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. 2020 Nov 18;11:594556. doi: 10.3389/fimmu.2020.594556

Table 4.

Clinical trials evaluating the efficacy and toxicity of immune checkpoint inhibitors, used as single agents or in combination regimens, for the treatment of patients with CLL.

Drug regimen Setting Efficacy Toxicities References
Pembrolizumab every 3 weeks for up to 2 years Phase II:
25 patients (9 Richter syndrome)
R/R CLL
ORR 16%
1% CR
Median PFS 3 months
Median OS 10.7 months
G≥3 neutropenia 20%
G≥3 thrombocytopenia 20%
G≥3 anemia 20%
G≥3 dyspnea 8%
G≥3 hypoxia 8%
G≥3 fatigue 8%
G≥3 febrile neutropenia 8%
G≥3 fever 4%
G≥3 maculopapular rash 4%
G3 lung infection 12%
G3 hepatic toxicity 8%
G5 sepsis 4%
Ding et al. (285)
NCT02332980
Nivolumab 3 mg/kg IV every 2 weeks and ibrutinib 420 mg/day Phase II
8 patients (4 Richter sydrome)
R/R CLL vs 3 patients PR CLL to 9-month ibrutinib therapy
ORR 75%
50% PR
vs
ORR 100%
100% PR
No G≥3 AEs Jain et al. (286)
NCT02420912
Pidilizumab Phase I
3 patients
R/R CLL
ORR 0
67% SD
No G≥3 AEs Berger et al. (287)
Samalizumab once every 28 days until progression or toxicity Phase I
23 patients
R/R CLL
ORR 4%
4PR
G≥3 hematological AEs 12%
G≥3 reduced visual acuity 4%
G≥3 muscular weakness 4%
G≥3 RSV infection 4%
G≥3 rash 4%
Mahadevan et al. (288)1
NCT00648739
Ibrutinib (420 mg or 560 mg) and nivolumab Phase I-IIa
56 patients (20 Richter syndrome)
ORR 97% G≥3 neutropenia 28%
G≥3 anemia 23%
G≥3 rash 8%
G≥3 increased ALT 2%
Serious AEs: anemia 4% and pneumonia 4%
Younes et al. (289)1
NCT02329847
For CLL: induction with umbralisib and ublituximab, consolidation with pembrolizumab, umbralisib and ublituximab, maintenance with umbralisib until progression or unacceptable AE.
For Richter syndrome: umbralisib, ublituximab and pembrolizumab
Phase I/II
14 patients (5 Richter syndrome)
R/R CLL
CLL: ORR 89%
Richter syndrome: ORR 50%, 50% CR PFS 71% (median follow-up 15 months)
G≥3 neutropenia 43%
G≥3 ALT/AST increase 21%
G≥3 hypophosphatemia 21%
G≥3 pneumonitis 7%
Mato et al. (290)
Nivolumab vs pembrolizumab
and ibrutinib in 3 patients and venetoclax in 1 patient
7 vs 3 patients
R/R CLL (Richter syndrome)
ORR 10% ND Rogers et al. (291)
Ipilimumab and lenalidomide Phase II
2 patients
R/R CLL to allogeneic HSCT
ORR 0 G≥3 neutropenia 40%
G2 anemia 40%
G2 thrombocytopenia 20%
Flare of GVHD 10%
G2 nausea 10%
G2 headache 10%
G2 diarrhea 10%%
G2 elevated transaminase 10%
G2 hypertension 10%
G2 hypothyroidism 10%
Khouri et al. (292)1
NCT01919619
Nivolumab single agent until progression or unacceptable toxicity, with planned deescalation based on toxicity Phase I
1 patient
R/R CLL to allogeneic HSCT
ORR 32%
1-year PFS 23%, 1-year OS 56%
G≥3 thrombocytopenia 14%
G≥3 neutropenia 14%
G≥3 anemia 11%
G≥3 febrile neutropenia 11%
G≥3 fatigue 7.1%
G≥3 rash 3.6%
G≥3 transaminitis 7.1%
G≥3 fever 3.6%
G≥3 lipase elevation 14%
G≥3 pneumonitis 3.6%
G≥3 abdominal pain 3.6%
G≥3 nausea 3.6%
G≥3 arthralgia 3.6%
G≥3 bilirubin elevation 11%
G 5 acute GVHD (liver and gut) 7.1%
G 5 APS complicated by thrombotic CVA 3.6%
G 5 sepsis with ARDS 3.6%
Davids et al. (293)1
NCT01822509
Umbralisib and pembrolizumab Phase I
R/R CLL
ND ND NCT03283137
Pembrolizumab Phase II
R/R CLL with Richter Syrndrome
ND ND NCT02576990
Ublituximab and umbralisib in combination with targeted immunotherapy Phase I
R/R CLL or Richter syndrome
ND ND NCT02535286
Ibrutinib, fludarabine and pembrolizumab Phase II
high-risk or R/R CLL/SLL
ND ND NCT03204188
Atezolizumab, obinutuzumab and venetoclax Phase II
CLL, SLL, R/R Richter syndrome
ND ND NCT02846623
Durvalumab monotherapy and in combination (with lenalidomide and rituximab; with ibrutinib; with bendamustine and rituximab) Phase I-II
lymphoma or CLL
ND ND NCT02733042
Anti-LAG-3 (BMS-986016) single agent and in combination with nivolumab Phase I/IIa
R/R CLL
ND ND NCT02061761

AE, adverse events; APS, anti-phospholipid antibody syndrome; ARDS, acute respiratory distress syndrome; CLL, chronic lymphocytic leukemia; CR, complete response; CVA, cerebral vascular accident; G≥3, grade ≥3; GVHD, graft-versus-host disease; HSCT, hematopoietic stem cell transplantation; ND, no data; ORR, overall response rate; OS, overall survival; PFS, progression free survival; PR, partial response; R/R, relapsed or refractory; SD, stable disease; SLL, small lymphocytic lymphoma.

1Data for CLL patients only non-available.