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SOHO State of the Art Updates and Next Questions |Treatment Approaches for Nodular Lymphocyte-Predominant Hodgkin Lymp…
Clinical Lymphoma Myeloma and Leukemia
Volume 23, Issue 7, July 2023, Pages 471-476
Review Article
SOHO State of the Art Updates and Next Questions |Treatment Approaches for Nodular
Lymphocyte-Predominant Hodgkin Lymphoma
Michael S. Binkley 1
, Ranjana H. Advani 2
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https://doi.org/10.1016/j.clml.2023.03.014 ↗
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Abstract
Nodular lymphocyte-predominant Hodgkin lymphoma (NLPHL) is a rare variant of Hodgkin lymphoma characterized by a persistent risk of
relapse but an excellent overall survival. Historically, it was treated similarly to classic Hodgkin lymphoma, but efforts have been made to
deintensify treatment due to risk of late toxicity associated with intensive therapy. For patients with completely resected stage IA NLPHL, no
further treatment may be considered, particularly for pediatric patients. For those with stage I-II NLPHL without risk factors such as B
symptoms, sites>2, or variant pattern histology, lower intensity treatment with radiotherapy or chemotherapy alone may be sufficient.
However, combined modality therapy is a standard treatment for favorable and unfavorable risk stage I-II NLPHL associated with excellent
progression-free and overall survival rates. For patients with advanced stage NLPHL, the optimal chemotherapy is not defined, but R-CHOP
appears to be an effective treatment. Efforts to study NLPHL through multicenter collaborative efforts are crucial to develop evidence based
and individualized treatments for patients with NLPHL.
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Keyword
Management; Hodgkin lymphoma; Adolescents; Young adults
Introduction
Nodular lymphocyte-predominant lymphoma (NLPHL) is a rare subtype of Hodgkin lymphoma representing approximately 5% of newly
diagnosed cases.1 Age of incidence is similar to that of classic Hodgkin lymphoma (cHL) with a peak occurring in the fourth decade of life.2
NLPHL has a male predominance, is diagnosed at early stages in approximately 75% of cases, and rarely is bulky or involves the mediastinum
as shown in Figure 1A.3,4 Many years after its recognition as a distinct subtype of Hodgkin lymphoma, NLPHL was reported to have a distinct
clinical course from cHL characterized by late relapses but an overall indolent course with excellent survival.5 Given its excellent prognosis
and young age of diagnosis, significant efforts have been made to deintensify treatment to limit late therapy related effects for patients.6, 7, 8
Due to its rarity, most large studies guiding management are retrospective.2,3
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Figure 1. Pathologic factors for NLPHL. Panel A demonstrates the anatomic sites most commonly involved for patients diagnosed with NLPHL.4
Panel B shows an excisional biopsy specimen with a focus of variant pattern D emphasizing the importance of characterizing the full extent of
the involved site.
Diagnosis
Workup for NLPHL is similar to that of cHL, and given the importance of assessing the immunoarchitectural patterns, excisional biopsy is
essential when at all possible.9,10 As shown in Figure 1B, a core needle biopsy may likely not capture representation of all of the
immunoarchitectural patterns present which can exist as small foci. NLPHL is avid on PET-CT similar to cHL, and therefore, bone marrow
biopsy should only be considered for patients with cytopenias, B symptoms, or if having focally avid skeletal lesions.11
Pathology
The malignant lymphocyte predominant cell (LP cell), is of B-cell origin and retains its B-cell receptor with expression of B-cell proteins
(CD19/20/79).9 However, there are very rare cases of NLPHL with LP cells negative for expression of CD20.12 Similar to cHL, the LP cell
represents approximately 1 out of every 100 cells and is surrounded by a vast abundance of immune cells.9 Characterization of the
microenvironment resulted in 6 immunoarchitectural patterns being described, A through F.13 Patterns A to D have nodularity and the diffuse
patterns E and F require at least a focus of nodularity to retain a diagnosis of NLPHL versus T-cell/Histiocyte-rich large B-cell lymphoma
(THRLBCL).9 Patients with variant pattern C to E more frequently present with advanced stage and bone marrow involvement.14, 15, 16 Several
studies have reported a worse prognosis for patients with variant patterns C through F in both pediatric and adult patients, but the number of
patients with pattern F in reported cohorts remains very few if any.3,17, 18, 19, 20 As many patients have multiple immunoarchitectural
patterns present (see Figure 1B as an example), and as no studies have thoroughly evaluated whether increasing percentages of variant
patterns portend a worse prognosis, the presence of any minor percentage of variant pattern is typically interpreted as variant pattern NLPHL.
Due to the rarity of the LP cells amidst a vast abundance of immune cells and the nonspecific CD20 positivity, genetic sequencing of NLPHL
remains very challenging to date. Genotyping efforts have demonstrated overlap of the observed somatic mutations seen for variant NLPHL
and THRLBCL, while mutations in immune surveillance pathways for typical NLPHL are similar to those observed for cHL.21 Although there has
been large success in genotyping cHL using circulating tumor DNA isolated from patient plasma,22 similar efforts for NLPHL are lacking but a
small pediatric cohort demonstrated a lower allele frequency for 3 patients with NLPHL as compared to those with cHL, suggesting genotyping
NLPHL using ctDNA may be more challenging than cHL.23 Finally, gene expression phenotyping has shown LP cells have greater similarity to
Reed-Sternberg cells as opposed to malignant cells from other B-cell lymphomas.24
Given the existing biologic understanding, there have been 2 classifications proposed for NLPHL. The International Consensus Classification of
Mature Lymphoid Neoplasms proposed reclassifying NLPHL as nodular lymphocyte-predominant B-cell lymphoma (NLPBL).25 However, the
WHO concluded there was not enough biologic evidence to consider such a renaming currently. Additionally, the WHO recommends reporting
patterns qualitatively given the aforementioned unknown utility of reporting percentage of variant pattern present.26 The classification of
NLPHL as either a subtype of Hodgkin lymphoma or a separate B-cell lymphoma remains to be clarified with further biologic evidence, but it
should be managed as unique from cHL or other B-cell lymphomas.
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Management by Clinical Stage
We have summarized treatment options for pediatric and adult patients by clinical stage in Table 1 and as summarized below.
Table 1. Management Options by Stage and Patient Age (Pediatric≤21 Years53 and Adult≥16 Years54)
Stage
IA completely
Age
Management
Systemic Therapy
Radiotherapy
Reference
Pediatric
Observation
Appel et al.7
Adult
Consider
Binkley et al.3, Borchmann
observation
et al.8
resected
I-IIA incompletely
Pediatric
Chemotherapy +/-
resected
3 cycles CVP+/- R
Response adapted
Shankar et al.17
30 Gy
Eichenauer et al.6, Binkley
RT
Adult
Radiotherapy
et al.3
alone
I-IIB
Pediatric
Chemotherapy +/-
2cycles OEPA–2cycles
Response adapted (21-
Mauz-Korholz et al.28,
RT
COPDac +/- R
30 Gy)
Friedman et al.53
20a-30 Gy
Fuchs et al.32, Eich et al.54
Mauz-Korholz et al.28
non-contiguous
involvement
or 4 cycles
ABVE-PC
Adult
Chemotherapy +/-
4 cycles of R-CHOP
RT
or
2*-4 cycles R-ABVD
III-IV
Pediatric
Chemotherapy +/-
2cycles OEPA–4cycles
Response adapted
RT
COPDac +/- R
(25.5-30 Gy)
Adult
Chemotherapy
6 cycles R-CHOP
Fanale et al.34
Adult - low disease burden
Rituximab alone
4 doses R +/- R
Advani et al.30
maintenance
Adult - low disease burden and
Active
asymptomatic
surveillance
Borchmann et al.8
Abbreviations: ABVD = Adriamycin, bleomycin, vinblastine, dacarbazine; ABVE-PC = adriamycin, bleomycin, vincristine, etoposide, cyclophosphamide, and
prednisone; COPDAC = cyclophosphamide, oncovin, prednisone, dacarbazine; CVP = cyclophosphamide, vinblastine, prednisone; OEPA = oncovin, etoposide,
prednisone, adriamycin; R = rituximab; RT = radiotherapy.
a
*=if favorable by the German Hodgkin Study Group criteria
Stage IA Without Risk Factors Completely Excised
Following early reports of pediatric patients receiving no further treatment after surgical excision enjoying an encouraging rate of disease
control,27 there has been interest in observing patients with stage IA NLPHL without adverse risk factors following complete surgical resection
confirmed by PET-CT.28 The Children's Oncology Group conducted a prospective clinical trial investigating no further treatment for 52
pediatric patients following complete excision confirmed by postoperative PET-CT with an encouraging 5-year event-free survival of 77.1% as
shown in Figure 2A.7 In that cohort, all relapses remained early stage involving either the initial site or an adjacent site with 13 of 52 patients
ultimately relapsing.7 Large retrospective studies in adult patients offered no further treatment after surgical excision have also shown
approximately three-quarters of patients may not develop progressive lymphoma within 5 years, but the pattern of relapse differs greatly
from pediatric populations as at least half of patients go on to develop advanced stage NLPHL.3,8 Thus, caution must be used when employing
observation for adult patients after excision as there may be an opportunity to definitively treat NLPHL using low intensity techniques such as
radiotherapy alone that may be lost if choosing observation after surgical excision.
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Figure 2. Selected studies reporting outcomes for patients with NLPHL. Panel A shows outcomes for patients with Stage IA. Panel B shows
outcomes for patients with stage I to II favorable NLPHL. Panel C shows results from a single study for patients with stage I to II unfavorable
NLPHL by the German Hodgkin Study Group criteria. Panel D shows results for patients with stage III to IV NLPHL. Corresponding references
are listed in superscript. Abbreviations: PFS = progression-free survival, EFS = event-free survival, OS = overall survival, RT = radiotherapy,
CT = chemotherapy alone, CMT = combined modality therapy.
Stage IA-IIB
For stage IA incompletely excised without risk factors, radiotherapy alone using limited volumes is a standard treatment.3,6,29 As demonstrated
by a large retrospective analysis of pooled data from the German Hodgkin Study Group prospective trials from 1988 to 2009, 8-year
progression-free survival (PFS) was excellent after involved-field radiotherapy alone (91.9%) and not significantly different from extended-field
radiotherapy or combined modality therapy.6 Further shrinkage of radiotherapy volumes using involved-site radiotherapy has also shown high
rates of disease control in a cohort reported by Pinnix et al. with just over 2.5 years of patient follow up.29 Although rituximab alone achieves a
high level of clinical response, it does not offer durable disease control as shown in Figure 2A.6,30 As the majority of patients with NLPHL do not
present with mediastinal involvement (Figure 1A), many late effects associated with radiotherapy including cardiovascular toxicity and risk of
secondary breast cancer observed for cHL do not pose significant long term risks.3 Although data is emerging, patients with variant
immunoarchitectural patterns should be considered for combined modality therapy as a large retrospective study of adult patients with early
stage NLPHL demonstrated worse progress-free survival for patients with variant pattern NLPHL treated with radiotherapy alone.3
For contiguous stage I to II favorable risk NLPHL with fewer than 3 Ann Arbor sites of involvement, radiotherapy alone with a dose of 30 Gy is a
reasonable option with a 5-year PFS of 91.1% in a large multicenter retrospective study (Figure 2B).3 As an alternative treatment for patients
with stage IA to IIA limited extent of involvement (amenable for radiotherapy), investigators at University of British Columbia reported
excellent PFS (89%) for patients treated with ABVDx2 followed by a PET-directed approach with 86% receiving chemotherapy alone without
radiotherapy (Figure 2B).31 Additional benefits of combined modality therapy include the potential for lower radiotherapy dose as per the
German Hodgkin Study Group HD16 trial and shrinkage of involved nodal site decreasing radiotherapy exposure to critical organs.32,33
For patients with stage I to II unfavorable risk NLPHL with B-symptoms, a larger number of involved nodal stations, or variant pattern
histology, combined modality therapy should be considered as it has demonstrated robust disease control in a pooled analysis of prospective
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trials performed by the German Hodgkin Study Group (10-year PFS of 72.1%, Figure 2C).2
Stage III-IV
As a minority of patients present with advanced stage NLPHL, there is a paucity of robust studies to guide management decisions, particularly
for pediatric patients. Early reports of improved disease control using R-CHOP have since been validated by Fanale et al.34,35 with an
encouraging 5-year PFS of 85.7% for 16 adult patients with stage III to IV NLPHL (Figure 2D). Thus, the increased alkylating chemotherapy dose
may be beneficial for advanced stage NLPHL as compared to ABVD-based regimens.36 Finally, 84 patients enrolled on the German Hodgkin
Study Group HD18 trial (which investigated PET-adaptation of therapy) had NLPHL, and those with a negative PET-CT after 2 cycles of
escalated BEACOPP had improved 5-year PFS compared with those who had a positive scan, 90.2% vs. 70.1%, respectively.37
Less intensive options include rituximab alone for which nearly all patients obtain at least a partial response and may alleviate symptomatic
disease despite not being a definitive option.30,38 Finally, active surveillance has been suggested as a viable option in the absence of high risk
clinical features and may be employed for patients with good clinical follow up.8 Some examples of high-risk disease factors include variant
pattern histology and splenic involvement which are both associated with transformation to aggressive large cell lymphomas and may
warrant more immediate treatment.18,39 To date, the optimal approach to manage patients with stage III to IV NLPHL remains undefined.
Relapsed NLPHL
As relapses for NLPHL may occur even decades after initial diagnosis and treatment, long-term clinical follow up is important.5 At time of
relapse, a repeat excisional biopsy and PET-CT should be obtained to confirm relapse, determine burden of disease, and evaluate for
progression of variant subtype or transformation. Patients who relapse within 1-year after initial diagnosis have been reported to have a worse
prognosis.40 Management of relapse depends on the relapse stage, prior therapies given, and whether the patient has bulky disease or is
symptomatic. Reasonable approaches may include active surveillance, rituximab monotherapy, radiotherapy, combined modality therapy, and
in cases of transformation or if progressing with aggressive disease even autologous bone marrow transplantation.3,40,41
Transformed Disease
There is a small but persistent risk of developing transformation to aggressive large cell lymphomas for patients diagnosed with NLPHL.39
Transformation is associated with an increased risk of death.42 Treatment of transformed disease should include chemotherapy with or
without autologous stem cell transplantation.39,43, 44, 45 Additionally, CD19 CART trials have included patients with transformation from
NLPHL.46
Future Therapies
Given the excellent outcomes observed for early stage NLPHL, introduction of alternative regimens, novel agents, and checkpoint inhibitors
may be most appropriate for advanced stage and relapsed NLPHL. Nevertheless, alternative regimens have been reported for small cohorts.
There was a 100% response rate for a cohort of 9 patients with stages I to IV NLPHL treated with bendamustine and rituximab.47 Despite the
high PD-1 positive T-cell rosettes and PD-L1 positive LP cells,9,48 only scant clinical evidence suggests relapsed cases may respond to
checkpoint inhibition.49 Finally, given the mature B-cell phenotype of NLPHL, patients with NLPHL are included in clinical trials for B-cell
lymphomas including patients with multiply relapsed/refractory lymphoma targeting the NFKB pathway.50
Conclusion
Although NLPHL is a rare type of Hodgkin lymphoma without many dedicated clinical trials or large studies to establish firm treatment
standards, the majority of patients will enjoy high overall survival independent of treatment selection. Although late relapses do occur,
patients tend to be diagnosed at young ages and should be considered for definitive treatment options as most will not have a relapse within
10 years of diagnosis. Large international collaboration is underway within the Global nLPHL One Working Group (GLOW) and will shed
further light on appropriate risk stratification of patients based on pathologic factors and reveal age specific risks of progression to advanced
stage and transformation.51,52
Disclosure
There are no conflicts of interest to disclose.
Acknowledgments
The human body art used for Figure 1A was in part produced using Servier Medical Art (https://smart.servier.com ↗). Servier Medical Art by
Servier is licensed under a Creative Commons Attribution 3.0 Unported License (https://creativecommons.org/licenses/by/3.0/ ↗). We also
thank Dr. Yaso Natkunam for providing interpretation of the immunoarchitectural patterns displayed on Figure 1B.
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