such patients who are relatively immobile due to persistent dyspnoea with risks for deep vein thrombosis.
Also, an episode of lower respiratory infection could aggravate the dyspnoea & underlying respiratory failure. Though the vast majority of organ supports are going to be futile, in certain patients (e.g., with underlying COPD), the respiratory crisis might have been precipitated by a potentially reversible infection that needs administration of antimicrobials. Ventilator-associated complications, including barotrauma & infections, could develop if invasive ventilatory support is employed in such scenarios.
When the cause of respiratory failure (eg.pulmonary lymphangitic carcinomatosis versus interstitial pneumonia) is undiagnosed at admission in a patient without underlying malignancy, then the complications could also result from attempts at definite diagnostic measures including transbronchial lung biopsy or open surgical biopsy.
The life expectancy in pulmonary lymphangitic carcinomatosis remains very poor. Most patients who present with signs & symptoms of pulmonary lymphangitic carcinomatosis will be having an underlying history of malignancy though occasionally, the initial presentation of occult malignancy could be pulmonary lymphangitic carcinomatosis. In a patient coming to the hospital, which is already diagnosed to have a malignancy with pulmonary lymphangitic carcinomatosis, pulmonary and critical care, as well as an oncology consult, is a must for further evaluation and coordination of the management.
Few patients might get benefit from intensive care (on a case to case basis), including a trial of non-invasive ventilation and/or mechanical ventilation if the respiratory failure is presumably precipitated by a potentially treatable or reversible causes like an infection or pulmonary embolism. Infectious disease consult could be obtained in difficult to diagnose cases. Occasionally the patient may present with signs & symptoms of pulmonary lymphangitic carcinomatosis without a history of underlying malignancy. Here again, extensive evaluation needs to carried out by pulmonologists to reach a definite diagnosis of the lung pathology, and the oncologists need to evaluate for a potential neoplastic primary.
A palliative care consult is routinely advised once the cytology/histopathology of pulmonary lymphangitic carcinomatosis is confirmed or a presumptive diagnosis of pulmonary lymphangitic carcinomatosis has been made because of an advanced non-treatable underlying malignancy with the patient being unfit to undergo a safe diagnostic procedure to ascertain the lung pathology. Psychologic or psychiatric counseling is recommended to help the patient & family to cope up with news of very advanced malignancy.
Maintenance of excellent communication skills by the caregivers helps the patient and family to make appropriate decisions in times of rough weather. Proved or suspected lymphangitic carcinomatosis typically represents an advanced underlying malignancy with very poor life expectancy. The usual complications and poor expected life span and the likely futility of invasive organ support measures need to discussed in detail with the patient and family members to help them to chalk out a clear plan of action. Attempts at definite histopathologic diagnosis in the form of transbronchial lung biopsy or surgical lung biopsy could be considered only in patients who are stable and safe for such procedures.
Many patients who are having advanced malignancy & who are unfit for a diagnostic procedure need have to be treated conservatively and palliatively with the presumptive diagnosis of pulmonary lymphangitic carcinomatosis. However, potentially reversible factors like a lower respiratory infection precipitating the acute respiratory crisis need to be always considered and merits a treatment trial on a case to case basis.
Occasionally the patient may present with signs and symptoms of pulmonary lymphangitic carcinomatosis without a history of underlying malignancy. Here again, extensive evaluation needs to carried out to reach a definite diagnosis of lung pathology, including the search for a potential primary. Here again, excellent communication skills by physicians and paramedical staff help the patient and family to endorse a concrete plan of action.
Pulmonary lymphangitic carcinomatosis represents end-stage malignancy, and the expected life span is usually poor though recent studies have noted an enhanced survival in the last two decades. The decision regarding the utilization as well as the choice of invasive diagnostic measures to achieve a definite tissue diagnosis should be decided on a case to case basis based on the nature and stage of underlying malignancy, the availability of effective and specific treatment measures, and most importantly the fitness of the patient to undergo a safe procedure. Presumptive diagnosis and palliative care need to be considered in patients with advanced underlying malignancy and in whom the life-threatening risks of invasive procedures far outweigh the potential benefit.
Management of a pulmonary lymphangitic carcinomatosis patient often encounters diagnostic,treatment-related, and ethical dilemmas. Close interaction, communication, and coordination between various specialty teams help to deliver the best management to a given patient. Excellent communication skills are a must to appraise the patient, as well as the family, regarding the given complex scenario in a particular patient, which will help them in making decisions about further evaluation &management measures.
A patient who is already having a diagnosed and treated malignancy might present with lymphangitic carcinomatosis features where the attending pulmonologist may have to consider confirming the diagnosis histopathologically by doing a transbronchial lung biopsy. BAL positivity for malignancy may strongly suggest lymphangitic carcinomatosis in the right clinical and radiologic settings though the negative BAL for malignancy can not rule out lymphangitic carcinomatosis. Close coordination and discussions with the radiology team could help to reach a presumptive diagnosis where invasive diagnostic measures are likely to cause more harm in a given unstable patient with poor cardiorespiratory reserve.
Oncology inputs are invaluable in trying certain newer available therapies on a compassionate basis. Palliative care physicians need to be involved to re-ensure that the patients with histopathologically/cytologically proved pulmonary lymphangitic carcinomatosis, and also the presumptively diagnosed patients due to an unstable and unsafe general condition to undergo invasive diagnostic procedures are provided appropriate comfort care. Psychologist or psychiatry help may be required for managing patients and families who are not able to cope with the negative emotional impact associated with the terminal diagnosis. The caregivers need to maintain close communication and empathy towards the patient and family in such a situation.
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