Autologous bone marrow cell therapy for peripheral arterial disease

Figures & data

Table 1 Two classifications of peripheral arterial disease (PAD): Fontaine and Rutherford

PAD		Fontaine		Rutherford
Symptoms	Pathophysiology	Stage	Clinical	Grade	Category	Clinical
Fortuitous discovery of aortic and iliac calcifications	ATS plaques Plaques at risk (inflammation of ATS plaques) Atherothrombosis	I	Asymptomatic	0	0	Asymptomatic
ACD > 200 m Recovery time < 2 minutes	Discrepancy between oxygen demand and arterial supply	IIa	Intermittent claudication	I	1	Intermittent claudication
ACD ≤ 200 m Recovery time > 2 minutes	Higher discrepancy between oxygen demand and arterial supply	IIb	Moderate or severe claudication	I	2	Moderate claudication
ACD < 100 m Recovery time > 2 minutes	Higher discrepancy between oxygen demand and arterial supply Acidosis			I	3	Severe claudication
Ischemic rest pain	Severe skin hypoxia and acidosis	III	Ischemic rest pain Critical limb ischemia	II	4	Ischemic rest pain Critical limb ischemia
Necrosis	Severe skin hypoxia and acidosis Infection	IV	Ischemic ulceration	III	5	Minor tissue loss
Gangrene	Severe skin hypoxia and acidosis Infection		Tissue loss and gangrene	III	6	Major tissue loss

Abbreviations: ACD, absolute claudication distance; ATS, atherosclerotic.

Figure 1 Schematic representation of neoangiogenesis promoted by circulating and bone marrow–resident stem cells.

Notes: Ischemia induces production of growth factors, cytokines, and hormones, which promotes proliferation, differentiation, and mobilization of mesenchymal stem cells (MSCs) and endothelial progenitor cells (EPCs) to form new vessels. In addition, the growth factors can stimulate EPCs sprouting from preexisting blood vessels.
Abbreviations: FGF, fibroblast growth factor; G-CSF, granulocyte colony-stimulating factor; IL, interleukin; NO, nitric oxide; VEGF, vascular endothelial growth factor.

Table 2 Clinical trials with cell therapy in peripheral arterial disease (PAD)

Published study	Delivery route	Condition	Patients (n)	Cell type	Follow-up time	Improved functional outcomes
Tateishi-Yuyama et al^Citation14	IM	PAD, DM	45	BMCs or PB-MNCs	4 and 24 weeks	ABI, TcPO2, rest pain, pain-free walking time
Esato et al^Citation15	IA	PAD	8	BMCs	N/D	Ulceration healing
Saigawa et al^Citation16	IM	PAD, DM	8	BMCs	4 weeks	ABI, TcPO2
Higashi et al^Citation17	IM	PAD	7	BMCs or BM-MNCs	4 and 24 weeks	ABI, TcPO2, pain-free walking time
Miyamoto et al^Citation18	IM	CLI	12	BMCs and EPCs	N/D	ABI, pain-free walking time
Huang et al^Citation19	IM	PAD	5	PB-MNCs	3 months	ABI, LDF
Kawamura et al^Citation20	IM	PAD, CLI	30	PB-MNCs	N/D	T°C
Lenk et al^Citation21	IA	CLI	7	PB-MNCs	20 weeks	ABI, TcPO2, rest pain, pain-free walking time
Huang et al^Citation22	IM	CLI, DM	28	MPB-MNCs	3 months	ABI, pain, ulcers
Ishida et al^Citation23	IM	PAD	6	MPB-MNCs	4 and 24 weeks	ABI, ulcers
Durdu et al^Citation24	IM	PAD	28	BM-MNCs	3 and 6 months	ABI, rest pain, pain-free walking time
Koshikawa et al^Citation25	IM	PAD	7	BM-MNCs	6 months	ABI, pain, ulcers
Arai et al^Citation26	IM	PAD	25	BMCs	1 month	ABI, TcPO2
Miyamoto et al^Citation27	IM	PAD, CLI	8	BM-MNCs	4 weeks, 4 and 7 months, and 1 year	Rest pain, ulcers
Kawamura et al^Citation28	IM	CLI	92	PB-MNCs	6 weeks	Limb salvage, VEGF serum level
Bartsch et al^Citation29	IM and IA	PAD, CLI	13	BMCs	2 and 13 months	ABI, pain-free walking distance
Huang et al^Citation30	IM	PAD	150	BM-MNCs or MPB-MNCs	12 weeks	ABI, rest pain
Kajiguchi et al^Citation31	IM	CLI	7	BM-MNCs or PB-MNCs	1 month	ABI
Hernández et al^Citation32	IM	CLI, DM	12	BM-MNCs	24 months	ABI, SaO2, pain-free walking time, rest pain
Saito et al^Citation33	IM	PAD	7	BM-MNCs	N/D	TcPO2
Matoba et al^Citation34	IM	PAD	115	BM-MNCs	3 years	Pain, ulcers, pain-free walking distance
Napoli et al^Citation35	IA	PAD	18	BM-MNCs	3, 6, 12, and 18 months	ABI, ulcers, pain-free walking distance
Gu et al^Citation36	IM or IA	PAD, DM	32	BM-MNCs	4 weeks	ABI, TcPO2, limb salvage
Chochola et al^Citation37	IA	PAD, DM	24	BM-MNCs	1 year	Limb salvage, wound healing
Wester et al^Citation38	IM	CLI	8	BMCs	4 and 8 months	ABI, TcPO2, ulcers
Van Tongeren et al^Citation39	IM and IA	CLI	27	BMCs	6 and 12 months	Pain-free walking distance, ABI, pain reduction
De Vriese et al^Citation40	IM	CLI	16	BM-MNCs	12 weeks	TcPO2, pain reduction
Cobellis et al^Citation41	IA	PAD	10	BM-MNCs	12 months	ABI, pain-free walking distance
Motukuru et al^Citation42	IM	PAD	38	BM-MNCs	6 months	Ulcer healing, limb salvage, ABI, TcPO2
Amann et al^Citation43	IM	CLI	45	BM-MNCs	3 months	Limb salvage, ABI, TcPO2, pain-free walking distance
Amann et al^Citation44	IM	PAD	51	BM-MNCs	6 months	Limb salvage, ABI, TcPO2, pain-free walking distance
Capiod et al^Citation45	IM	CLI	24	BM-MNCs or PB-MNCs	N/D	No clinical evaluation reported
Franz et al^Citation46	IM and IA	PAD	9	BM-MNCs	2 weeks and 3 months	ABI, pain reduction, ulcers, limb salvage
Franz et al^Citation47	IM and IA	PAD	20	BM-MNCs	3 months	ABI, pain reduction, ulcers, limb salvage
Zafarghandi et al^Citation48	IM	CLI	50	BM-MNCs and G-CSF	4 and 24 weeks	ABI, pain-free walking distance
Procházka et al^Citation49	IM	CLI, DF	37	BMSCs	3 months	LDF, ABI, TcPO2, limb salvage
Procházka et al^Citation3	IM	PAD	96	BMSCs	4 months	ABI, limb salvage
Lara-Hernandez et al^Citation50	IM	CLI	28	Mobilized EPCs	14 and 18 months and 1 year	ABI, limb salvage
Iso et al^Citation51	IM	CLI	13	BM-MSCs	4 months	TcPO2, rest pain
Sprengers et al^Citation52	IA	CLI	120	BM-MNCs	6 months	Limb salvage, ulcers, rest pain, ABI, TcPO2
Murphy et al^Citation53	IM	CLI	29	BM-MNCs	1 year	First-toe pressure and toe-brachial index increase, perfusion index by computed tomography, rest pain
Walter et al^Citation54	IA	CLI	40	BM-MNCs	3 months	ABI, ulcer healing, rest pain
Iafrati et al^Citation55	IM	CLI, DM	48	BMSCs	12 weeks	Limb salvage, pain, ABI, Rutherford classification, quality of life
Idei et al^Citation56	IM	CLI	97	BM-MNCs	56 months	ABI, TcPO2, pain, amputation-free survival rate
Ruiz-Salmeron et al^Citation57	IA	CLI	20	BM-MNCs	3 and 12 months	Rutherford classification, diabetic wound scales, ABI, mortality rate
Lu et al^Citation58	IM	CLI, DM	82	BM-MNCs, BMSCs	6 and 24 weeks	Pain-free walking time, ABI, TcPO2, ulcers, limb salvage
Gabr et al^Citation59	IM	CLI	20	BM-MNCs	3 months	Walking distance, rest pain, skin condition, ABI
Benoit et al^Citation60	IM	CLI	48	BMSCs	6 months	Limb salvage, Rutherford classification, ABI, pain
Powell et al^Citation61	IM	CLI	86	BMCs	6 and 12 months	Limb salvage, TTF, wound healing
Perin et al^Citation62	IM	CLI	21	BM-MNCs	6 and 12 weeks	Rutherford classification, ABI, TcPO2, quality of life, pain
Smadja et al^Citation63	IM	CLI	11	BM-MNCs	6 and 12 months	TcPO2, wound healing, limb salvage
Powell et al^Citation64	IM	CLI	77	Multicellular therapy	12 months	TTF, limb salvage
Klepanec et al^Citation65	IM or IA	CLI	41	BMCs	6 months	Rutherford classification, ABI, TcPO2, pain, limb salvage, wound healing
Schiavetta et al^Citation66	IA	CLI, DM	60	BM-MNCs	12 months	LDF, TcPO2, limb salvage

Abbreviations: ABI, ankle-brachial index; BMCs, bone marrow cells; BMSCs, bone marrow stem cells; BM-MNCs, bone marrow–derived mononuclear cells; CLI, critical limb ischemia; DF, diabetic foot; DM, diabetes mellitus; EPCs, endothelial progenitor cells; G-CSF, granulocyte colony-stimulating factor; IA, intra-arterial injection; IM, intramuscular injection; LDF, laser Doppler flowmetry; MPB-MNCs, mobilized peripheral blood–derived mononuclear cells; N/D, not determined; PB-MNCs, peripheral blood–derived mononuclear cells; SaO₂, arterial oxygen saturation; T°C, temperature expressed in degrees Celsius; TcPO₂, transcutaneous oxygen tension; TTF, time to first occurrence of treatment failure; VEGF, vascular endothelial growth factor.

Table 3 Clinical trials with intralesional administration of stem cells in foot ulcers

Published study	Condition	Patients (n)	Cell type	Follow-up time	Improved functional outcomes
Vojtassák et al^Citation67	DF	1	BMSCs	29 days	Wound size and ulcer healing
Dash et al^Citation68	DF ulcers, PAD	24	BMSCs	3 months	Wound size and pain-free walking distance
Subrammaniyan et al^Citation69	CLI	6	BM-MNCs	6 months	ABI and pain-free walking distance, limb salvage, ulcer healing, and rest pain

Abbreviations: ABI, ankle-brachial index; BM-MNCs, bone marrow–derived mononuclear cells; BMSCs, bone marrow stem cells; CLI, critical limb ischemia; DF, diabetic foot; PAD, peripheral arterial disease.

Table 4 Controlled clinical trials with cell therapy in peripheral arterial disease

Published study	Year	Patients
		Total (N)	Treated (n)	Control (n)
Powell et al^Citation64	2012	72	48	24
Benoit et al^Citation60	2011	48	34	14
Lu et al^Citation58	2011	82	41	41
Powell et al^Citation61	2011	46	32	14
Idei et al^Citation56	2011	97	51	46
Iafrati et al^Citation55	2011	48	34	14
Walter et al^Citation54	2011	40	19	21
Procházka et al^Citation3	2010	96	42	54
Sprengers et al^Citation52	2010	110	55	55
Cobellis et al^Citation41	2008	19	10	9
Bartsch et al^Citation29	2007	25	13	12
Arai et al^Citation26	2006	25	13	12
Huang et al^Citation22	2005	28	14	14

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