Research progress and value of albumin-related inflammatory markers in the prognosis of non-small cell lung cancer: a review of clinical evidence

Figures & data

Figure 1. Pro-inflammatory activity of C-reactive protein and peripheral blood cells in non-small cell lung cancer patients with involvement of albumin. Figure created with BioRender.com. IL: interleukin; TNF: tumour necrosis factor; TGF: transforming growth factor; IFN: interferon; VEGF: vascular endothelial growth factor; PDGF: platelet-derived growth factor.

Figure 2. Bibliometric analysis of albumin and non-small cell lung cancer. (A) Number and trend of annual publications about albumin and non-small cell lung cancer. (B) Keyword frequency analysis of albumin and non-small cell lung cancer. (C) Analysis of associated genes of albumin and non-small cell lung cancer.

Table 1. Description of the CAR, GPS, mGPS, Hs-mGPS, and a-GPS.

Full name	Abbreviation	Calculation formula	Reference
C-reactive protein albumin ratio	CAR	C-reactive protein/Albumin	[15]
Glasgow prognostic score	GPS	CRP ≤10 mg/L and albumin ≥35 g/L, score 0; CRP >10 mg/L or albumin <35 g/L, score 1; CRP >10 mg/L and albumin <35 g/L, score 2	[19]
Modified Glasgow prognostic score	mGPS	CRP ≤10 mg/L and albumin ≥35 g/L, score 0; CRP >10 mg/L and albumin ≥35 g/L, score 1; CRP >10 mg/L and albumin <35 g/L, score 2	[21]
High-sensitivity modified Glasgow prognostic score	Hs-mGPS	CRP ≤3 mg/L and albumin ≥35 g/L, score 0; CRP >3 mg/L and albumin ≥35 g/L, score 1; CRP >3 mg/L and albumin <35 g/L, score 2	[23]
Adjusted Glasgow prognostic score	a-GPS	CRP ≤3 mg/L and albumin ≥39 g/L, score 0; CRP >3 mg/L or albumin ≥39 g/L, score 1; CRP >3 mg/L and albumin <39 g/L, score 2	[24]

Table 2. Summary of the characteristics of CAR in clinical studies.

Parameter	Participants’ conditions	cut-off value	Low/ High(N)	Outcome	AUC	Clinical findings	Reference
CAR	Elderly patients with operable NSCLC	0.28	59/49	OS	0.59	CAR is a prognostic marker, but GPS is not.	[17]
	Patients in pN2-stage IIIA with LADC	0.6	122/25	RFS	–	CAR is a prognostic marker, better than GPS, mGPS, Hs-mGPS, and PNI.	[30]
	Patients with operable NSCLC	0.424	492/125	DFS, OS	–	CAR is a prognostic marker.	[31]
	Patients with advanced NSCLC	0.2357	287/149	OS	0.700	CAR is a prognostic marker, better than GPS, mGPS, NLR, PLR and MLR.	[32]
	Chinese patients with NSCLC	0.14/0.22	148/110/129	OS	–	CAR is a prognostic marker, better than CRP, Alb.	[33]
	Patients with advanced NSCLC	0.35	38/39	OS	–	CAR may be a cheap, easy, and effective tool for predicting the death and its time of hospitalized NSCLC patients better than CRP.	[34]
	Patients with NSCLC underwent surgery	0.4	320/172	RFS	–	CAR and GPS may be independent risk factors for early recurrence.	[4]
	Patients with NSCLC underwent surgical resection	0.156	116/480	RFS, OS	0.587	CAR is a prognostic marker, better than GPS, mGPS.	[35]
	Patients with NSCLC treated with nivolumab	0.83	74/39	PFS, OS	–	CAR may be predictive of therapeutic response to nivolumab and long-term survival in NSCLC patients better than GPS, and NLR.	[36]

NSCLC: non-small cell lung cancer; LADC: lung adenocarcinoma; NLR: neutrophil-to-lymphocyte ratio; OS: overall survival; RFS: relapse-free survival; DFS: disease-free survival; PFS: progression-free survival; N: number of patients.

Table 3. Description of the PNI, ALI, COA-NLR, NLDA, ANPG, and HALP.

Full name	Abbreviation	Calculation formula	Cut-off value	Reference
Prognostic nutritional index	PNI	10 × albumin (g/dL) + 0.005 × absolute lymphocyte count (/μL)	48	[46]
Advanced lung cancer inflammation Index	ALI	(BMI × albumin) / NLR	18	[47]
Alb concentration combined with NLR	COA-NLR	NLR >2.5 or Alb <35 g/L, score 0; NLR >2.5 or Alb <35 g/L, score 1; NLR >2.5 and Alb <35 g/L, score 2	–	[48]
NLR × D-dimer count/Albumin	NLDA	NLR × D-dimer count/albumin	0.15	[49]
Albumin and neutrophil combined prognostic grade	ANPG	Grade 1 = elevated albumin and low neutrophil; Grade 2 = low albumin and low neutrophil, as well as elevated albumin and elevated neutrophil; Grade 3 = low albumin and elevated neutrophil.	albumin: 42.55 g/L; neutrophil: 2.895 × 10^9/L	[50]
Haemoglobin, albumin, lymphocyte, and platelet score	HALP	haemoglobin (g/L) × albumin (g/L) × lymphocyte (/L)/platelet (/L)	48	[51]

NLR: neutrophil-to-lymphocyte ratio; BMI: body mass index.

Table 4. Summary of the characteristics of PNI, ALI, NLDA, and HALP in clinical studies.

Parameter	Participants’ conditions	Cut-off value	Low/ High(N)	Outcome	AUC	Clinical findings	Reference
PNI	Patients with NSCLC	49.5	69/69	OS	–	PNI is an independent prognostic marker.	[45]
	Patients with completely resected NSCLC	50	149/241	OS	0.63	PNI is an independent prognostic marker.	[52]
	Elderly (aged > 75 years) patients with completely resected NSCLC	49.6	146/126	OS	0.532	PNI is an independent prognostic marker.	[53]
	Patients with NSCLC underwent radical surgery	52	912/504	OS	–	Higher PNI in NSCLC patients suggests a favourable prognosis.	[54]
	Patients with completely resected NSCLC	48	46/202	OS, RFS	–	PNI is an independent prognostic marker.	[55]
	Patients with completely resected NSCLC	45/50	57/134/324	OS	–	PNI is an independent prognostic marker.	[56]
	Patients with NSCLC underwent open thoracotomy for curative resection	50	285/726	OS, RFS	0.727	PNI was associated with postoperative pulmonary complications and long-term outcomes.	[57]
	Patients with NSCLC underwent surgical pulmonary resection and receive neoadjuvant therapy	46.810	37/73	OS, RFS	0.628	PNI is an independent prognostic marker.	[58]
	Patients with NSCLC received adjuvant chemotherapy	50	54/52	RFS	–	PNI is an independent prognostic marker.	[59]
	Patients with NSCLC treated with EGFR TKI	45	177/453	OS, PFS	–	Pre-treatment nutritional status is a prognostic marker.	[60]
	Patients with NSCLC treated with ICIs	45.5	52/50	OS, PFS	0.694	PNI is an independent prognostic marker.	[62]
	Patients with NSCLC underwent curative radiotherapy	45.45	–	OS	0.666	PNI is an independent prognostic marker.	[63]
	Patients with aNSCLC treated with PD-1 inhibitors	45	47/55	OS, PFS	–	PNI may be a useful predictive marker of clinical outcomes and irAEs.	[64]
	Patients with advanced NSCLC treated with platinum-based chemotherapeutics	52.525	54/45	OS, PFS	–	PNI is an independent prognostic marker.	[65]
	Patients with recurrence NSCLC after complete pulmonary resection who received ICI monotherapy during the therapeutic course	50	–	PFS	–	PNI is an independent prognostic marker.	[66]
	Patients with aNSCLC treated with PD-1 inhibitors	46.05	53/70	OS, PFS	0.780	PNI was an independent predictor of early progression and survival outcomes.	[67]
	Patients with metastatic or recurrent ALK-positive NSCLC received first-line alectinib	40	11/31	PFS	–	PNI is important in predicting, which reflect the nutritional status of the host	[68]
	Patients in stage IA-IIIB with NSCLC underwent chest surgery	47	193/282	OS, RFS	0.62	PNI has high predictive values for postoperative complications and survival.	[70]
	Patients with bone mNSCLC without any anti-tumor therapy	54.5	154/105	OS	–	PNI is an independent prognostic marker.	[71]
	patients in stage IIIB/IV with NSCLC	50	179/136	OS	–	PNI is an independent prognostic marker.	[72]
	Patients with aNSCLC	46.1	67/116	OS	0.55	Nutritional status is an important prognostic factor.	[73]
	Patients with mNSCLC treated with first-line chemotherapy	46.7	184/149	OS, PFS	0.617	PNI is an independent prognostic marker.	[74]
	Patients in stage IIIB with NSCLC	40.5	190/168	OS, PFS, LPFS	0.841	PNI is an independent prognostic marker.	[75]
	Patients with aNSCLC	38.4	52/108	OS, PFS	0.69	PNI is an independent prognostic marker.	[76]
ALI	Patients with mNSCLC	18	83/90	OS, PFS	0.67	ALI is an independent prognostic marker.	[47]
	Patients with mNSCLC	23.2	21/20	OS, PFS	–	ALI is an independent prognostic marker.	[78]
	Patients in stage IV with NSCLC	18	38/74	OS	–	ALI is an independent prognostic marker.	[79]
	Patients with aNSCLC initiated nivolumab treatment	18	69/128	PFS	–	ALI is an independent prognostic marker.	[80]
	Patients with mNSCLC received complete first-line treatment with chemotherapy	11	19/90	OS, PFS	0.52	ALI is associated with survival.	[81]
	Patients with NSCLC received complete resection	37.66	121/220	OS	0.681	ALI is an independent prognostic marker.	[82]
	Patients with NSCLC underwent VATS	41.20	125/214	OS	0.324	ALI is an independent prognostic marker.	[83]
	Patients in stage IA with NSCLC underwent lung resection	22.2	18/148	OS, RFS	0.610	ALI is an independent prognostic marker.	[85]
	Patients with early-stage NSCLC received VATS pulmonary resection as their only therapy	50	155/137	OS, DFS	–	ALI is an independent prognostic marker.	[86]
	Patients with NSCLC treated with nivolumab	18	–	PFS	–	A high ALI was predictive of better PFS in patients with poor performance status.	[87]
	Patients with mNSCLC	32.6	191/127	OS	–	ALI is an independent prognostic marker.	[88]
NLDA	IV stage NSCLC patients	0.15	32/12	OS	0.7	NLDA is an independent prognostic marker.	[49]
HALP	Patients with NSCLC underwent radical lung cancer resection	48	99/139	OS	0.666	HALP is an independent prognostic marker.	[51]

NSCLC: non-small cell lung cancer; aNSCLC: advanced non-small cell lung cancer; mNSCLC: metastatic non-small cell lung cancer; LA-NSCLC: locally advanced non-small cell lung cancer; TKI: tyrosine kinase inhibitor; PD-1: programmed cell death protein‑1; ICI: immune checkpoint inhibitor; irAE: immune-related adverse event; NLR: neutrophil-to-lymphocyte ratio; OS: overall survival; PFS: progression-free survival; LPFS: local progression-free survival; DFS: disease-free survival; RFS: relapse-free survival; VATS: video-assisted thoracic surgery; N: number of patients.

Table 5. Comparison of advantages and disadvantages of albumin-related inflammatory markers, its suitable patients, and range of cut-off value.

Albumin-related inflammatory markers	Advantages	Disadvantages	Suitable patients	Range of cut-off value
CAR	An effective tool for predicting the survival of NSCLC patients.	The cut-off value is controversial.	Operable elderly patients with NSCLC.	0.14–0.83
GPS, mGPS, Hs-mGPS, a-GPS	More objective than CAR.	Inflexible. Lack of research on prognostic value in NSCLC patients after being treated with immunotherapy.	NSCLC patients, whose CRP and Alb values do not fluctuate around normal values.	–
PNI	A sensitive tool for predicting the survival of NSCLC patients.	Poor specificity.	Postoperative or advanced NSCLC patients.	38.4–52.525
ALI	The prognostic value is not affected by age.	Poor sensitivity and specificity.	Patients with aNSCLC or treated with immunotherapy.	11–50
COA-NLR	Preoperative COA-NLR can effectively stratify the prognosis of patients.	Inflexible. There are few related studies.	Patients with NSCLC underwent lung resection.	–
NLDA	Coagulation factors are considered.	There are few related studies.	Patients with NSCLC in the IV stage.	0.15
HALP	It is less likely to change under the influence of one factor.	There are few related studies.	Patients with NSCLC underwent lung resection.	48

NSCLC: non-small cell lung cancer; aNSCLC: advanced non-small cell lung cancer; CAR: C-reactive protein albumin ratio; GPS: Glasgow prognostic score; mGPS: modified Glasgow prognostic score; Hs-mGPS: high-sensitivity modified Glasgow prognostic score; a-GPS: adjusted Glasgow prognostic score; PNI: prognostic nutritional index; ALI: advanced lung cancer inflammation Index; COA-NLR: Alb concentration combined with NLR; NLDA: NLR × D-dimer count/Albumin; ANPG: albumin and neutrophil combined prognostic grade; HALP: haemoglobin, albumin, lymphocyte and platelet score.

Figure 3. Conceptual framework for albumin-related inflammatory markers in the prognosis and immune microenvironment of non-small cell lung cancer. (A) Increased or decreased albumin-related inflammatory markers predict poor prognosis in patients with non-small cell lung cancer. (B) Albumin, C-reactive protein, and peripheral blood cells play a role in the immune microenvironment of NSCLC. Figure created with BioRender.com. CAR: C-reactive protein albumin ratio; GPS: Glasgow prognostic score; mGPS: modified Glasgow prognostic score; Hs-mGPS: high-sensitivity modified Glasgow prognostic score; a-GPS: adjusted Glasgow prognostic score; PNI: Prognostic nutritional index; ALI: Advanced lung cancer inflammation Index; COA-NLR: Alb concentration combined with NLR; NLDA: NLR × D-dimer count/albumin; ANPG: albumin and neutrophil combined prognostic grade; HALP: haemoglobin: albumin: lymphocyte and platelet score; DC: dendritic cell; MDSC: myeloid-derived suppressor cell; CAF: cancer-associated fibroblast; NK: natural killer.

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Data availability statement

All data were included in the manuscript and there was no restriction on availability.