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Lymphoplasmacytic lymphoma Microchapters

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Editor-In-Chief: C. Michael Gibson, M.S., M.D. [1]; Associate Editor(s)-in-Chief: Sara Mohsin, M.D.[2]

Synonyms and keywords: Waldenstrom's macroglobulinemia; Waldenstrom's disease; Primary macroglobulinemia; Hyperviscosity syndrome

Overview

Historical Perspective

  • In 1936, Jens Bing and Axel Valdemar Neel, discovered a late and rare complication of WM known as Bing-Neel syndrome (BNS), who observed a case of 2 women, 56 and 39 years old, presenting with rapid neurodegeneration in the setting of hyperglobulinemia.
  • In 1944, Jan G. Waldenstrom, a Swedish doctor of internal medicine, first discovered Waldenstrom macroglobulinemia(WM). He reported an unusal presentation of fatigue, lymphadenopathy, bleeding from nose and mouth, worsening anemia, elevated sedimentation rate, low serum fibrinogen levels (hypofibrinogenemia), hyperviscosity, and hypergammaglobulinemia in two patients due to increased levels of a class of an abnormal high molecular weight serum protein called macroglobulins.[1][2]
  • In 1962, the first report on familiality in WM was published, and since then many cohort studies as well as small case-control studies have been published showing familial aggregation of WM.[3][4][5][6][7][8][9][10][11] [12][13][14][15]
  • In 1994, a Revised European-American classification of lymphoid neaoplasms (REAL) was published by International Lymphoma Study Group which placed WM in the category of lymphoplasmacytic lymphoma (an indolent subtype of non-hodgkins lymphoma). The REAL classification is based on the morphology, immunophenotype, genetic features, and clinical features.[16][17]
  • In 2001, WHO also classified the pathology of WM as lymphoplasmacytic lymphoma/Waldenstrom macroglobulinemia based on REAL classification.[2]
  • In September 26-30, 2002, a consensus group at the Second International Workshop on WM in Athens, Greece, defined WM as a distinct clinicopathologic entity with characteristics of bone marrow infiltration associated with IgM monoclonal gammopathy by WM and proposed a diagnostic criteria forn WM.[2][18]
  • In 2009, in Arkansas, a patient of Bing-Neel syndrome discontinued the treatment for BNS which included, "intrathecal chemotherapy with several cycles of systemic chemotherapy followed by autologous stem cell-supported High-dose chemotherapy and bone marrow transplant|high-dose therapy transplant", and in 2013, was still asymptomatic when a follow-up report was published.[19]

Classification

There is no established system for the classification of Waldenström's macroglobulinemia. However, according to a devised criteria based upon patient's symptoms, it can be classified into:[18]

  • Symptomatic Waldenstrom macroglobulinemia.
  • Asymptomatic/Smoldering Waldenstrom macroglobulinemia (SWM).[20]
Classification of WM and Related Disorders
Criteria Symptomatic WM Asymptomatic WM IgM-Related Disorders MGUS
IgM monoclonal protein + + + +
Bone marrow infiltration + + - -
Symptoms attributable to IgM + - + -
Symptoms attributable to tumor infiltration + - - -

Pathophysiology

Genetics

Cytogenetics

Epigenetics

Associated Conditions

Several studies showed an increased incidence of following second cancers in patients with Waldenström macroglobulinemia:[37]

Microscopic Pathology

WM/LPL is a form of an indolent (slowly growing) non-hodgkin lymphoma. LPL is called so because the lymphoma cells have the characteristics of both lymphocytes and plasma cells. After a detailed clinicopathological assessment and review of the published literature, the following diagnostic criteria was proposed for WM:[39]

  • IgM monoclonal gammopathy of any concentration.
  • Bone marrow infiltration by:[40][41][42]
    • Small lymphocytes with clumped chromatin, inconspicuous nucleoli, and sparse cytoplasm.
    • Well-formed plasma cells.
    • Plasmacytoid lymphocytes (have cytologic features intermediate between above 2 extremes), in following patterns:[43][44]
      • Diffuse.
      • Interstitial.
      • Nodular.
      • Paratrabecular.
      • Nodular-interstitial.
      • Mixed paratrabacular-nodular.
  • Following lymphoid organs are involved in WM:
    • Bone marrow.
    • Lymph nodes(nodal involvement is characterized by paracortical and hilar infiltration with frequent sparing of the subscapular and marginal sinuses).
    • Spleen.
  • WM has two histologic subtypes:[44]
    • Lymphoplasmacytoid (73%).
    • Lymphoplasmacytic (27%).
  • The cytologic composition and the degree of plasmacytic differentiation varies from case to case.
  • The bone marrow contains variable numbers of pleomorphic lymphoid cells.
  • Dutcher bodies may be seen in plasma cells, as intracytoplasmic inclusions positive for periodic acid Schiff.
  • Mast cell hyperplasia is common and may stimulate tumor cell proliferation and monoclonal IgM secretion.
  • Gene expression profiling has indicated that lymphoid cells of WM more closely resemble those of chronic lymphocytic leukemia than those of myeloma.[45]

Immunohistochemistry

Malignant cells in Waldenström macroglobulinemia have following immunophenotypic characteristics:[42] [22]

Causes

Genetic Causes

  • Waldenström Macroglobulinemia is most probably caused by a somatic mutation in the MYD88 gene (seen in 90% of cases) or CXR4 gene (seen in 30% of cases).[48][49]

Less Common Causes

Less common causes of Waldenström macroglobulinemia may include:[22][50]

  • Chromosomal abnormalities: deletions of 6q23 and 13q14, and gains of 3q13-q28, 6p and 18q.
  • Personal and family history of autoimmune diseases with autoantibodies and chronic immune stimulation leads to 2-3 fold higher risk of developing WM, especially elevated risks are associated with following:
    • Hepatitis C virus infection (overall 20-30% increased risk for non-Hodgkin lymohoma and 3-fold increased risk for WM).[51][52][53]
    • HIV.[52]
    • Rickettsiosis.[52]
    • Sjogren syndrome.[54][55]
    • Autoimmune hemolytic anemia.[54][55]
    • Sarcoidosis.[56]
    • SLE.[55]
  • Hay fever.
  • Environmental factors:
    • According to some recent studies, exposure to following environmental factors seems to have association with the development of WM:[21][57]
      • Occupational (Farming).
      • Pesticides.
      • Paint.
      • Rubber dyes.
      • Benzene.
      • Coal dust.
      • Leather manufacturing.
      • Wood dust.
      • Organic solvents.

Differentiating Lymphoplasmacytic Lymphoma from Other B cell lymphoid neoplasms

Waldenström macroglobulinemia must be differentiated from other B cell lymphoid neoplasms including:

  • Always express CD5
  • Usually CD23 positive[58]
  • Express CD10, HLA-DR, pan B-cell antigens (CD19, CD20, CD79a), CD21, and surface IgM, IgG, or IgA
  • Rearrangement of Bcl-2[61][62]
  • Express CD138, CD38, CD79a, VS38c and CD56 (70%)
  • Presence of plasmacytic cell infiltration of bone marrow, osteolytic lesions, and renal insufficiency
  • Translocation involving chromosome 11 (t11;14)[63]
  • Expresses CD5+ and CD23+
  • Expresses surface IgM, IgD, and cyclin D1 in majority of cases
  • Infiltration of bone marrow by monomorphous small lymphoid cells with irregular nuclei[64][65]
  • Expresses B cell markers CD19, CD20, and CD22
  • Infiltrates the bone marrow with a characteristic intertrabecular and intrasinusoidal pattern
  • Most common cytogenetic abnormalities are loss of 7q (19%) along with +3q (19%) and +5q (10% )[66][67]

Epidemiology and Demographics

  • Lymphoplasmacytic lymphoma is one of the rare subtypes of NHL accounting just 1-2% of it.

Prevalence

  • The prevalence of Waldenström macroglobulinemia is estimated to be 1000-1,500 cases in United States annually.[68][69]

Incidence

  • WM accounts for approximately 1% to 2% of hematologic cancers.[70][69]
  • World-wide, the overall age-adjusted incidence of Waldenström macroglobulinemia is 0.38 cases per 100,000 persons annually, increasing with age to 2.85 in patients above 80 years (or 5 cases per 1 million persons per year).[71]
  • The age-adjusted incidence rate for males is 0.92 per 100,000 person-years.[72]
  • The age-adjusted incidence rate for females is 0.30 per 100,000 person-years.[72]
  • Combined age and sex-adjusted incidence is 0.57 per 100,000 person-years.[72]

Age

  • The incidence of Waldenström's macroglobulinemia increases after 50 years of age.[73]

Gender

  • Men are twice more likely than women to develop WM(5.4 vs. 2.7 per million, respectively). [68][32][74][70]

Race

  • Higher incidence in whites (4.1 per million per year) comparative to blacks (1.8 per million per year) and in past 20 years, incidence in whites has elevated.[68][32][75][70]

Epidemiology and demographics of Smoldering Waldenstrom macroglobulinemia

According to a recent study done in 2017, the following data was found out regarding epidemiology and demographics of SWM.[76]

Epidemiology and demographics of Smoldering Waldenstrom macroglobulinemia according to Sex, Race and Age
Risk factors Proportion of SWM
Sex Males:27.72%, Females:28.31%
Race White, non-hispanic:28.97%, White, Hispanic:24.79%, Black:21.01%, Asian:20.41%, Other:26.08%.
Age in years 18-49:18.32%, 50-64:25.91%, 65-79:30.8%, ≥80 : 27.26%

Risk Factors

Common risk factors in the development of Waldenström macroglobulinemia include:[73]

  • Hepatitis C:
    • Patients with chronic hepatitis C infection have an overall 20-30% increased risk for developing non-Hodgkin lymohoma and 3-fold increased risk for WM.[51][52][53]

Screening

According to the the U.S. Preventive Service Task Force (USPSTF), there is insufficient evidence to recommend routine screening for Waldenström macroglobulinemia.[78]

Natural History, Complications, and Prognosis

Natural History

Complications

Late and rare complications

  • Large cell transformation (Richter syndrome).
    • Dr. Richter of the University of Minnesota first recognized the blockage in maturity of the lymphoma cells at a point when they can't mature beyond the large cell stage thus, leading to large cell transformation.
  • Central Nervous system Lymphoma (Bing-Neel syndrome).[86]
    • The development of Waldenström macroglobulinemia cells in the central nervous system was first described by Drs. Bing and Neel and carries their names as the Bing-Neel syndrome. WM involves CNS in following two forms:
      • Actual tumor developing in the brain substance causing seizures and paralysis.
      • Tumor cells invading meninges and cranial nerves without causing the actual tumors and with or without CSF cryoglobulinemia,[87] leading to following symptoms:[88]
        • Headache.
        • Confusion.
        • Neck stiffness.
        • Sporadic loss of motor function.
        • Facial paralysis.
        • Drooping eyelid.
        • Double vision.
        • Difficult swallowing.
        • Visual loss.
        • Hearing loss.

Prognosis

  • Prognosis is generally poor.
  • The median survival from the time of diagnosis is 6.4 years.[89]
  • The median disease-specific survival is 11.2 years.[89]
  • Approximately 10% patients still live at 15 years.[90][91]
  • 5-year survival rate is 78%.
  • In the last decade (2001-2010), the median overall survival for all WM groups has improved to just over 8 years compared to 6 years in the previous decade (1991-2000).
  • After 2000, a 2-fold increased mortality is reported in patients diagnosed with WM when compared with expected population mortality.[72]
  • The presence of symptoms is associated with a particularly poor prognosis among patients with the disease.
  • Prognosis of asymptomatic patients is similar to that of the general population.[92]

Adverse prognostic factors

  • Some of the pretreatment factors associated with shorter survival in WM patients are:[93][89]
    • Age >/=65 years.
    • Organomegaly (Hepatosplenomegaly).
    • B-symptoms (weight loss, fever or night sweats).
    • Anaemia (Hb < 10.0 g/dl).
    • Platelets <100 x 10(6)/dl.
    • Albumin <3.5 g/dl.
    • Bone marrow lymphoplasmacytic infiltrate >/=50%.
    • Elevated beta2-microglobulin ( associated with 3-fold increase in death).
    • Leucopenia (<4.0 x 10(9)/l).
    • Thrombocytopenia (<150 x 10(9)/l).
    • Quantitative IgM < 0.4 g/l.
    • Hyperviscosity.
  • Other prognostic factors recently studied are:
    • Serum free light chain.[94]
    • Serum lactate dehydrogenase.[95]
    • Serum soluble CD27.[96]
  • Most of the prognostic factors have defined the outcome of Waldenström macroglobulinemia in patients requiring treatment. However, very few studies have evaluated the prognostic factors in patients who don't initially need the treatment.

Risk Stratification Criteria

All the above prognostic data has been combined to risk stratify the WM patients and to formulate a standardized scoring system known as the International Prognostic Staging System for Waldenström's Macroglobulinemia (IPSSWM):[97]

Risk factors Score
Age > 65 1
Hemoglobin ≤ 11.5g/dl 1
Platelet ≤ 100,000μl 1
β-microglobulin > 3mg/l 1
IgM > 70g/l 1
International prognostic scoring system for Waldenström macroglobulinemia
Risk group Score 5-year survival
Low 0-1 (except age) 87%
Intermediate 2 or age>65 68%
High ≥3 36%
International prognostic scoring system for Waldenström macroglobulinemia
Risk group Score Median survival
Low 0-1 (except age) 12 years
Intermediate 2 or age>65 8 years
High ≥3 3.5 years

Diagnosis

  • Not all the diagnostic tests mentioned are performed in a WM patient. A doctor takes into account the following factors before choosing diagnostic tests in a particular patient:
    • Suspected type of cancer.
    • Signs and symptoms.
    • Age.
    • Medical condition of the patient.
    • Results of earlier medical tests.

Diagnostic Study of Choice

There is no single diagnostic study of choice for the diagnosis of Waldenström macroglobulinemia (WM), but bone marrow aspiration and biopsy is considered to be mandatory for assessment of patients with WM and further supported by monoclonal protein/immunophenotypic studies like immunohistochemistry, flow cytometry and cytogenetics to distinguish WM from other types of B-cell lymphomas.[18][98]

Diagnostic Criteria

In September 26-30, 2002, in Athens, Greece,the Second International Workshop was held in which a diagnostic criteria for Waldenstrom's Macroglobulinemia was proposed. According to this criteria, the following findings on performing bone marrow biopsy and serum protein analysis are confirmatory of Waldenström macroglobulinemia:[18]

  1. Presence of IgM monoclonal gammopathy of any concentration on serum protein analysis.
  2. A bone marrow biopsy demonstrating more than 10% infiltration by small lymphocytes showing plasmacytoid/plasma-cell differentiation.with an intertrabecular pattern consistent with lymphoplasmacytic lymphoma.
    • IgM concentration widely varies in WM, and it is not possible to define a concentration that reliably distinguishes WM from other lymphoproliferative disorders. Hence, a diagnosis of WM can be made irrespective of IgM concentration if there is evidence of bone marrow infiltration by lymphoplasmacytoid lymphoma as defined by the Revised European-American Lymphoma classification and WHO criteria.[17] This is a tumor of small lymphocytes showing evidence of plasmacytoid or plasma-cell differentiation.
    • A recent study found that, in 39% of patients, the bone marrow aspirate contained a spectrum of small lymphocytes, plasmacytoid lymphocytes, and plasma cells; in 39% of patients, there was a predominance of small lymphocytes with fewer plasmacytoid lymphocytes or plasma cells, and 22% of patients contained a mixture of small lymphocytes and plasma cells, with rare plasmacytoid cells. Mast cells were increased in 26% of patients.[99]
  3. Intertrabecular pattern of bone marrow infiltration.
  4. Immunophenotype of the lymphoplasmacytic infiltrate consistent with Waldenstrom's macroglobulinemia. This includes: IgM+, CD5-, CD10-, CD11c-, CD19+, CD20+, CD22+, CD23-, CD25+, CD27+, FMC7+, CD103- and CD138+.[100][43][101]

(3,4 are supportive of but not necessary for WM diagnosis).

  • Another diagnostic Criteria for Waldenström Macroglobulinemia and Associated Disorders is as follow:[42]
  1. Waldenström macroglobulinemia:
    • IgM monoclonal gammopathy (regardless of the size of the M protein) with >10% bone marrow lymphoplasmacytic infiltration (usually intertrabecular) by small lymphocytes that exhibit plasmacytoid or plasma cell differentiation and a typical immunophenotype (surface IgM+, CD5–, CD10–, CD19+, CD20+, CD23–) that satisfactorily excludes other lymphoproliferative disorders, including chronic lymphocytic leukemia and mantle cell lymphoma.
  2. IgM MGUS:
    • Serum IgM monoclonal protein level <3 g/dL, bone marrow lymphoplasmacytic infiltration <10%, and no evidence of anemia, constitutional symptoms, hyperviscosity, lymphadenopathy, or hepatosplenomegaly.
  3. Smoldering Waldenström macroglobulinemia (also referred to as indolent or asymptomatic Waldenström macroglobulinemia):
    • Serum IgM monoclonal protein level ≥3 g/dL and/or bone marrow lymphoplasmacytic infiltration ≥10% and no evidence of end-organ damage, such as anemia, constitutional symptoms, hyperviscosity, lymphadenopathy, or hepatosplenomegaly, that can be attributed to a lymphoplasmacytic proliferative disorder.

Definitive Diagnostic Tests

  • Genetic Testing.
    • ARIDA.
    • IG gene rearrangement.
    • CXCR4 5338X.
    • MYD88 L265P.
  • Immunophenotyping.
  • Serum paraprotein.

History and Symptoms

History

  • The onset of Waldenström macroglobulinemia is insidious and non-specific.
  • Approximately 25% of patients with WM are asymptomatic upon presentation; their diagnosis is often made incidentally from routine blood tests done for some other reason. WM found this way is sometimes called asymptomatic or Smoldering WM (SWM).[79]
  • Symptoms develop depending on the tissues involved in the malignant cell infiltration or IgM deposition.[102]

Manifestations of WM

Following is a list of WM manifestations with attributable causes:[18][103][104][105][106][107][108][109][110][111][86][112][113][114][115][116][117][118][119][120][121][122]

Manifestations of WM
Cause Manifestations
Tumor infiltration Cytopenia, fever, night sweats, weight loss, lymphadenopathy, hepatomegaly, spleenomegaly, pulmonary infiltrates, nodules or masses, pleural effusion, abdominal pain, swelling and blood in stools secondary to stomach and bowel infiltration, renal and perirenal masses, maculopapular lesions, plaques or nodules secondary to dermis infiltration, lesions involving retro-orbital lymphoid tissue and lacrimal glands, infiltration of the conjunctiva and malignant vitreitis, Bing-Neel syndrome consists of confusion, memory loss, disorientation, motor dysfunction, and eventually coma.
Circulating monoclonal IgM Hyperviscosity syndrome, Type 1 Cryoglobulinemia (consists of Raynaud's phenomenon, skin ulcers & necrosis and cold urticaria), frequent bruising, prolonged bleeding and clotting times.
IgM deposition into tissues Sub-endothelial deposits in glomerular loops leading to non-selective proteinuria, dehydration, and uremia, Firm, flesh-colored skin papules and nodules have been reported and are called macroglobulinemia cutis, Diarrhea, malabsorption, or gastrointestinal bleeding.
Amyloidogenic properties of IgM Organs more commonly affected by amyloidosis were the heart (44%), the peripheral nerves (38%), the kidneys (32%), the soft tissues (18%), the liver (14%), and lungs (10%), nephrotic syndrome and gastrointestinal involvement.
Autoantibody activity of IgM Distal, symmetric, chronic demyelinating peripheral neuropathy, Type 2 cryoglobulinemia characterized by vasculitis affecting small vessels of skin, kidneys, liver, and peripheral nerves, Extravascular chronic hemolytic anemia called cold agglutinin disease exacerbated by cold exposure, glomerulonephritis, paraneoplastic pemphigus, and retinitis/retinopathy.

Common Symptoms

Common symptoms of Waldenström macroglobulinemia include:[79][123]

  • Constitutional B symptoms as seen in other types of NHL:
    • Weakness (due to normocytic anemia associated with IgM binding to RBCs).
    • Anorexia.
    • Unexplained weight loss.
    • Unexplained fever.
    • Heavy sweating, especially at night causing drenching of one's cloths and bedsheet.
    • Severe/extensive skin itchiness.
  • Fatigue.
  • Sensorimotor peripheral neuropathy (mostly associated with numbness and tingling, i.e. painful pins and needle sensation, of the fingers or toes).
  • Blurry vision or blind spots.
  • Abdominal pain.

Less Common Symptoms

Less common symptoms of Waldenström macroglobulinemia include:[79][123]

  • Enlarged lymph nodes (appearing as 1-2 inches sized lumps under the skin in neck, groin or the armpits).
  • Swollen belly/abdomen (due to hepatosplenomegaly).
  • Pain or a feeling of fullness below the ribs on the left side.
  • Painless lumps in the neck, underarm, stomach, or groin
  • Headache.
  • Raised pink/flesh-colored lesions on skin.
  • Altered mental status due to decreased blood flow and infiltration of CNS leading to:
  • Symptoms resembling stroke like slurred speech or weakness on one side of body (such patients are advised to consult from their doctor right away).
  • Abnormal mucous membrane bleeding (epistaxis, bleeding gums).
  • Vision problems (blurred vision, double vision or blind spots).
  • Kidney problems (leading to weakness, trouble breathing and fluid buildup in body tissues associated with accumulation of excess salt, fluid and waste products in blood secondary to amyloidosis).
  • Heart problems (Secondary to amyloidosis, build up of M protein in heart affects its pumping ability, and also the heart has to work harder to pump the thick blood ultimately leading to CHF with following symptoms).
    • Palpitations.
    • Feeling of tiredness and weakness.
    • Cough.
    • Shortness of breath.
    • Rapid weight gain.
    • Swelling of feet and legs.
  • Infections (high levels of abnormal antibody in WM slows down the production of normal antibodies).
  • Digestive problems due to deposition of IgM protein in the lamina propria of the intestinal wall include:
    • Diarrhea.
    • Poor absorption of vitamins.
    • GIT bleeding/steatorrhea (blood in stools/dark stools).
  • Sensitivity to cold (Raynaud's phenomenon due to cryoglobulinemia in 5% WM patients), which is associated with reduced blood flow leading to pain, itching, bluish discoloration or sores in following body parts:
    • Tip of nose.
    • Ears.
    • Fingers.
    • Toes.
  • Cryoglobulinemia also leads to:
    • Numbness and tingling in hands and feet.
    • Joint aches.
    • Small bruises.
    • Skin ulcers.

Symptoms Secondary to Hyperviscosity Syndrome

The lymphoma cells make varying amounts of a monoclonal protein called immunoglobulin M (IgM, or macroglobulin). Higher amounts of this protein than normal in blood tends to make it thick leading to hyperviscosity syndrome which occurs in approximately 15-20% patients of WM. When blood becomes thick, it is harder for blood to flow through small blood vessels, and when this occurs, the condition is termed as Waldenstrom macroglobulinemia. This excess amount of IgM antibodies can be ultimately associated with circulatory problems leading to less blood flow to the brain, the eyes or other organs.Clinical manifestations of hyperviscosity syndrome occur only if serum viscosity is >4 centipoises and include:[79]

Physical Examination

General Appearance

Patients with Waldenström macroglobulinemia are generally well-appearing.[36]

Skin

HEENT

  • Pallor.
  • Papilledema.
  • Malignant vitreitis.[111]
  • Congestion/sludging of blood in conjunctival vessels.
  • Retinitis/retinopathy including dilation, segmentation and tortuosity of retinal vessels, mid-peripheral retinal hemorrhages, serous retinal/macular neurosensory detachment, blurred disc margins and fundal exudates on fundoscopic examination.[124][125][126]

Neck

Respiratory

Cardiovascular system

Abdomen

Extremity

Neuromuscular

Laboratory Findings

WM is mostly suspected when a patient has low blood counts and/or high levels of unusual protein levels on blood tests. Then usually after that, a blood test called serum protein electrophoresis is ordered to find out what type of protein is there. And mostly, only after these tests are done that a biopsy of either the bone marrow or a lymph node is considered to confirm the WM diagnosis. Laboratory findings consistent with the diagnosis of Waldenström macroglobulinemia include:[79]

Bone Marrow Aspirate

A bone marrow aspirate is essential in the diagnosis of Waldenström macroglobulinemia.

Findings suggestive of Waldenström macroglobulinemia include:[131]

  • A hypercellular bone marrow aspirate.
  • Lymphoplasmacytic infiltrate with characteristic immunophenotype.

Bone Marrow Biopsy

A bone marrow biopsy may be helpful in the diagnosis of Waldenström macroglobulinemia. [131]

Findings on the biopsy suggestive of Waldenström macroglobulinemia include:[131]

  • Dutcher bodies (PAS positive intra-nuclear vacuoles containing IgM monoclonal protein).
    • Characteristic feature of Waldenström macroglobulinemia.

Three patterns of marrow involvement are described, as follows:

  • Lymphoplasmacytoid cells (lymphoplasmacytic and small lymphocytes) in a nodular pattern.
  • Lymphoplasmacytic cells (small lymphocytes, mature plasma cells, mast cells) in an interstitial/nodular pattern.
  • A polymorphous infiltrate (small lymphocytes, plasma cells, plasmacytoid cells, immunoblasts with mitotic figures).

Electrophoresis and Immunofixation

Serum protein electrophoresis is important for the diagnosis of Waldenström's macroglobulinemia.

Findings on an electrophoresis diagnostic of Waldenström's macroglobulinemia include:[132]

  • Sharp, narrow spike of monoclonal IgM protein
  • Dense band of monoclonal IgM protein
  • The paraprotein can be of any size

Serum immunofixation is important for the diagnosis of Waldenström's macroglobulinemia. It helps in confirming the presence of a monoclonal protein, in addition to determining its type.[132]

Electrocardiogram

There are no ECG findings associated with Waldenström macroglobulinemia.

X-ray

Key Chest X-Ray Findings in Waldenström's Macroglobulinemia:

  • Chest x-ray may be used to evaluate the following:[133]
    • Enlarged lymph nodes.
    • Pulmonary infiltrates: This is especially important in patients who are immunocompromised while receiving chemotherapy.
    • Nodules.
    • Effusion.
    • Cardiomegaly (due to Congestive heart failure).

Echocardiography or Ultrasound

There are no echocardiography and ultrasound findings associated with Waldenström's macroglobulinemia. However, ultrasound of the spleen is more accurate at quantitation compared to physical examination findings alone. Ultrasound can be used to look at lymph nodes near body surface or to look for enlarged abdominal lymph nodes or organs such as the liver, spleen, and kidneys. (It can’t be used to look at organs or lymph nodes in the chest because the ribs block the sound waves.) It is sometimes used to help guide a biopsy needle into an enlarged lymph node.

CT scan

  • CT scan imaging of chest, abdomen, and pelvis can be done to measure the tumor load.[134]
  • Waldenström's macroglobulinemia shows evidence of lymphadenopathy, and hepatosplenomegaly.[134]
  • CT of the lungs or abdomen can also be diagnostic for infection, which is particularly relevant to immunocompromised patients.

MRI

There are no specific MRI findings associated with Waldenström macroglobulinemia. However, MRI of the brain, spinal cord and orbits is important when assessing for hyperviscosity in the presence of high IgM paraprotein in the blood.

PET scan

A PET scan can be helpful in spotting small collections of cancer cells. It is even more valuable when combined with a CT scan (PET/CT scan). PET scans also can help tell if an enlarged lymph node contains lymphoma or not. It can help spot small areas that might be lymphoma, even if the area looks normal on a CT scan. These tests can be used to tell if a lymphoma is responding to treatment. They can also be used after treatment to help decide whether an enlarged lymph node still contains lymphoma or is merely scar tissue.

Other Diagnostic Studies

Other diagnostic studies for Waldenström macroglobulinemia include:

  • Nerve conduction study and electromyography, which demonstrates:[135]
  • Fundoscopy, which demonstrates:[136]
  • Plasma viscosity, which demonstrates:[137]
    • Values > 1.5 centipoise
      • Should be measured in patients presenting with signs and symptoms suggestive of hyperviscosity syndrome or whenever the monoclonal IgM protein spike is > 4 g/dL.
  • Mutational analysis for the MYD88 gene, since the MYD88 L265P mutation is found in 90% of patients with Waldenstrom's macroglobulinemia[130]

Treatment

There are several different options for treating Waldenström macroglobulinemia depending on stage of the disease:[138]

Asymptomatic/Smoldering Waldenström's Macroglobulinemia

There is no treatment for asymptomatic Waldenström macroglobulinemia. Asymptomatic waldenström's macroglobulinemia can be monitored every 3-6 months.[139] Active surveillance includes monitoring of the following laboratory parameters:

  • Complete blood count (CBC) with differential
  • Complete metabolic panel (CMP)
  • Immunoglobulin levels in the serum (quantitative)
  • Serum protein electrophoresis

Symptomatic Waldenström's Macroglobulinemia

Symptomatic patients with waldenström macroglobulinemia are started on chemotherapy depending on the stage.[140]

  • Initial stage of waldenström's macroglobulinemia associated with:
  • Late stage of Waldenström's macroglobulinemia associated with:
Treatment Regimen[140]

Drugs Side effects

CHOP-R regimen

Ibrutinib

Rituximab

  • Infusion related reaction
  • Hepatitis B reaction
  • Progressive multi-focal leukoencephaloptahy

FR regimen

BDR regimen

DRC regimen

CR regimen

IR regimen

Hyperviscosity syndrome

  • Waldenström macroglobulinemia complicated with hyperviscosity syndrome is a medical emergency and requires prompt treatment with plasmapheresis.[140]
  • Plasmapheresis temporarily lowers IgM levels by removing some of the abnormal IgM from the blood, which makes blood thinner.
  • Plasmapheresis is usually given until chemotherapy starts to work.
  • Plasmapheresis is combined with chemotherapy to control the disease for a longer period of time.

Surgery

Stem cell transplant is usually reserved for patients with either relapse or refractory Waldenström's macroglobulinemia.[141]

Primary Prevention

Primary prevention of Waldenström macroglobulinemia depends on the type of risk factor causing the disease.[142]

Modifiable risk factors

Non-modifiable risk factors

Secondary Prevention

There are no established measures for the secondary prevention of Waldenström's macroglobulinemia.

One or more of the following treatments can be given for lymphoplasmacytic lymphoma.

Watchful waiting

Watchful waiting (also called active surveillance) may be offered for lymphoplasmacytic lymphoma because it develops slowly and may not need to be treated right away. The healthcare team will carefully monitor the person with lymphoplasmacytic lymphoma and start treatment when symptoms appear, such as hyperviscosity syndrome, or there are signs that the disease is progressing more quickly.

Chemotherapy

  • People with lymphoplasmacytic lymphoma who have symptoms or hyperviscosity syndrome are usually given chemotherapy. Chemotherapy drugs that may be used with or without prednisone include:
    • Chlorambucil (Leukeran)
    • Fludarabine (Fludara)
    • Bendamustine (Treanda)
    • Cyclophosphamide (Cytoxan, Procytox)
  • Combinations of chemotherapy drugs that may be used include:
    • DRC – dexamethasone (Decadron, Dexasone), rituximab (Rituxan) and cyclophosphamide
    • BRD – bortezomib (Velcade) and rituximab, with or without dexamethasone
    • CVP – cyclophosphamide, vincristine (Oncovin) and prednisone
    • R-CVP – CVP with rituximab
    • Thalidomide (Thalomid) and rituximab

Targeted therapy

  • Targeted therapy uses drugs to target specific molecules (such as proteins) on the surface of cancer cells. These molecules help send signals that tell cells to grow or divide. By targeting these molecules, the drugs stop the growth and spread of cancer cells while limiting harm to normal cells.
  • Targeted therapy drugs used alone or in combination to treat lymphoplasmacytic lymphoma include rituximab, bortezomib and ibrutinib (Imbruvica).

Immunotherapy

  • Immunotherapy works by stimulating, boosting, restoring or acting like the body’s immune system to create a response against cancer cells. Immunomodulatory drugs are a type of immunotherapy that interferes with the growth and division of cancer cells.
  • Thalidomide is a type of immunomodulatory drug that may be used to treat lymphoplasmacytic lymphoma.

Radiation therapy

External beam radiation therapy may be used to treat lymphoplasmacytic lymphoma that develops outside of the lymphatic system (called extralymphatic disease), but this is rare.

Stem cell transplant

  • Some people with lymphoplasmacytic lymphoma may be offered a stem cell transplant.
  • It may be used if the lymphoma comes back (recurs) after treatment or doesn’t respond to other treatments (called refractory disease).
  • Many people with lymphoplasmacytic lymphoma are older or may not be in good health, so a stem cell transplant may not be a good treatment option for them.


Read more: http://www.cancer.ca/en/cancer-information/cancer-type/non-hodgkin-lymphoma/non-hodgkin-lymphoma/more-types-of-nhl/lymphoplasmacytic-lymphoma/?region=on#ixzz5eb6iT7G6

References

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  49. ↑ Zachary R. Hunter, Lian Xu, Guang Yang, Yangsheng Zhou, Xia Liu, Yang Cao, Robert J. Manning, Christina Tripsas, Christopher J. Patterson, Patricia Sheehy & Steven P. Treon (2014). "The genomic landscape of Waldenstrom macroglobulinemia is characterized by highly recurring MYD88 and WHIM-like CXCR4 mutations, and small somatic deletions associated with B-cell lymphomagenesis". Blood. 123 (11): 1637–1646. doi:10.1182/blood-2013-09-525808. PMID 24366360. Unknown parameter |month= ignored (help)
  50. ↑ Roelandt F. J. Schop, W. Michael Kuehl, Scott A. Van Wier, Gregory J. Ahmann, Tammy Price-Troska, Richard J. Bailey, Syed M. Jalal, Ying Qi, Robert A. Kyle, Philip R. Greipp & Rafael Fonseca (2002). "Waldenstrom macroglobulinemia neoplastic cells lack immunoglobulin heavy chain locus translocations but have frequent 6q deletions". Blood. 100 (8): 2996–3001. doi:10.1182/blood.V100.8.2996. PMID 12351413. Unknown parameter |month= ignored (help)
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    • Bone marrow infiltration of small, cleaved cells that are usually paratrabecular
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  67. ↑ Harris NL, Jaffe ES, Stein H, Banks PM, Chan JK, Cleary ML, Delsol G, De Wolf-Peeters C, Falini B, Gatter KC (1994). "A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group". Blood. 84 (5): 1361–92. PMID 8068936.
  68. ↑ 68.0 68.1 68.2 68.3 68.4 Wang H, Chen Y, Li F, Delasalle K, Wang J, Alexanian R; et al. (2012). "Temporal and geographic variations of Waldenstrom macroglobulinemia incidence: a large population-based study". Cancer. 118 (15): 3793–800. doi:10.1002/cncr.26627. PMID 22139816.
  69. ↑ 69.0 69.1 Groves FD, Travis LB, Devesa SS, Ries LA, Fraumeni JF (1998). "Waldenström's macroglobulinemia: incidence patterns in the United States, 1988-1994". Cancer. 82 (6): 1078–81. PMID 9506352.
  70. ↑ 70.0 70.1 70.2 70.3 Herrinton LJ, Weiss NS (1993). "Incidence of Waldenström's macroglobulinemia". Blood. 82 (10): 3148–50. PMID 8219203.
  71. ↑ Monge J, Braggio E, Ansell SM (2013). "Genetic factors and pathogenesis of Waldenström's macroglobulinemia". Curr Oncol Rep. 15 (5): 450–6. doi:10.1007/s11912-013-0331-7. PMC 3807757. PMID 23901022.
  72. ↑ 72.0 72.1 72.2 72.3 Kyle, Robert A.; Larson, Dirk R.; McPhail, Ellen D.; Therneau, Terry M.; Dispenzieri, Angela; Kumar, Shaji; Kapoor, Prashant; Cerhan, James R.; Rajkumar, S. Vincent (2018). "Fifty-Year Incidence of Waldenström Macroglobulinemia in Olmsted County, Minnesota, From 1961 Through 2010: A Population-Based Study With Complete Case Capture and Hematopathologic Review". Mayo Clinic Proceedings. 93 (6): 739–746. doi:10.1016/j.mayocp.2018.02.011. ISSN 0025-6196.
  73. ↑ 73.0 73.1 Waldenström's macroglobulinemia. American Cancer Society (2015)http://www.cancer.org/cancer/waldenstrommacroglobulinemia/detailedguide/waldenstrom-macroglobulinemia-risk-factors Accessed on November 6, 2015
  74. ↑ Giordano TP, Henderson L, Landgren O, Chiao EY, Kramer JR, El-Serag H; et al. (2007). "Risk of non-Hodgkin lymphoma and lymphoproliferative precursor diseases in US veterans with hepatitis C virus". JAMA. 297 (18): 2010–7. doi:10.1001/jama.297.18.2010. PMID 17488966.
  75. ↑ Morton LM, Wang SS, Devesa SS, Hartge P, Weisenburger DD, Linet MS (2006). "Lymphoma incidence patterns by WHO subtype in the United States, 1992-2001". Blood. 107 (1): 265–76. doi:10.1182/blood-2005-06-2508. PMC 1895348. PMID 16150940.
  76. ↑ Pophali, Priyanka Avinash; Bartley, Adam C.; Kapoor, Prashant; Gonsalves, Wilson I.; Ashrani, Aneel A.; Marshall, Ariela L.; Siddiqui, Mustaqeem Ahmad; Go, Ronald S. (2017). "Smoldering Waldenström's macroglobulinemia (SWM): Analysis from the National Cancer Database (NCDB)". Journal of Clinical Oncology. 35 (15_suppl): 1573–1573. doi:10.1200/JCO.2017.35.15_suppl.1573. ISSN 0732-183X.
  77. ↑ McMaster ML, Csako G, Giambarresi TR, Vasquez L, Berg M, Saddlemire S; et al. (2007). "Long-term evaluation of three multiple-case Waldenstrom macroglobulinemia families". Clin Cancer Res. 13 (17): 5063–9. doi:10.1158/1078-0432.CCR-07-0299. PMID 17785558.
  78. ↑ Recommendations. US preventive services task force(2015) http://www.uspreventiveservicestaskforce.org/BrowseRec/Search?s=waldenstrom+macroglobulinemia Accessed on November 10, 2015
  79. ↑ 79.0 79.1 79.2 79.3 79.4 79.5 79.6 García-Sanz R, Montoto S, Torrequebrada A, de Coca AG, Petit J, Sureda A; et al. (2001). "Waldenström macroglobulinaemia: presenting features and outcome in a series with 217 cases". Br J Haematol. 115 (3): 575–82. PMID 11736938.
  80. ↑ Michael AB, Lawes M, Kamalarajan M, Huissoon A, Pratt G (2004). "Cryoglobulinaemia as an acute presentation of Waldenstrom's macroglobulinaemia". Br J Haematol. 124 (5): 565. PMID 14871241.
  81. ↑ Levine T, Pestronk A, Florence J, Al-Lozi MT, Lopate G, Miller T; et al. (2006). "Peripheral neuropathies in Waldenström's macroglobulinaemia". J Neurol Neurosurg Psychiatry. 77 (2): 224–8. doi:10.1136/jnnp.2005.071175. PMC 2077569. PMID 16421127.
  82. ↑ Zimmermann I, Gloor HJ, Rüttimann S (2001). "[General AL-amyloidosis: a rare complication in Waldenstrom macroglobulinemia]". Praxis (Bern 1994) (in German). 90 (47): 2050–5. PMID 11763619.
  83. ↑ Owen RG, Pratt G, Auer RL, Flatley R, Kyriakou C, Lunn MP; et al. (2014). "Guidelines on the diagnosis and management of Waldenström macroglobulinaemia". Br J Haematol. 165 (3): 316–33. doi:10.1111/bjh.12760. PMID 24528152.
  84. ↑ Veloso FT, Fraga J, Saleiro JV (1988). "Macroglobulinemia and small intestinal disease. A case report with review of the literature". J Clin Gastroenterol. 10 (5): 546–50. PMID 3141496.
  85. ↑ Vos JM, Gustine J, Rennke HG, Hunter Z, Manning RJ, Dubeau TE; et al. (2016). "Renal disease related to Waldenström macroglobulinaemia: incidence, pathology and clinical outcomes". Br J Haematol. 175 (4): 623–630. doi:10.1111/bjh.14279. PMID 27468978.
  86. ↑ 86.0 86.1 Civit T, Coulbois S, Baylac F, Taillandier L, Auque J (1997). "[Waldenström's macroglobulinemia and cerebral lymphoplasmocytic proliferation: Bing and Neel syndrome. Apropos of a new case]". Neurochirurgie. 43 (4): 245–9. PMID 9686227.
  87. ↑ Fintelmann F, Forghani R, Schaefer PW, Hochberg EP, Hochberg FH (2009). "Bing-Neel Syndrome revisited". Clin Lymphoma Myeloma. 9 (1): 104–6. doi:10.3816/CLM.2009.n.028. PMID 19362988.
  88. ↑ Grewal JS, Brar PK, Sahijdak WM, Tworek JA, Chottiner EG (2009). "Bing-Neel syndrome: a case report and systematic review of clinical manifestations, diagnosis, and treatment options". Clin Lymphoma Myeloma. 9 (6): 462–6. doi:10.3816/CLM.2009.n.091. PMID 19951888.
  89. ↑ 89.0 89.1 89.2 Ghobrial IM, Fonseca R, Gertz MA, Plevak MF, Larson DR, Therneau TM; et al. (2006). "Prognostic model for disease-specific and overall mortality in newly diagnosed symptomatic patients with Waldenstrom macroglobulinaemia". Br J Haematol. 133 (2): 158–64. doi:10.1111/j.1365-2141.2006.06003.x. PMID 16611306.
  90. ↑ Morel, P.; Duhamel, A.; Gobbi, P.; Dimopoulos, M. A.; Dhodapkar, M. V.; McCoy, J.; Crowley, J.; Ocio, E. M.; Garcia-Sanz, R.; Treon, S. P.; Leblond, V.; Kyle, R. A.; Barlogie, B.; Merlini, G. (2009). "International prognostic scoring system for Waldenstrom macroglobulinemia". Blood. 113 (18): 4163–4170. doi:10.1182/blood-2008-08-174961. ISSN 0006-4971.
  91. ↑ Kyle RA, Greipp PR, Gertz MA, Witzig TE, Lust JA, Lacy MQ; et al. (2000). "Waldenström's macroglobulinaemia: a prospective study comparing daily with intermittent oral chlorambucil". Br J Haematol. 108 (4): 737–42. PMID 10792277.
  92. ↑ Gobbi PG, Baldini L, Broglia C, Goldaniga M, Comelli M, Morel P; et al. (2005). "Prognostic validation of the international classification of immunoglobulin M gammopathies: a survival advantage for patients with immunoglobulin M monoclonal gammopathy of undetermined significance?". Clin Cancer Res. 11 (5): 1786–90. doi:10.1158/1078-0432.CCR-04-1899. PMID 15756000.
  93. ↑ Dimopoulos MA, Hamilos G, Zervas K, Symeonidis A, Kouvatseas G, Roussou P; et al. (2003). "Survival and prognostic factors after initiation of treatment in Waldenstrom's macroglobulinemia". Ann Oncol. 14 (8): 1299–305. PMID 12881396.
  94. ↑ Leleu X, Moreau AS, Weller E, Roccaro AM, Coiteux V, Manning R; et al. (2008). "Serum immunoglobulin free light chain correlates with tumor burden markers in Waldenstrom macroglobulinemia". Leuk Lymphoma. 49 (6): 1104–7. doi:10.1080/10428190802074619. PMID 18452095.
  95. ↑ Kastritis E, Zervas K, Repoussis P, Michali E, Katodrytou E, Zomas A; et al. (2009). "Prognostication in young and old patients with Waldenström's macroglobulinemia: importance of the International Prognostic Scoring System and of serum lactate dehydrogenase". Clin Lymphoma Myeloma. 9 (1): 50–2. doi:10.3816/CLM.2009.n.012. PMID 19362972.
  96. ↑ Ho AW, Hatjiharissi E, Ciccarelli BT, Branagan AR, Hunter ZR, Leleu X; et al. (2008). "CD27-CD70 interactions in the pathogenesis of Waldenstrom macroglobulinemia". Blood. 112 (12): 4683–9. doi:10.1182/blood-2007-04-084525. PMC 2597134. PMID 18216294.
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  98. ↑ Swerdlow SH, Campo E, Pileri SA, Harris NL, Stein H, Siebert R; et al. (2016). "The 2016 revision of the World Health Organization classification of lymphoid neoplasms". Blood. 127 (20): 2375–90. doi:10.1182/blood-2016-01-643569. PMC 4874220. PMID 26980727.
  99. ↑ Remstein ED, Hanson CA, Kyle RA, Hodnefield JM, Kurtin PJ (2003). "Despite apparent morphologic and immunophenotypic heterogeneity, Waldenstrom's macroglobulinemia is consistently composed of cells along a morphologic continuum of small lymphocytes, plasmacytoid lymphocytes, and plasma cells". Semin Oncol. 30 (2): 182–6. doi:10.1053/sonc.2003.50073. PMID 12720133.
  100. ↑ San Miguel JF, Vidriales MB, Ocio E, Mateo G, Sánchez-Guijo F, Sánchez ML; et al. (2003). "Immunophenotypic analysis of Waldenstrom's macroglobulinemia". Semin Oncol. 30 (2): 187–95. doi:10.1053/sonc.2003.50074. PMID 12720134.
  101. ↑ Konoplev S, Medeiros LJ, Bueso-Ramos CE, Jorgensen JL, Lin P (2005). "Immunophenotypic profile of lymphoplasmacytic lymphoma/Waldenström macroglobulinemia". Am J Clin Pathol. 124 (3): 414–20. doi:10.1309/3G1X-DX0D-VHBN-VKB4. PMID 16191510.
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  103. ↑ 103.0 103.1 Dimopoulos, Meletios A.; Panayiotidis, Panayiotis; Moulopoulos, Lia A.; Sfikakis, Petros; Dalakas, Marinos (2000). "Waldenström's Macroglobulinemia: Clinical Features, Complications, and Management". Journal of Clinical Oncology. 18 (1): 214–214. doi:10.1200/JCO.2000.18.1.214. ISSN 0732-183X.
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  110. ↑ 110.0 110.1 110.2 Daoud MS, Lust JA, Kyle RA, Pittelkow MR (1999). "Monoclonal gammopathies and associated skin disorders". J Am Acad Dermatol. 40 (4): 507–35, quiz 536-8. PMID 10188670.
  111. ↑ 111.0 111.1 Orellana J, Friedman AH (1981). "Ocular manifestations of multiple myeloma, Waldenström's macroglobulinemia and benign monoclonal gammopathy". Surv Ophthalmol. 26 (3): 157–69. PMID 6801795.
  112. ↑ Kwaan HC, Bongu A (1999). "The hyperviscosity syndromes". Semin Thromb Hemost. 25 (2): 199–208. doi:10.1055/s-2007-994921. PMID 10357087.
  113. ↑ Farhangi M, Merlini G (1986). "The clinical implications of monoclonal immunoglobulins". Semin Oncol. 13 (3): 366–79. PMID 3094151.
  114. ↑ "Case records of the Massachusetts General Hospital. Weekly clinicopathological exercises. Case 3-1990. A 66-year-old woman with Waldenström's macroglobulinemia, diarrhea, anemia, and persistent gastrointestinal bleeding". N Engl J Med. 322 (3): 183–92. 1990. doi:10.1056/NEJM199001183220308. PMID 2104668.
  115. ↑ Gertz, M A; Kyle, R A; Noel, P (1993). "Primary systemic amyloidosis: a rare complication of immunoglobulin M monoclonal gammopathies and Waldenström's macroglobulinemia". Journal of Clinical Oncology. 11 (5): 914–920. doi:10.1200/JCO.1993.11.5.914. ISSN 0732-183X.
  116. ↑ Gertz MA, Kyle RA (2003). "Amyloidosis with IgM monoclonal gammopathies". Semin Oncol. 30 (2): 325–8. doi:10.1053/sonc.2003.50060. PMID 12720162.
  117. ↑ Gardyn J, Schwartz A, Gal R, Lewinski U, Kristt D, Cohen AM (2001). "Waldenström's macroglobulinemia associated with AA amyloidosis". Int J Hematol. 74 (1): 76–8. PMID 11530809.
  118. ↑ Ropper AH, Gorson KC (1998). "Neuropathies associated with paraproteinemia". N Engl J Med. 338 (22): 1601–7. doi:10.1056/NEJM199805283382207. PMID 9603799.
  119. ↑ Vital A (2001). "Paraproteinemic neuropathies". Brain Pathol. 11 (4): 399–407. PMID 11556684.
  120. ↑ Crisp D, Pruzanski W (1982). "B-cell neoplasms with homogeneous cold-reacting antibodies (cold agglutinins)". Am J Med. 72 (6): 915–22. PMID 6807086.
  121. ↑ Lindström FD, Hed J, Eneström S (1980). "Renal pathology of Waldenström's macroglobulinaemia with monoclonal antiglomerular antibodies and nephrotic syndrome". Clin Exp Immunol. 41 (2): 196–204. PMC 1537007. PMID 6777101.
  122. ↑ Sen HN, Chan CC, Caruso RC, Fariss RN, Nussenblatt RB, Buggage RR (2004). "Waldenström's macroglobulinemia-associated retinopathy". Ophthalmology. 111 (3): 535–9. doi:10.1016/j.ophtha.2003.05.036. PMID 15019332.
  123. ↑ 123.0 123.1 Merlini G, Baldini L, Broglia C, Comelli M, Goldaniga M, Palladini G; et al. (2003). "Prognostic factors in symptomatic Waldenstrom's macroglobulinemia". Semin Oncol. 30 (2): 211–5. doi:10.1053/sonc.2003.50064. PMID 12720138.
  124. ↑ Pilon AF, Rhee PS, Messner LV (2005). "Bilateral, persistent serous macular detachments with Waldenström's macroglobulinemia". Optom Vis Sci. 82 (7): 573–8. PMID 16044069.
  125. ↑ Avashia JH, Fath DF (1989). "Bilateral central retinal vein occlusion in Waldenström's macroglobulinemia". J Am Optom Assoc. 60 (9): 657–8. PMID 2507620.
  126. ↑ Goen TM, Terry JE (1986). "Mid-peripheral hemorrhages secondary to Waldenström's macroglobulinemia". J Am Optom Assoc. 57 (2): 109–12. PMID 3081619.
  127. ↑ Coimbra J, Costa AP, Pita F, Rosado P, de Almeida LB (1995). "[Neuropathy in Waldenstrom's macroglobulinemia]". Acta Med Port (in Portuguese). 8 (4): 253–7. PMID 7625222.
  128. ↑ Katzmann JA, Kyle RA, Benson J, Larson DR, Snyder MR, Lust JA; et al. (2009). "Screening panels for detection of monoclonal gammopathies". Clin Chem. 55 (8): 1517–22. doi:10.1373/clinchem.2009.126664. PMC 3773468. PMID 19520758.
  129. ↑ Penny R, Castaldi PA, Whitsed HM (1971). "Inflammation and haemostasis in paraproteinaemias". Br J Haematol. 20 (1): 35–44. PMID 4924493.
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  133. ↑ Rausch PG, Herion JC (1980). "Pulmonary manifestations of Waldenstrom macroglobulinemia". Am. J. Hematol. 9 (2): 201–9. PMID 6776807.
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  138. ↑ Lymphoplasmacytic lymphoma. Canadian Cancer Society 2015. http://www.cancer.ca/en/cancer-information/cancer-type/non-hodgkin-lymphoma/non-hodgkin-lymphoma/types-of-nhl/lymphoplasmacytic-lymphoma/?region=ab Accessed on November 6 2015
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  142. ↑ Waldenström's macroglobulinemia. American Cancer Society. (2015)http://www.cancer.org/cancer/waldenstrommacroglobulinemia/detailedguide/waldenstrom-macroglobulinemia-prevention Accessed on November 11, 2015
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