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The role of immune checkpoint inhibitor pembrolizumab in treatment of patients with non small cell lung cancer: Review

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Lung cancer is the leading cause of deaths with 1.88 million cases and ranks fifth in the incidence of cancer in human (3.34 million) according to 2017 statistics worldwide and emerges as a global health burden.

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THE ROLE OF IMMUNE CHECKPOINT INHIBITOR

PEMBROLIZUMAB IN TREATMENT OF PATIENTS

WITH NON-SMALL CELL LUNG CANCER: REVIEW

Pham Thi Kim Nhung 1 ; Ta Ba Thang 1 ; Dao Ngoc Bang 1

SUMMARY

Lung cancer is the leading cause of deaths with 1.88 million cases and ranks fifth in the incidence of cancer in human (3.34 million) according to 2017 statistics worldwide and emerges

as a global health burden Immunotherapy, especially using immune checkpoint inhibitors has opened novel therapeutic opportunities that are effective for patients with advanced stage of lung cancer, who poorly responds or does not respond to chemoradiation therapy Pembrolizumab (keytruda) is a monoclonal antibody against PD-1 on surface of T-lymphocytes that have been shown improvement of overall survival, progression-free survival and mortality in non-small cell lung cancer patients based on the results of a series of clinical trials such as Keynote 010, 024, 021, 042, 189, 407 This is also the scientific basis for indication of keytruda that was approved by the United States Food and Drug Administration

* Keywords: Non-small cell lung cancer; PD-1; Pembrolizumab

IMMUNE CHECKPOINT INHIBITOR

DRUGS AND MECHANISM OF

PEMBROLIZUMAB (KEYTRUDA)

Immunotherapy is becoming increasingly

an effective treatment in malignant

diseases It differs from other methods

such as surgery, chemotherapy, radiotherapy,

targeted therapy in enhancing action of

the immune system to fight against

cancer cells by a “natural” way

In the past, immunotherapy in cancer

treatment was mainly non-specific

viaenhancing the function of the general

immune system or reducing the favorable micro-environment for the development and spread of cancer cells, such as vaccination against viruses that can lead to cancer, using cytokines (IL-2, IFN)

as an mediator… Currently, specific immunotherapy is focused on helping the component of the patient’s immune system to identify cancer cell easier and improve the effectiveness of immune response killing cancer cells such as using monoclonal antibodies (mAbs) or using of modified immune cells

1 103 Military Hospital

Corresponding author: Pham Thi Kim Nhung (khanhnhu106@gmail.com)

Date received: 09/09/2019

Date accepted: 15/10/2019

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Monoclonal antibodies are the most

common passive immunotherapy with many

types of antibodies approved by the United

States Food and Drug Administration

These antibodies can attack cancer cells

directly or attach specific protein on cancer

cells that help to transport chemotherapy

or radiotherapy, or flag cancer cells to the

immune system to recognize and destroy

In addition, monoclonal antibodies can

release or “unlock” immune checkpoint

inhibitor so that the immune system

becomes activated and perform the

function of killing cancer cells

Immune checkpoints are surface

receptors which regulate cell signals and

inhibit immune activity of T lymphocytes

In cancerous microenvironment, cancer

cells often express CTLA-4 ligand, PD-L1

ligand, thereby inhibiting T cell activity As

a result, immune checkpoint inhibitor

drugs will be a potential approach for

cancer immunotherapy

PD-1 (programmed cell death receptor 1)

is an immunosuppressant receptor

defined after CTLA-4 This receptor has

2 ligands (PD-L1 or B7-H1 or CD274) and

PD-L2 or B7-DC or CD273) [1] Although

the interaction between PD-L2 and PD-1

is 2 - 6 times higher than PD-L1 and PD-1,

PD-L1 is still the main ligand of PD-1 [2]

PD-1 is a negative regulatory receptor,

expressed only on the surface of

activated T lymphocytes while its ligands

(PD-L1 and PD-L2) can be expressed in

tumor cells under the action of cytokines

and interferons produced by activated

T cells or soluble in serum

The interaction of PD-L1 with the PD-1 receptor transmits an immunosuppressive signal to the T cell, resulting in an inactivated status of T cell or inhibited

T cells PD-1 also inhibits T cell activity by reducing the activating signal of the CD28 receptor, inhibiting the activity of the CD28 receptor PD-1 mainly controls the activity of activated T cell in peripheral tissues In addition, PD-1/PD-L1 pathway

is also thought to play a role in controlling the T cell invasion into the tumor, hence preventing the direct contact of activated

T cells and cancer cells [3] Therefore, monoclonal antibodies against PD-1 or PD-L1 will interact with PD-1 or PD-L1 respectively, helping to reactivate T cell

PD-L1 is a type 1 transmembrane protein (B7-H1); PD-L1 expression in tumor cells promotes regulations and self-tolerance of immune system by eliminating tumor cells by binding to

T lymphocyte Mechanism of “escaping” the control of immune system of the tumor cells: The immune system plays an important dual role in cancer through the process of immune repair Both the innate and adaptive immune system inhibit tumor growth and kill cancer cells during the elimination phage or immuno-surveillance However, tumor cells are able to escape this elimination phase by a variety of mechanisms such as creating a local immunosuppressive state, producing cytokines that have an immunosuppressive function, creating defects in the presentation

of tumor antigens to T cell or expression

of molecules that regulate immune check point like CTLA-4, PD-1 and PD-L1 Hence, tumor cells disrupt normal

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immune function to create favorable

conditions for tumor cells to grow For

example, the heterozygous loss of HLA

(human leukocyte antigen) appearing in

approximately 40% of patients with early

stage non-small cell lung cancer (NSCLC)

is a special manifestation of “escaping”

One of the cancer therapeutic strategies

to combat “escaping” is to reactivate T

cell mediated antitumor activity by

modulating the interaction between the

receptor and the ligand of immune

checkpoint In normal conditions, the

receptor of immune check point has the

function of limiting the activity of T cell,

preventing the destruction of normal cells,

creating balance

Mechanism of pembrolizumab (keytruda):

pembrolizumab is a monoclonal antibody

against the PD-1 receptor on the surface

of T cell Until now, there have been many

applications of immune checkpoint inhibitor

drugs in cancer treatment such as NSCLC,

colorectal cancer, stomach cancer, cervical

cancer, kidney cancer, melanoma…

However, for NSCLC, pembrolizumab

(keytruda) and nivolumab (opdivo),

atezolizumab (tecentriq) are the main

choice

CLINICAL STUDIES/TRIALS ON THE

EFFECTIVENESS OF

PEMBROLIZUMAB (KEYTRUDA) ON

NSCLC

1 General information

Pembrolizumab (keytruda) is a product

of MSD company This drug has been

applied in a series of clinical trials such as

Keynote 010, 024, 021, 042, 189, 407

and has shown positive results, opening

up new opportunities for patients with

NSCLC It is also the scientific basis for keytruda’s indications for this group of patients

2 Clinical trials

KEYNOTE 010 is a randomized,

open-label, phase 2/3 study that evaluate the efficacy of keytruda compared with standard chemotherapy in 1,034 advanced stage NSCLC patients, progression after platinum regimen with PD-L1 expression

on at least 1% Patients were randomly assigned (1:1:1) in 3 groups: 345 patients received pembrolizumab 2 mg/kg every

3 weeks; 346 patients received pembrolizumab 10 mg/kg every 3 weeks and 343 patients received docetaxel

75 mg/m2 every 3 weeks In addition, the number of patients with high PD-L1 expression (TPS ≥ 50%) were 139, 151 and 152 in 3 groups, respectively The endpoints were overall survival and progression free survival, rate of complete response and time of response [4] In this trial, treatment was discontinued for adverse reactions in 8% of the 682 patients receiving keytruda across both doses The most common adverse events resulting in permanent discontinuation of keytruda occurred in 23% of patients, the most common were diarrhea (1%), fatigue (1.3%), pneumonia (1%), liver enzyme elevation (1.2%), decrease appetite (1.3%) and pneumonitis (1%) Grade 3 - 5 treatment - related adverse events were less common with pembrolizumab than with docetaxel (43 of 339 patients (13%) received 2 mg/kg, 55 of 343 patients (16%) received 10 mg/kg, and 109 of 309 patients (35%) received docetaxel In the total population, median overall survival was

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10.4 months with pembrolizumab 2 mg/kg,

12.7 months with pembrolizumab

10 mg/kg, and 8.5 months with docetaxel

Overall survival was significantly longer

for pembrolizumab 2 mg/kg versus

docetaxel (hazard ratio [HR] 0.71, 95%CI:

0.58 - 0.88; p = 0.0008) and for

pembrolizumab 10 mg/kg versus docetaxel

(0.61, 0.49 - 0.75; p < 0.0001) Median

progression-free survival was 3.9 months

with pembrolizumab 2 mg/kg, 4.0

months with pembrolizumab 10 mg/kg, and

4.0 months with docetaxel, with no

significant difference in pembrolizumab

2 mg/kg versus docetaxel (0.88, 0.74 -

1.05; p = 0.07) or for pembrolizumab 10

mg/kg versus docetaxel (HR 0.79, 95%CI:

0.66 - 0.94; p = 0.004) Among patients

with at least 50% of tumor cells

expressing PD-L1, overall survival was

significantly longer with pembrolizumab

2 mg/kg than with docetaxel (median 14.9

months vs 8.2 months; HR 0.54, 95%CI:

0.38 - 0.77; p = 0.0002) and with

pembrolizumab 10 mg/kg than with

docetaxel (17.3 months vs 8.2 months;

0.50, 0.36 - 0.70; p < 0.0001) Likewise,

for this patient population,

progression-free survival was significantly longer with

pembrolizumab 2 mg/kg than with

docetaxel (median 5.0 months vs 4.1

months; HR 0.59, 95%CI: 0.44 - 0.78; p =

0.0001) and with pembrolizumab

mg/kg than with docetaxel (5.2 months vs

4.1 months; 0.59, 0.45 - 0.78; p <

0.0001) Keytruda was approved for

treatment of advanced stage NSCLC with

the fix dose of 200 mg every 3 weeks until

disease progression or unacceptable

toxicity or up to 24 months in patients

without disease progression [5]

KEYNOTE 042 is a randomized,

multi-center, open-label, active-controlled trial conducted in large scale of 32 countries,

in 21 centers in 1,274 patients with stage III NSCLC who were not candidates for surgical resection or definitive chemoradiation or metastatic NSCLC and whose tumors expressed PD-L1 (TPS ≥ 1%) and who had not received prior systemic treatment for metastatic NSCLC, no EGFR or ALK genomic tumor aberration Patients were randomized (1:1) to receive keytruda 200 mg intravenously every three weeks up to 35 cycles (n = 637) or investigator’s choice of either of the following chemotherapy regimens (n = 637): pemetrexed 500 mg/m2 or paclitaxel

200 mg/m2 and carboplatin AUC 5 to

6 mg/mL/min every three weeks on day 1 for a maximum of 6 cycles followed by optional pemetrexed 500 mg/m2 every three weeks for patients with nonsquamous histologies PD-L1 expression detected by IHC: 599/1,274 patients (47%) with PD-L1 expression TPS ≥ 50%; 818/1,274 patients (64%) with PD-L1 TPS ≥ 20%

Overall survival was significantly longer in the pembrolizumab group than

in the chemotherapy group in all three TPS populations (≥ 50% HR 0.69, 95%CI: 0.56 - 0.85, p = 0.0003; ≥ 20% 0.77, 0.64 - 0.92, p = 0.0020, and ≥ 1% 0.81, 0.71 - 0.93, p = 0.0018) The median survival values by TPS population were 20.0 months (95%CI: 15.4 - 24.9) for pembrolizumab versus 12.2 months (10.4 - 14.2) for chemotherapy, 17.7 months (15.3 - 22.1) versus 13.0 months (11.6 - 15.3), and 16.7 months (13.9 - 19.7) versus 12.1 months (11.3 - 13.3),

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respectively Treatment-related adverse

events of grade 3 or worse occurred in

113 of 636 patients (18%) treated in the

pembrolizumab group and in 252 of

615 patients (41%) in the chemotherapy

group and led to death in 13 patients (2%)

and 14 patients (2%), respectively The

benefit-to-risk profile suggests that

pembrolizumab monotherapy can be

extended as first-line therapy to patients

with locally advanced or metastatic

non-small-cell lung cancer without sensitizing

EGFR or ALK alterations and with low

PD-L1 TPS [6]

KEYNOTE 024 is a randomized,

open-label, phase 3 study evaluating keytruda

monotherapy compared to standard

of care (SOC) platinum-containing

chemotherapy for the treatment of

patients with both squamous (18%) and

non-squamous (82%) metastatic NSCLC

The study enrolled patients who had not

received prior systemic chemotherapy

treatment and whose tumors had high

PD-L1 expression (TPS ≥ 50%) and with

no EGFR or ALK aberrations 305 patients

randomized receive keytruda 200 mg

every 3 weeks or investigator-choice

SOC platinum-based chemotherapy

(pemetrexed + carboplatin, pemetrexed +

cisplatin, gemcitabin + cisplatin,

gemcitabin + carboplatin or paclitaxel +

carboplatin) Pemetrexed maintenance

therapy was permitted for patients with

non squamous histologies The primary

endpoint was progression free survival

(PFS), overall survival (OS) and objective

response rate (ORR) [7] At May 2016,

the trial was followed 11.2 months There

were 189 patients progressive or died

Median PFS was 10.3 months (95%CI:

6.7 to not reached) in the pembrolizumab group versus 6.0 months (95%CI: 4.2 - 6.2)

in the chemotherapy group The estimated percentage of patients who were alive and had no disease progression at 6 months was 62.1% (95%CI: 53.8 - 69.4)

in the pembrolizumab group and 50.3 (95%CI: 41.9 - 58.2) in the chemotherapy group Progression free survival was significantly longer in the pembrolizumab group than in the chemotherapy group (HR for disease progression or death, 0.5;

95%CI: 0.37 - 0.68, p < 0.001) At this time, 108 deaths were reported The estimated percentage of patients who were alive at 6 months was 80.2%

(95%CI: 72.9 - 85.7) in the pembrolizumab group and 72.4% (95%CI: 64.5 - 78.9) in the chemotherapy group; median overall survival was not reached in either group

Overall survival was significantly longer in the pembrolizumab group than in the chemotherapy group (hazard ratio for death, 0.60; 95%CI: 0.41 - 0.89; p = 0.005)

The objective response rate, assessed according to RECIST, was 44.8% (95%CI:

36.8 - 53.0) in the pembrolizumab group and 27.8% (95%CI: 20.8 - 35.7) in the chemotherapy group The median time to response was 2.2 months in both groups

Keytruda combined pemetrexed and platinum using for patients with advanced stage nonsquamous NSCLC without EGFR/ALK aberrations had been demonstrated improvement in OS (HR 0.49, 95%CI: 0.38 - 0.64, p < 0.00001);

PFS (HR 0.52, 95%CI: 0.43 - 0.64,

p < 0.00001) and a half decreasing risk of death compared to chemotherapy group

This results were observed in KEYNOTE

189 clinical trial [8]

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KEYNOTE 407 is a randomized,

double-blind, multicenter, placebo-controlled

study The criteria for this study were

metastatic squamous NSCLC, regardless

of tumor PD-L1 expression status and no

prior systemic treatment for metastatic

disease Keytruda in combination with

chemotherapy (carboplatin and either

paclitaxel or nab-paclitaxel) significantly

improved overall survival, reducing the

risk of death by 36% compared to

chemotherapy alone (HR = 0.64; 95%CI:

0.49 - 0.85; p = 0.0017) This results are

the basis for FDA approval of keytruda in

first step treatment in combination with

carboplatin and paclitaxel/nab-paclitaxel

for patients with advanced squamous

NSCLC regardless of tumor PD-L1

expression status [9]

KEYNOTE 021 was conducted on 123

previously untreated patients with metastatic

nonsquamous NSCLC with no EGFR or

ALK genomic tumor aberrations and

irrespective of PD-L1 expression In this

trial, keytruda + pem/carbo demonstrated

an objective response rate (ORR) that

was nearly double the ORR of pem/carbo

alone (55% [95%CI: 42 - 68] compared to

29% [95%CI: 18 - 41], respectively; all

responses were partial responses) In

addition, median PFS in patient treated

with keytruda + pem/carbo is 13 months

compared to 8.9 months in patients with

pem/carbo alone Patients in the keytruda

combination arm received keytruda 200 mg,

pemetrexed 500 mg/m2 and carboplatin

AUC 5 mg/mL/min every three weeks for

four cycles followed by keytruda every

three weeks [10]

INDICATIONS OF PEMBROLIZUMAB (KEYTRUDA) FOR NSCLC

From the first approval on October

2nd 2015, FDA has updated 6 times of keytruda indications for NSCLC patients, including:

- To treat patients with advanced (metastatic) NSCLC whose disease has progressed after other treatment and with tumors that express a protein called PD-L1

- To treat patients with metastatic NSCLC (as the first line treatment) whose tumors have high PD-L1 expression (tumor proportion score-TPS-of 50% or more) as determined by an FDA-approved test, with no EGFR or ALK genomic tumor aberration

- To treat patients with stage III NSCLC (as monotherapy for the first step treatment) who are not candidates for surgical resection or definitive chemoradiation or metastatic NSCLC and whose tumors express PD-L1 ≥ 1% with

no EGFR or ALK genomic tumor aberration

- To treat as monotherapy for the second step or greater treatment of patients with metastatic NSCLC whose tumors express PD-L1 (TPS ≥ 1%) with disease progression on or after platinum-containing chemotherapy Patients with EGFR or ALK genomic tumor aberration should have disease progression on FDA-approved therapy for these aberration prior to receiving keytruda

- To treat in combination with pemetrexed and platinum chemotherapy for the first line treatment of patients with metastatic nonsquamous NSCLC with no EGFR or ALK genomic tumor aberration, irrespective

of PD-L1 expression

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- To treat in combination with carboplatin

and either paclitaxel or nab-paclitaxel for

the first line treatment of patients with

metastatic squamous NSCLC regardless

of tumor PD-L1 expression status

CONCLUSION

Pembrolizumab (keytruda) is a

monoclonal antibody against PD-L1 and a

potential immuno-therapy for NSCLC

patients It has been demonstrated

effectively with improvement of OS, PFS

and mortality

REFERENCES

1 Latchman Y et al PD-L2 is a second

ligand for PD-1 and inhibits T cell activation

Nat Immunol 2001, 2 (3), pp.261-268

2 Youngnak P et al Differential binding

properties of B7-H1 and B7-DC to programmed

death-1 Biochem Biophys Res Commun

2003, 307 (3), pp.672-677

3 Teixido et al PD-L1 expression testing

in non-small cell lung cancer Ther Adv Med

Oncol 2018, 10, p.1758835918763493

4 Herbst R.S et al Pembrolizumab versus

docetaxel for previously treated,

PD-L1-positive, advanced non-small cell lung cancer

(KEYNOTE-010): A randomised controlled trial Lancet 2016, 387(10027), pp.1540-1550

5

https://www.fda.gov/drugs/resources- information-approved-drugs/pembrolizumab-keytruda-checkpoint-inhibitor Pembrolizumab (KEYTRUDA) Checkpoint Inhibitor 2016

6 Mok T.S.K et al Pembrolizumab

versus chemotherapy for previously untreated, PD-L1-expressing, locally advanced or metastatic non-small cell lung cancer (KEYNOTE-042): A randomized, open-label, controlled, phase 3 trial Lancet, 2019

7 Reck M et al Pembrolizumab versus

chemotherapy for PD-L1-positive non-small cell lung cancer N Engl J Med 2016, 375 (19), pp.1823-1833

8 Gandhi L et al Pembrolizumab plus

chemotherapy in metastatic non-small cell lung cancer N Engl J Med 2018, 378 (22), pp.2078-2092

9

https://www.fda.gov/drugs/fda-approves- pembrolizumab-combination-chemotherapy-first-line-treatment-metastatic-squamous-nsclc FDA approves pembrolizumab in combination with chemotherapy for first-line treatment of metastatic squamous NSCLC 2018

10

https://www.fda.gov/drugs/resources- information-approved-drugs/pembrolizumab-keytruda-5-10-2017 Pembrolizumab (keytruda)

2017, 5,10

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