Skip to main content
Top
Published in: BMC Musculoskeletal Disorders 1/2019

Open Access 01-12-2019 | Foreign Body Aspiration | Research article

The effect of a single consecutive volume aspiration on concentrated bone marrow from the proximal humerus for clinical application

Authors: Lukas N. Muench, Cameron Kia, Alexander Otto, Julian Mehl, Joshua B. Baldino, Mark P. Cote, Mary Beth McCarthy, Knut Beitzel, Augustus D. Mazzocca

Published in: BMC Musculoskeletal Disorders | Issue 1/2019

Login to get access

Abstract

Background

Low aspiration volumes have been recommended to allow for higher concentrations of progenitor cells during bone marrow harvesting. However, these guidelines then require multiple aspiration attempts in order to maximize cellular yield. The purpose of this study was to investigate the effect of a single, high-volume aspiration with four consecutive aliquots on the number of nucleated cells (NCs) and colony-forming units (CFUs) in concentrated bone marrow aspirate (cBMA) taken from the proximal humerus.

Methods

cBMA was taken from the proximal humerus of patients undergoing arthroscopic rotator cuff surgery. Four 12-mL double syringes were used consecutively from a single trocar to obtain four 10 cc aliquots. Each then underwent centrifugation to create a fractionated layer rich in nucleated cells. Following cellular separation, NCs were counted and CFUs were evaluated after incubation of 7–10 days. Cellular comparisons between each aliquot were performed along with their interaction with patient age and sex.

Results

Twenty-nine patients (55.9 ± 4.6 years) were included in this study. The number of NCs and CFUs showed significant differences between the four aliquots of aspirate, with the first 10 cc aliquot providing the highest amount (p < 0.001, respectively). No significant differences were found between the sum of the three sequential aliquots compared to the initial 10 cc sample. There were no significant differences between male and female patients (p > 0.05). Increasing age resulted in no significant decrease in the number of NCs and CFUs across the four consecutive aliquots (p > 0.05).

Conclusion

In conclusion, while the initial aliquot provided the greatest number of nucleated cells and cultured CFUs, the addition of each sequential volume aspirate yielded similar amounts in total. This demonstrates the potential effectiveness of obtaining of higher volume aspirates from the proximal humerus during rotator cuff repair.
Literature
1.
go back to reference Tomaru Y, Yoshioka T, Sugaya H, Aoto K, Wada H, Akaogi H, Yamazaki M, Mishima H. Hip preserving surgery with concentrated autologous bone marrow aspirate transplantation for the treatment of asymptomatic osteonecrosis of the femoral head: retrospective review of clinical and radiological outcomes at 6 years postoperatively. BMC Musculoskelet Disord. 2017;18(1):292.CrossRef Tomaru Y, Yoshioka T, Sugaya H, Aoto K, Wada H, Akaogi H, Yamazaki M, Mishima H. Hip preserving surgery with concentrated autologous bone marrow aspirate transplantation for the treatment of asymptomatic osteonecrosis of the femoral head: retrospective review of clinical and radiological outcomes at 6 years postoperatively. BMC Musculoskelet Disord. 2017;18(1):292.CrossRef
2.
go back to reference Freitag J, Bates D, Boyd R, Shah K, Barnard A, Huguenin L, Tenen A. Mesenchymal stem cell therapy in the treatment of osteoarthritis: reparative pathways, safety and efficacy - a review. BMC Musculoskelet Disord. 2016;17:230.CrossRef Freitag J, Bates D, Boyd R, Shah K, Barnard A, Huguenin L, Tenen A. Mesenchymal stem cell therapy in the treatment of osteoarthritis: reparative pathways, safety and efficacy - a review. BMC Musculoskelet Disord. 2016;17:230.CrossRef
3.
go back to reference Centeno CJ, Al-Sayegh H, Bashir J, Goodyear S, Freeman MD. A dose response analysis of a specific bone marrow concentrate treatment protocol for knee osteoarthritis. BMC Musculoskelet Disord. 2015;16:258.CrossRef Centeno CJ, Al-Sayegh H, Bashir J, Goodyear S, Freeman MD. A dose response analysis of a specific bone marrow concentrate treatment protocol for knee osteoarthritis. BMC Musculoskelet Disord. 2015;16:258.CrossRef
4.
go back to reference Mazzocca AD, McCarthy MB, Chowaniec DM, Cote MP, Arciero RA, Drissi H. Rapid isolation of human stem cells (connective tissue progenitor cells) from the proximal humerus during arthroscopic rotator cuff surgery. Am J Sports Med. 2010;38(7):1438–47.CrossRef Mazzocca AD, McCarthy MB, Chowaniec DM, Cote MP, Arciero RA, Drissi H. Rapid isolation of human stem cells (connective tissue progenitor cells) from the proximal humerus during arthroscopic rotator cuff surgery. Am J Sports Med. 2010;38(7):1438–47.CrossRef
5.
go back to reference Patterson TE, Boehm C, Nakamoto C, Rozic R, Walker E, Piuzzi NS, Muschler GF. The efficiency of bone marrow aspiration for the harvest of connective tissue progenitors from the human iliac crest. J Bone Joint Surg Am. 2017;99(19):1673–82.CrossRef Patterson TE, Boehm C, Nakamoto C, Rozic R, Walker E, Piuzzi NS, Muschler GF. The efficiency of bone marrow aspiration for the harvest of connective tissue progenitors from the human iliac crest. J Bone Joint Surg Am. 2017;99(19):1673–82.CrossRef
6.
go back to reference Carballo C, Lebaschi A, Rodeo SA. Cell-based approaches for augmentation of tendon repair. Tech Shoulder Elb Surg. 2017;18(3):e6–e14.CrossRef Carballo C, Lebaschi A, Rodeo SA. Cell-based approaches for augmentation of tendon repair. Tech Shoulder Elb Surg. 2017;18(3):e6–e14.CrossRef
7.
go back to reference Hernigou P, Poignard A, Beaujean F, Rouard H. Percutaneous autologous bone-marrow grafting for nonunions. Influence of the number and concentration of progenitor cells. J Bone Joint Surg Am. 2005;87(7):1430–7.PubMed Hernigou P, Poignard A, Beaujean F, Rouard H. Percutaneous autologous bone-marrow grafting for nonunions. Influence of the number and concentration of progenitor cells. J Bone Joint Surg Am. 2005;87(7):1430–7.PubMed
8.
go back to reference Muschler G, Boehm C, Easley K. Aspiration to obtain osteoblast progenitor cells from human bone marrow: the influence of aspiration volume. J Bone Joint Surg Am. 1997;79(11):1699–709.CrossRef Muschler G, Boehm C, Easley K. Aspiration to obtain osteoblast progenitor cells from human bone marrow: the influence of aspiration volume. J Bone Joint Surg Am. 1997;79(11):1699–709.CrossRef
9.
go back to reference Yandow SM, Van de Velde SK, Siebert J, Perkins SL. The influence of aspiration volume on the number of osteoblastic progenitors obtained from bone marrow in children. J Pediatr Orthop. 2017;39(7):382–6.CrossRef Yandow SM, Van de Velde SK, Siebert J, Perkins SL. The influence of aspiration volume on the number of osteoblastic progenitors obtained from bone marrow in children. J Pediatr Orthop. 2017;39(7):382–6.CrossRef
10.
go back to reference Hernigou P, Mathieu G, Poignard A, Manicom O, Beaujean F, Rouard H. Percutaneous autologous bone-marrow grafting for nonunions. Surgical technique. J Bone Joint Surg Am. 2006;88:322–7.CrossRef Hernigou P, Mathieu G, Poignard A, Manicom O, Beaujean F, Rouard H. Percutaneous autologous bone-marrow grafting for nonunions. Surgical technique. J Bone Joint Surg Am. 2006;88:322–7.CrossRef
11.
go back to reference Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult mesenchymal stem cells. Science. 1999;284(5411):143–7.CrossRef Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult mesenchymal stem cells. Science. 1999;284(5411):143–7.CrossRef
12.
go back to reference Voss A, McCarthy MB, Singh H, Beitzel K, DiVenere J, Cote MP, Hoberman AR, Nowak M, Imhoff AB, Mazzocca AD. The influence of trocar fenestration and volume on connective tissue progenitor cells (stem cells) in arthroscopic bone marrow aspiration from the proximal Humerus. Arthroscopy. 2017;33(6):1167–74 e1161.CrossRef Voss A, McCarthy MB, Singh H, Beitzel K, DiVenere J, Cote MP, Hoberman AR, Nowak M, Imhoff AB, Mazzocca AD. The influence of trocar fenestration and volume on connective tissue progenitor cells (stem cells) in arthroscopic bone marrow aspiration from the proximal Humerus. Arthroscopy. 2017;33(6):1167–74 e1161.CrossRef
13.
go back to reference Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–7.CrossRef Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8(4):315–7.CrossRef
14.
go back to reference Castro-Malaspina H, Gay RE, Jhanwar SC, Hamilton JA, Chiarieri DR, Meyers PA, Gay S, Moore MA. Characteristics of bone marrow fibroblast colony-forming cells (CFU-F) and their progeny in patients with myeloproliferative disorders. Blood. 1982;59:5.CrossRef Castro-Malaspina H, Gay RE, Jhanwar SC, Hamilton JA, Chiarieri DR, Meyers PA, Gay S, Moore MA. Characteristics of bone marrow fibroblast colony-forming cells (CFU-F) and their progeny in patients with myeloproliferative disorders. Blood. 1982;59:5.CrossRef
15.
go back to reference Hernigou P, Beaujean F, Lambotte JC. Decrease in the mesenchymal stem-cell pool in the proximal femur in corticosteroid-induced osteonecrosis. J Bone Joint Surg (Br). 1999;81(2):349–55.CrossRef Hernigou P, Beaujean F, Lambotte JC. Decrease in the mesenchymal stem-cell pool in the proximal femur in corticosteroid-induced osteonecrosis. J Bone Joint Surg (Br). 1999;81(2):349–55.CrossRef
16.
go back to reference Hustedt JW, Jegede KA, Badrinath R, Bohl DD, Blizzard DJ, Grauer JN. Optimal aspiration volume of vertebral bone marrow for use in spinal fusion. Spine J. 2013;13(10):1217–22.CrossRef Hustedt JW, Jegede KA, Badrinath R, Bohl DD, Blizzard DJ, Grauer JN. Optimal aspiration volume of vertebral bone marrow for use in spinal fusion. Spine J. 2013;13(10):1217–22.CrossRef
17.
go back to reference Hernigou P, Homma Y, Flouzat Lachaniette CH, Poignard A, Allain J, Chevallier N, Rouard H. Benefits of small volume and small syringe for bone marrow aspirations of mesenchymal stem cells. Int Orthop. 2013;37(11):2279–87.CrossRef Hernigou P, Homma Y, Flouzat Lachaniette CH, Poignard A, Allain J, Chevallier N, Rouard H. Benefits of small volume and small syringe for bone marrow aspirations of mesenchymal stem cells. Int Orthop. 2013;37(11):2279–87.CrossRef
18.
go back to reference Lamo-Espinosa JM, Mora G, Blanco JF, Granero-Molto F, Nunez-Cordoba JM, Sanchez-Echenique C, Bondia JM, Aquerreta JD, Andreu EJ, Ornilla E, et al. Intra-articular injection of two different doses of autologous bone marrow mesenchymal stem cells versus hyaluronic acid in the treatment of knee osteoarthritis: multicenter randomized controlled clinical trial (phase I/II). J Transl Med. 2016;14(1):246.CrossRef Lamo-Espinosa JM, Mora G, Blanco JF, Granero-Molto F, Nunez-Cordoba JM, Sanchez-Echenique C, Bondia JM, Aquerreta JD, Andreu EJ, Ornilla E, et al. Intra-articular injection of two different doses of autologous bone marrow mesenchymal stem cells versus hyaluronic acid in the treatment of knee osteoarthritis: multicenter randomized controlled clinical trial (phase I/II). J Transl Med. 2016;14(1):246.CrossRef
19.
go back to reference Nishida S, Endo N, Yamagiwa H, Tanizawa T, Takahashi HE. Number of osteoprogenitor cells in human bone marrow markedly decreases after skeletal maturation. J Bone Miner Metab. 1999;17:171–7.CrossRef Nishida S, Endo N, Yamagiwa H, Tanizawa T, Takahashi HE. Number of osteoprogenitor cells in human bone marrow markedly decreases after skeletal maturation. J Bone Miner Metab. 1999;17:171–7.CrossRef
20.
go back to reference Hernigou P, Beaujean F. Abnormalities in the bone marrow of the iliac crest in patients who have osteonecrosis secondary to corticosteroid therapy or alcohol abuse. J Bone Joint Surg Am. 1997;79(7):1047–53.CrossRef Hernigou P, Beaujean F. Abnormalities in the bone marrow of the iliac crest in patients who have osteonecrosis secondary to corticosteroid therapy or alcohol abuse. J Bone Joint Surg Am. 1997;79(7):1047–53.CrossRef
21.
go back to reference Beyth S, Mosheiff R, Safran O, Daskal A, Liebergall M. Cigarette smoking is asssociated with a lower concentration of CD105(+) bone marrow progenitor cells. Bone Marrow Res. 2015. Beyth S, Mosheiff R, Safran O, Daskal A, Liebergall M. Cigarette smoking is asssociated with a lower concentration of CD105(+) bone marrow progenitor cells. Bone Marrow Res. 2015.
22.
go back to reference McLain RF, Fleming JE, Boehm C, Muschler G. Aspiration of osteoprogenitor cells for augmenting spinal fusion: comparison of progenitor cell concentrations from the vertebral body and iliac crest. J Bone Joint Surg Am. 2005;87(12):2655–61.PubMedPubMedCentral McLain RF, Fleming JE, Boehm C, Muschler G. Aspiration of osteoprogenitor cells for augmenting spinal fusion: comparison of progenitor cell concentrations from the vertebral body and iliac crest. J Bone Joint Surg Am. 2005;87(12):2655–61.PubMedPubMedCentral
23.
go back to reference Zumstein MA, Ladermann A, Raniga S, Schar MO. The biology of rotator cuff healing. Orthop Traumatol Surg Res. 2017;103(1S):S1–S10.CrossRef Zumstein MA, Ladermann A, Raniga S, Schar MO. The biology of rotator cuff healing. Orthop Traumatol Surg Res. 2017;103(1S):S1–S10.CrossRef
24.
go back to reference Imam MA, Holton J, Ernstbrunner L, Pepke W, Grubhofer F, Narvani A, Snow M. A systematic review of the clinical applications and complications of bone marrow aspirate concentrate in management of bone defects and nonunions. Int Orthop. 2017;41(11):2213–20.CrossRef Imam MA, Holton J, Ernstbrunner L, Pepke W, Grubhofer F, Narvani A, Snow M. A systematic review of the clinical applications and complications of bone marrow aspirate concentrate in management of bone defects and nonunions. Int Orthop. 2017;41(11):2213–20.CrossRef
25.
go back to reference Hernigou J, Picard L, Alves A, Silvera J, Homma Y, Hernigou P. Understanding bone safety zones during bone marrow aspiration from the iliac crest: the sector rule. Int Orthop. 2014;38(11):2377–84.CrossRef Hernigou J, Picard L, Alves A, Silvera J, Homma Y, Hernigou P. Understanding bone safety zones during bone marrow aspiration from the iliac crest: the sector rule. Int Orthop. 2014;38(11):2377–84.CrossRef
26.
go back to reference Juneja SC, Viswanathan S, Ganguly M, Veillette C. A simplified method for the aspiration of bone marrow from patients undergoing hip and knee joint replacement for isolating Mesenchymal stem cells and in vitro Chondrogenesis. Bone Marrow Res. 2016;2016:3152065.CrossRef Juneja SC, Viswanathan S, Ganguly M, Veillette C. A simplified method for the aspiration of bone marrow from patients undergoing hip and knee joint replacement for isolating Mesenchymal stem cells and in vitro Chondrogenesis. Bone Marrow Res. 2016;2016:3152065.CrossRef
27.
go back to reference El-Jawhari JJ, Cuthbert R, McGonagle D, Jones E, Giannoudis PV. The CD45lowCD271high cell prevalence in bone marrow samples may provide a useful measurement of the bone marrow quality for cartilage and bone regenerative therapy. JBJS Am. 2017;99(15):1305–13.CrossRef El-Jawhari JJ, Cuthbert R, McGonagle D, Jones E, Giannoudis PV. The CD45lowCD271high cell prevalence in bone marrow samples may provide a useful measurement of the bone marrow quality for cartilage and bone regenerative therapy. JBJS Am. 2017;99(15):1305–13.CrossRef
28.
go back to reference Kwee E, Saidel G, Powell K, Heylman C, Boehm C, Muschler G. Quantifying proliferative and surface marker heterogeneity in Colony founding connective tissue progenitors and their progeny using time-lapse microscopy. J Tissue Eng Regen Med. 2018. Kwee E, Saidel G, Powell K, Heylman C, Boehm C, Muschler G. Quantifying proliferative and surface marker heterogeneity in Colony founding connective tissue progenitors and their progeny using time-lapse microscopy. J Tissue Eng Regen Med. 2018.
29.
go back to reference Muschler G, Nitto H, Boehm CA, Easley K. Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J Orthop Res. 2001;19:117–25.CrossRef Muschler G, Nitto H, Boehm CA, Easley K. Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors. J Orthop Res. 2001;19:117–25.CrossRef
30.
go back to reference Hernigou P, Flouzat Lachaniette CH, Delambre J, Zilber S, Duffiet P, Chevallier N, Rouard H. Biologic augmentation of rotator cuff repair with mesenchymal stem cells during arthroscopy improves healing and prevents further tears: a case-controlled study. Int Orthop. 2014;38(9):1811–8.CrossRef Hernigou P, Flouzat Lachaniette CH, Delambre J, Zilber S, Duffiet P, Chevallier N, Rouard H. Biologic augmentation of rotator cuff repair with mesenchymal stem cells during arthroscopy improves healing and prevents further tears: a case-controlled study. Int Orthop. 2014;38(9):1811–8.CrossRef
31.
go back to reference Pierini M, Di Bella C, Dozza B, Frisoni T, Martella E, Bellotti C. The posterior iliac crest outperforms the anterior iliac crest when obtaining mesenchymal stem cells from bone marrow. J Bone Joint Surg Am. 2013;95:1101–7.CrossRef Pierini M, Di Bella C, Dozza B, Frisoni T, Martella E, Bellotti C. The posterior iliac crest outperforms the anterior iliac crest when obtaining mesenchymal stem cells from bone marrow. J Bone Joint Surg Am. 2013;95:1101–7.CrossRef
Metadata
Title
The effect of a single consecutive volume aspiration on concentrated bone marrow from the proximal humerus for clinical application
Authors
Lukas N. Muench
Cameron Kia
Alexander Otto
Julian Mehl
Joshua B. Baldino
Mark P. Cote
Mary Beth McCarthy
Knut Beitzel
Augustus D. Mazzocca
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2019
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/s12891-019-2924-2

Other articles of this Issue 1/2019

BMC Musculoskeletal Disorders 1/2019 Go to the issue