Mesenchymal stem cells in maxillary sinus augmentation: A systematic review with meta-analysis

Table 1 Histomorphometric results of the animal studies included in the review

Ref.	Animal model	Study design	Histomorphometry (% of newly formed bone)
Kang et al[42]	Minipig	SDSCs + AL	NR
		AL alone	NR
Sununliganon et al[59]	Rabbit	BMSCs + BBM	59.2 ± 2.1 (4 wk)
			55.9 ± 3.6 (8 wk)
		BBM alone	54.3 ± 2.8 (4 wk)
			51.5 ± 2.6 (8 wk)
		AB	NR
		Saline solution	NR
Yu et al[60]	Dog	BMSCs + BBM	NR
		PDLSCs + BBM	NR
		BBM alone	NR
Oshima et al[61]	Sheep	BMSCs + GBP-L + BBM	17.0 ± NR (8 wk)
			23.0 ± NR (16 wk)
		BMSCs + BBM	18.0 ± NR (8 wk)
			23.0 ± NR (16 wk)
Jhin et al[62]	Rabbit	BMP-2/BMSCs + BBM	12.6 ± 2.8 (2 wk)
			29.3 ± 4.6 (4 wk)
			25.7 ± 3.8 (8 wk)
		BMSCs + BBM	6.2 ± 2.6 (2 wk)
			25.7 ± 2.8 (4 wk)
			27.7 ± 8.2 (8 wk)
		BBM alone	4.2 ± 2.0 (2 wk)
			15.1 ± 2.9 (4 wk)
			22.7 ± 3.3 (8 wk)
Gutwald et al[63]	Sheep	MNCs + BBM	19.0 ± 11 (8 wk)
			29.0 ± 12 (16 wk)
		AB	20.0 ± 13 (8 wk)
			16.0 ± 6 (16 wk)
Sauerbier et al[64]	Sheep	MSCs + BBM	NR
		BBM alone	NR
Zhao et al[65]	Goat	DTSCs + CPC	41.8 ± 6.2 (12 wk)
		CPC alone	30.1 ± 8.0 (12 wk)
		AB	23.0 ± 10.2 (12 wk)
Zhang et al[66]	Dog	BMSCs + CPC	NR
		ADSCs + CPC	NR
		CPC alone	NR
Barboni et al[41]	Sheep	AESCs + CPC	NR
		CPC alone	NR
Berardinelli et al[40]	Sheep	AFSCs + MgHA/collagen	NR
		MgHA/collagen alone	NR
Zeng et al[67]	Rabbit	BMSCs + CPC	11.7 ± 1.8 (2 wk)
			25.4 ± 3.4 (8 wk)
		CPC alone	5.9 ± 1.4 (2 wk)
			20.5 ± 3.6 (8 wk)
		BMSCs + MPC	5.1 ± 1.7 (2 wk)
			13.5 ± 3.5 (8 wk)
		MPC alone	4.0 ± 1.2 (2 wk)
			6.5 ± 2.0 (8 wk)
		BMSCs + CMPC	12.7 ± 1.9 (2 wk)
			30.9 ± 3.1 (8 wk)
		CMPC alone	6.8 ± 1.3 (2 wk)
			25.5 ± 4.1 (8 wk)
Zou et al[68]	Goat	BMSCs + CPC	35.6 ± 9.4 (12 wk)
		CPC alone	22.4 ± 4.2 (12 wk)
		AB	28.2 ± 8.0 (12 wk)
Xia et al[69]	Rabbit	BMSCs + rhBMP-2/CPC	17.9 ± 4.3 (2 wk)
			30.5 ± 5.7 (4 wk)
			42.2 ± 4.0 (8 wk)
		BMSCs + CPC	13.9 ± 2.5 (2 wk)
			21.8 ± 4.4 (4 wk)
			28.7 ± 3.7 (8 wk)
		rhBMP-2/CPC	12.8 ± 3.0 (2 wk)
			18.9 ± 2.6 (4 wk)
			31.1 ± 4.5 (8 wk)
		CPC alone	8.0 ± 2.0 (2 wk)
			12.2 ± 3.1 (4 wk)
			22.7 ± 5.7 (8 wk)
Sun et al[70]	Rabbit	BMSCs + CPC	21.0 ± 2.6 (2 wk)
			23.4 ± 3.0 (4 wk)
			35.3 ± 10.5 (8 wk)
		CPC alone	19.2 ± 2.2 (2 wk)
			22.9 ± 2.1 (4 wk)
			19.5 ± 2.4 (8 wk)
		AB	34.7 ± 7.1 (2 wk)
			28.7 ± 5.8 (4 wk)
			NR (8 wk)
		Blood clot	NR (2 wk)
			17.5 ± 3.3 (4 wk)
			13.8 ± 4.0 (8 wk)
Sun et al[71]	Rabbit	BMP-2/BMSCs + CPC	21.2 ± 2.1 (2 wk)
			31.9 ± 2.2 (4 wk)
		EGFP/BMSCs + CPC	18.9 ± 1.9 (2 wk)
			23.19 ± 1.9 (4 wk)
Pieri et al[72]	Minipig	BMSCs + PRP + HA	42.5 ± 7.0 (12 wk)
		HA alone	18.9 ± 0.9 (12 wk)
Ohya et al[73]	Rabbit	BMSCs + PRP	29.1 ± 4.4 (2 wk)
			24.1 ± 3.6 (4 wk)
			20.9 ± 4.1 (8 wk)
		PCBM + PRP	35.0 ± 5.2 (2 wk)
			28.6 ± 3.4 (4 wk)
			20.6 ± 4.0 (8 wk)

SDSCs: Skin-derived stem cells; AL: Allograft; NR: Not reported; BMSCs: Bone marrow stem cells; BBM: Bovine bone mineral; AB: Autogenous bone; PDLSCs: Periodontal ligament stem cells; GBP-L: Gabapentin-lactam; MNCs: Mononuclear cells; DTSCs: Deciduos tooth stem cells; CPC: Calcium phosphate ceramics; AESCs: Amniotic epithelial stem cells; AFSCs: Amniotic fluid stem cells; Mg/HA: Magnesium/hydroxyapatite; MPC: Magnesium phosphate cement; CMPC: Calcium-magnesium phosphate cement; Rh-BMP-2: Recombinant human bone morphogenetic protein 2; PRP: Platelet rich in plasma; HA: Hydroxyapatite; PCBM: Particulate cancellous bone and marrow; ADSC: Adipose stem cell.

Table 2 Histomorphometric results of the human studies included in the review

Ref.	Patients	Study design	Histomorphometry (% of newly formed bone)
McAllister et al[74]	5	5 MSA: MSCs + AL	33.0 ± NR (16 wk)
Gonshor et al[75]	18	18 MSA: MSCs + AL	32.5 ± 6.8 (12 wk)
		8 MSA: AL	18.3 ± 10.6 (12 wk)
Duttenhoefer et al[77]	11	12 MSA: BMAC + BBM	NR
		6 MSA: Ficoll + BBM
Rickert et al[78]	12	12 MSA: BMSCs + BBM	NR
		12 MSA: AB + BBM
Kühl et al[79]	13	13 MSA: BMA + BBM	NR
		13 MSA: BMAC + BBM
Wildburger et al[80]	7	7 MSA: BMSCs + BBM	7.4 ± 4.1 (12 wk)
			13.5 ± 5.4 (24 wk)
		7 MSA: BBM	11.8 ± 6.2 (12 wk)
			13.9 ± 8.5 (24 wk)
Sauerbier et al[81]	26	34 MSA: BMAC + BBM	12.6 ± 1.7 (12 wk)
		11 MSA: AB + BBM	14.3 ± 1.8 (12 wk)
Rickert et al[82]	12	12 MSA: BMSCs + BBM	17.7 ± 7.3 (14 wk)
		12 MSA: AB + BBM	12.0 ± 6.6 (14 wk)
Schmelzeisen et al[83]	1	2 MSA: BMAC + BBM	26.9 ± NR (12 wk)
Fuerst et al[84]	12	22 MSA: BMSCs + BBM	17.9 ± 4.6 (24 wk)
Beaumont et al[85]	3	6 MSA: PDSCs + BBM	NR
Shayesteh et al[86]	6	6 MSA: BMSCs + HA/β-TCP	41.3 ± NR (24 wk)
Smiler et al[87]	4	2 MSA: BMSCs + β-TCP	40.0 ± NR (16 wk)
		1 MSA: BMSCs + BBM	13.0 ± NR (16 wk)
		1 MSA: BMSCs + HA	31.0 ± NR (16 wk)
Trautvetter et al[88]	10	10 MSA: PDSCs + PLGA	NR
Mangano et al[89]	1	1 MSA: PDSCs + PLGA	28.8 ± NR
Voss et al[91]	35	50 MSA: PDSCs + PLGA	NR
		63 MSA: AB
Mangano et al[90]	5	5 MSA: PDSCs + PLGA	37.3 ± 19.5 (24 wk)
		5 MSA: HA	54.6 ± 21.1 (24 wk)
Zizelmann et al[92]	20	14 MSA: PDSCs + PLGA	NR
		17 MSA: AB
Schimming et al[93]	27	27 MSA: PDSCs + PLGA	NR
Yamada et al[94]	23	23 MSA: BMSCs + PRP	NR
Ueda et al[95]	6	6 MSA: BMSCs + PRP	NR

MSA: Maxillary sinus augmentation; MSCs: Mesenchymal stem cells; AL: Allograft; NR: Not reported; BMAC: Autologous bone marrow aspirate concentrate; BBM: Bovine bone mineral; BMSCs: Bone marrow stem cells; AB: Autogenous bone; BMA: Bone marrow aspirate; PDSCs: Periosteal derived stem cells; HA/β-TCP: Hydroxyapatite/beta-tricalcium phosphate; PLGA: Polylactid-co-glycolic acid; PRP: Platelet rich in plasma.