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63 (); 216-223
doi:
10.1016/j.jor.2025.04.008

Bone marrow aspirate concentrate (BMAC) harvested in the axial and appendicular skeleton does not differ in progenitor cell count: A systematic review and meta-analysis

, , , , , , , ,
a Department of Orthopedic Surgery, Rush University Medical Center, Chicago, IL, USA
b University of Illinois College of Medicine at Chicago, Chicago, IL, USA
c Hackensack Meridian School of Medicine, Nutley, NJ, USA
d Hospital Italiano de Buenos Aires, Buenos Aires, Argentina

⁎Corresponding author: Jorge Chahla. jorge.chahla@rushortho.com

Received: , Accepted: ,
Professor P K Surendran Memorial Education Foundation
Disclaimer:
This article was originally published by Reed Elsevier India Pvt. Ltd. and was migrated to Scientific Scholar after the change of Publisher.

Abstract

Abstract

Bone marrow aspirate concentrate (BMAC) is a reliable source of progenitor cells that facilitate healing, and it is typically harvested from the iliac crest. The purpose of this systematic review and meta-analysis was to compare total nucleated cell (TNC) count and the presence of colony-forming units (CFUs) in BMAC harvested from axial versus appendicular harvest sites.

In accordance with Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, PubMed, Embase, and Cochrane Library databases were searched in August 2024 for studies published after 2004. Studies were included if they evaluated cell counts within BMAC samples harvested from males and females of any age and were prospective. Studies that had no reported cell count within BMAC samples, had evaluations of biologic material other than BMAC, or were translational or cadaveric studies, as well as review articles or technical notes, were excluded. Patients were divided into two cohorts based on whether BMAC was harvested from their axial or appendicular skeleton.

The initial search identified 2126 studies, of which 15 non-randomized prospective studies with a total of 583 patients were included. Each study had low risk of bias. In the axial skeleton, TNC counts ranged from 0.1–502 × 106 cells/mL, and CFU concentration ranged from 0 to 807 CFU/mL. In the appendicular skeleton, TNC counts ranged from 0.1–87 × 106 cells/mL and CFU counts ranged from 0 to 802.7 CFU/mL. No significant differences in TNC or CFU count in BMAC harvested from the axial versus appendicular skeleton were observed.

BMAC harvested from the axial and appendicular skeletons demonstrate significant variability in progenitor cell concentration. These findings suggest that harvesting at appendicular sites near the operative location allows the surgeon to extract sufficient quality BMAC as compared to harvest sites within the axial skeleton, such as the iliac crest.

Level II, systematic review of level II studies.

Keywords

Bone marrow aspirate concentrate
Biology of bone
Cell/Molecular biology
Stem cell therapy
1

1 Introduction

In recent years, there has been an increasing interest in biologic cellular-based treatments in orthopedics.1–3 One such treatment involves the use of mesenchymal signaling cells (MSCs), which are multipotent cells that can differentiate into cartilage and connective tissue, in addition to producing cellular microenvironments that are conducive to musculoskeletal healing.1,4,5 A frequently used source of MSCs, as well as progenitor cells and growth factors, in orthopedic surgery is bone marrow aspirate concentrate (BMAC), which is currently United States Food and Drug Administration-approved.1,5,6 However, BMAC typically has a low composition of MSCs, with estimates of 0.001–0.02 % of total cell count in a given sample.7 Therefore, optimizing the total nucleated cell (TNC) count and colony forming units (CFUs) contained within a BMAC sample is of importance to facilitate healing and improve outcomes.

Previous studies have established the iliac crest as the gold standard site for safe and effective harvest of BMAC with a relatively high density of desired progenitor cells.1,8–11 However, for procedures distal in the extremities, such as knee, ankle, or upper extremity procedures, harvesting BMAC from the iliac crest requires either multiple areas to be draped and prepped, or intraoperative repositioning, both of which lead to increased operating room time and costs.12 Thus, the ability to harvest BMAC near common operative sites, such as the proximal tibia and proximal humerus, may reduce morbidity for the patient and increase operating room efficiency.12 However, in this decision, surgeons face the hypothetical risk of harvesting BMAC away from the classic gold standard iliac crest, potentially sacrificing the quantity or quality of progenitor cells.

There is limited literature and no consensus comparing progenitor cell counts in BMAC across different anatomic harvest sites. The purpose of this systematic review and meta-analysis was to compare TNC count and the presence of CFUs in BMAC harvested from axial versus appendicular harvest sites. We hypothesized that TNC count and CFUs would not differ in BMAC harvested from the axial or appendicular skeleton.

2

2 Methods

2.1

2.1 Literature search methodology

A comprehensive search of PubMed, Embase, and Cochrane Library databases was performed in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines in August 2024. The following search strategy was utilized: “(‘bone marrow aspirate concentrate’ OR ‘BMAC’).” The search was performed by author (initials blinded for peer review).

Studies were included if they evaluated cell counts within BMAC samples harvested from males and females of any age group, were prospective studies, and were published after 2004. Studies that did not directly report cell counts with BMAC samples or evaluated biologic material other than BMAC, as well as studies that were translational studies, systematic reviews, narrative reviews, conference abstracts, technical notes, letters to editors, or meta-analyses were excluded. Two authors (initials blinded for review) independently screened titles, abstracts, and full article texts using the online software program Covidence (Veritas Health Innovation Ltd; Melbourne, Australia). Any disagreements were resolved with discussion leading to consensus between the two screening authors and a third senior author (initials blinded for peer review).

2.2

2.2 Data extraction and quality assessment

Data items extracted from each study included the total number of patients who produced a BMAC sample, patient sex, patient age, harvest site, cell type, mean TNC count, and CFU count. Assessment of study quality for each of the prospective non-randomized studies included in this systematic review and meta-analysis was performed with the Methodological Index for Non-Randomized Studies (MINORS) criteria.13

2.3

2.3 Statistical analysis

Data from each study were pooled utilizing the DerSimonian-Laird random-effects model. Compared to fixed-effects data pooling models, this model provides conservative estimates utilizing wider confidence intervals by assuming that included studies represent only a sample of all possible studies, accounting for an inherent limitation of systematic reviews that all relevant studies may not be ultimately included.14 For studies only reporting ranges, the standard deviation was approximated as the range divided by four. Given that patients from each study were divided into two cohorts depending on whether BMAC was harvested from the axial or appendicular skeleton, cell counts and CFU concentration were evaluated with subgroup analysis to compare means across these two cohorts.

3

3 Results

3.1

3.1 Search results

A total of 2126 studies were identified in the initial search, 512 of which were duplicates and were subsequently excluded. The remaining 1614 studies underwent a title and abstract screening; 1595 were found to be irrelevant to the study aims and therefore excluded. The remaining 19 studies were assessed for eligibility with full-text review. After excluding 4 studies for having an incorrect study design, incorrect intervention, or incorrect outcomes, 15 studies were ultimately included for data extraction (Fig. 1). Specifically, two studies were excluded for having incorrect study design: one was a matched case control series, and one was a matched cohort study. One study was excluded for having an incorrect intervention and was excluded for comparing the effect of aliquoting on BMAC cell content. One study was excluded for incorrect reporting of outcomes as it did not report raw data for various cell concentrations.

PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) study selection flow diagram. The numbers of screened, excluded, and included studies are shown.
Fig. 1 PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) study selection flow diagram. The numbers of screened, excluded, and included studies are shown.
3.2

3.2 Study quality

Table 1 summarizes study quality based on Methodological Index for Non-Randomized Studies (MINORS) criteria for non-randomized studies.13 Each of the studies included had a prospective, non-randomized study design. The ideal MINORS score for non-comparative studies is 16, with scores ≤8 being the accepted cut-off for poor study quality.13 Each of the included studies had a score >12, indicating moderate to high quality and sufficiently low risk of bias. Of note, none of the included studies had an unbiased assessment of the primary endpoint, and only Landry et al. and Otto et al. scored any points for prospective calculation of sample size for power analysis, which earned them the highest score (13/16) among all included studies.15,16

Table 1 Summary of study quality and risk of bias assessment with Methodological Index for Non-Randomized Studies (MINORS) criteria.
Study (Year) A clearly stated aim Inclusion of consecutive patients Prospective collection of data Endpoints appropriate to the aim of the study Unbiased assessment of the study endpoint Follow-up period appropriate to the aim of the study Loss to follow up less than 5 % Prospective calculation of the study size Total
Anz (2022)11 2 2 2 2 0 2 2 0 12
Anz (2020)17 2 2 2 2 0 2 2 0 12
Badrinath (2014)18 2 2 2 2 0 2 2 0 12
Beitzel (2013)19 2 2 2 2 0 2 2 0 12
Brozovich (2021)20 2 2 2 2 0 2 2 0 12
Cavallo (2023)9 2 2 2 2 0 2 2 0 12
Henrich (2016)21 2 2 2 2 0 2 2 0 12
Hyer (2013)22 2 2 2 2 0 2 2 1 13
Landry (2020)15 2 2 2 2 0 2 2 0 12
McLain (2005)23 2 2 2 2 0 2 2 0 12
Min (2010)24 2 2 2 2 0 2 2 0 12
Muench (2021)25 2 2 2 2 0 2 2 0 12
Narbona-Carceles (2014)26 2 2 2 2 0 2 2 0 12
Otto (2020)16 2 2 2 2 0 2 2 1 13
Pierini (2013)27 2 2 2 2 0 2 2 0 12
3.3

3.3 Study characteristics

Fifteen studies9,11,15–27 totaling 583 patients met inclusion criteria and were included in this systematic review and meta-analysis. These fifteen studies were split into two groups based on BMAC harvest site location, with eleven studies9,11,16–18,21–24,26,27 reporting patients who had BMAC harvested from axial skeleton sites, and ten studies9,11,15,16,19–22,25,26 reporting patients who had BMAC harvested from appendicular skeleton sites. Overall, BMAC harvest sites included axial sites such as the posterior superior iliac spine (PSIS),11,27 anterior superior iliac spine (ASIS),27 iliac crest (not otherwise specified),9,17,21–24,26 “body of the ilium,“16 vertebral body,18,23,24 as well as appendicular sites such as the distal femur,19–21,26 proximal humerus,11,15,16,19,20,25 proximal tibia,9,26 and calcaneal body.22Table 2 summarizes study characteristics of all included studies for patient cohorts with an axial skeleton harvest site including patient demographics, harvest site, cell type, and CFUs. Table 3 summarizes these factors for the appendicular skeleton harvest site cohort. Each study reported values for a different assortment of cell types, each of which are delineated in these two tables.

Table 2 Summary of demographics, cell count, and CFU count for each patient cohort with axial skeleton harvest sites.
Study N Mean Age (SD)(years) Sex (M) Sex (F) Harvest Site Cell Type Mean Cell Count (x106 cells/mL) (SD) Cell Count Range (x106 cells/mL) Mean CFU/mL (SD) CFU/mL Range
Anz 202211 12 64.3 (7.8) 7 5 PSIS TNC 55.9 (52.9) 25.3–86.4 32.5 (33.1) 11.5–53.5
Anz202017 10 23.1 (5.0) 10 0 Iliac Crest HPC 7.4 (4.8) – 446.0 (247.0) –
10 23.1 (5.0) 10 0 Iliac Crest MNC 6.3 (5.8) – 446.0 (247.0) –
Badrinath 201418 7 52.6 (12.0) 2 5 Vertebral Body TNC 11.0 – – –
Cavallo 20239 20 37.9 18 2 Iliac Crest MNC 12.0 (8.0) – 21.7 (23.0) –
Henrich 201621 7 51.0 (median) 5 2 Iliac Crest MNC 1.4 (Median) – 39.0 –
Hyer 201322 40 51.4 (13.3) 18 22 Anterior Iliac Crest TNC 15.6 (38.7) 0.1–222.0 136.4 (141.9) 0–530
McLain 200523 21 59.0 (14.0) 11 10 Vertebral Body TNC 19.8 – – –
21 59.0 (14.0) 11 10 Iliac Crest TNC 17.0 – – –
Min201024 14 54.7 (11.0) 10 4 Vertebral Body MNC 36.5 (20.0) 4.0–84.0 – –
14 54.7 (11.0) 10 4 Iliac Crest MNC 39.7 (20.5) 10.0–92.0 – –
Narbona-Carceles 201426 20 70.9 (2.8) 4 16 Iliac Crest MNC 10.1 (14.4) – – –
20 70.9 (2.8) 4 16 Iliac Crest MSC 0.6 (0.2) – – –
Otto202016 30 30.2 (7.6) 20 10 Body of Ilium TNC 24.0 (5.1) 979.2 (740.3)
Pierini 201327 22 37.5 15 7 ASIS TNC 49.0 (20.8) 18.6–94.2 269.3 (185.1) 80–807
22 37.6 15 7 PSIS TNC 54.7 (27.7) 11.7–121.0 166.4 (133.8) 7–567
22 37.5 15 7 ASIS MNC 186.8 (117.5) 23.6–502.0 – –
22 37.5 15 7 PSIS MNC 214.3 (106.0) 39.4–399.0 – –
Table 3 Summary of demographics, cell count, and CFU count for each patient cohort with appendicular skeleton harvest sites.
Study N Mean Age (years) Sex (M) Sex (F) Harvest Site Cell Type Mean Cell Count (x106 cells/mL) (SD) Cell Count Range (x106 cells/mL) CFU/mL (SD) CFU/mL Range
Anz202211 12 64.3 (7.8) 7 5 Proximal Humerus TNC 18.7 (24.8) 4.4–33.0 3.9 (5.7) 0.3–7.5
Beitzel 201319 29 42.1 (12.0) 16 13 Distal Femur TNC 25.9 (14.3) – 551.3 (408.1) –
55 55.9 (8.9) 36 19 Proximal Humerus TNC 38.7 (52.6) – 883.9 (577.6) –
Brozovich 202120 2 29.0 (6.0) 1 1 Distal Femur MSC 20.0 12.0–25.0 – –
6 58.7 (5.0) 5 1 Proximal Humerus MSC 4.2 0–14.0 – –
Cavallo 20239 20 37.9 18 2 Proximal Tibia MNC 3.0 (2.0) – 2.9 (4.2) –
Henrich 201621 13 48.0 (median) 7 6 Femur MNC 6.8 (Median) – 63.5 –
Hyer201322 40 51.4 (13.3) 18 22 Distal Tibial Metaphysis TNC 5.8 (11.7) 0.1–46.8 15.2 (32.2) 0–130
40 51.4 (13.3) 18 22 Calcaneal Body TNC 7.1 (15.7) 0.1–87.0 5.3 (12.6) 0–60
Landry 202015 92 57.0 64 28 Greater Tuberosity of Humerus TNC 0.1 – 1459.0 (729.0) –
Muench 202125 96 56.2 (7.0) 67 29 Proximal Humerus TNC 26.3 (6.8) – 1421.7 (802.7) 98.0–802.7
Narbona-Carceles 201426 20 70.9 (2.8) 4 16 Distal Femur MNC 0.7 (1.1) – – –
20 70.9 (2.8) 4 16 Distal Femur MSC 0.3 (0.7) – – –
20 70.9 (2.8) 4 16 Proximal Tibia MNC 1.7 (4.8) – – –
20 70.9 (2.8) 4 16 Proximal Tibia MSC 0.3 (0.3) – – –
Otto202016 87 56.8 (7.1) 58 29 Proximal Humerus TNC 27.1 (6.3) – 1516.6 (763.6) –

In the eleven studies that included patients with BMAC harvest sites within the axial skeleton, there were a total of 203 patients with 120 (59.1 %) males and 83 (40.9 %) females.9,11,16–18,21–24,26,27 Across these studies, the mean age ranged from 23.1 to 70.9 years. Cell types collected within harvested samples included TNC, hematopoietic progenitor cells (HPC), and mononuclear cells. Ranges in TNC count per milliliter were reported by three studies (Table 2).11,22,27

In the ten studies that included patients with BMAC harvest sites within the appendicular skeleton, there were a total of 472 patients with 301 (63.8 %) males and 171 (36.2 %) females.9,11,15,16,19–22,25,26 Across these studies, the mean age ranged from 29 to 70.9 years. Cell types collected within harvested samples included mononuclear cells, mesenchymal signaling cells, and TNC. Ranges in TNC count per milliliter were reported by two studies (Table 3).11,22

3.4

3.4 Total nucleated cell comparison

TNC concentration was compared between the appendicular and axial cohorts with subgroup analysis, with pooled axial TNC count calculated to be 38.3 × 106 cells/mL (95 % confidence interval: 22.4–54.1 × 106 cells/mL) and pooled appendicular TNC count calculated to be 20.5 × 106 cells/mL (95 % confidence interval: 14.3–26.6 × 106 cells/mL). The overlap in confidence intervals suggests that there is no significant difference in TNC count between BMAC harvested from the axial versus appendicular skeleton. Fig. 2 displays a forest plot comparing TNC concentrations across the axial and appendicular cohorts with subgroup analysis. The I-squared value of 95.41 % is indicative of a very high level of heterogeneity.28,29

Forest plot comparing TNC concentrations in BMAC harvested from axial versus appendicular harvest sites.
Fig. 2 Forest plot comparing TNC concentrations in BMAC harvested from axial versus appendicular harvest sites.
3.5

3.5 Colony forming unit comparison

In addition, CFU concentration was compared with subgroup analysis, with pooled axial CFU count calculated to be 192.2 CFU/mL (95 % confidence interval:123.8–260.7 CFU/mL) and pooled appendicular CFU count calculated to be 204.7 CFU/mL (95 % confidence interval: 173.4–236.1 CFU/mL). As found with TNC concentration, the overlap in confidence intervals suggests that there is also no a significant difference in CFU concentration between BMAC harvested from the axial versus appendicular skeleton. Fig. 3 displays a forest plot comparing CFU concentrations across the axial and appendicular cohorts with subgroup analysis. The I-squared value of 98.94 % is indicative of a very high level of heterogeneity.28,29

Forest plot comparing CFU concentrations in BMAC harvested from axial versus appendicular harvest sites.
Fig. 3 Forest plot comparing CFU concentrations in BMAC harvested from axial versus appendicular harvest sites.
4

4 Discussion

Overall, this systematic review and meta-analysis found no statistically significant differences between BMAC quality harvested from the axial skeleton versus appendicular skeleton, demonstrating similar concentrations and very high variability of total nucleated cells, mononuclear cells, and colony forming units between the two sites, supporting our hypothesis. More significantly, there was substantial variability in BMAC quantity even across similar harvest sites, both within and across studies, as indicated by I-squared values above 90 % for comparisons of both TNC and CFU concentrations.

A greater number of TNCs within a BMAC sample is often used as a proxy measure for a greater concentration of bone marrow progenitor cells, including connective tissue progenitors that can promote healing post-operatively.30–33 Furthermore, of these TNCs, mononuclear cells are of particular importance as this classification of cell type includes the mesenchymal signaling cells of interest.8,34–36 CFUs are also used as a proxy measure for the number of connective tissue progenitors within the full sample of nucleated cells, as each colony is formed from a singular progenitor cell.37,38 TNC, mononuclear cell count, and CFU concentration are each measurements that can be used to estimate the concentration of the cell types in BMAC that have therapeutic value. In this study, mean TNC concentration across axial sites ranged from 11.0–55.0 × 106 cells/mL, in line with mean TNC concentration across appendicular sites, which ranged from 0.1–38.7 × 106 cells/mL. Similarly, mean CFU concentration across axial sites ranged from 21.7 to 979.2 CFU/mL which was in line with mean CFU concentration across appendicular sites, which ranged from 2.9 to 1516.6 CFU/mL.

Previous studies have established that BMAC is a viable source of MSCs, which promote microcellular environments conducive to healing,1,4,5 due to their ability to differentiate into cartilage and connective tissue.1,4,5 Among the studies included in this meta-analysis, only Brozovich et al. and Narbona-Carceles et al. directly reported MSC concentrations.20,26 Brozovich et al. found a greater range in concentration of MSCs in the distal femur than the proximal humerus; however, it is important to note that this study had a very small sample size of two patients who underwent distal femur BMAC harvest (range 12–25 × 106 cells/mL) and six patients with proximal humerus harvest (range 0–14 × 106 cells/mL).20 Additionally, Narbona-Carceles et al. reported no statistically significant difference in MSC concentration in BMAC extracted from the distal femur (mean 0.3 × 106 cells/mL, standard deviation 0.7 × 106 cells/mL), proximal tibia (mean 0.3 × 106 cells/mL, standard deviation 0.3 × 106 cells/mL), or iliac crest (mean 0.6 × 106 cells/mL, standard deviation 0.2 × 106 cells/mL).26 Brozovich et al. estimated that MSCs accounted for only 0.001 % of the TNC in the entire BMAC sample,20 which corroborates estimates from previous studies that have established that mesenchymal signaling cells account for between 0.001 and 0.02 % of all nucleated cells in any given sample of isolated bone marrow aspirate.39–41

In addition to being a relatively robust source of MSCs, BMAC is a rich source of heterogeneous mononuclear cell types.30,31,33 In particular, the mononuclear components of BMAC consists of osteogenic progenitor cells that facilitate regeneration of musculoskeletal components, including osteoblasts, fibroblasts, lymphocytes, macrophages, pericytes, and endothelial progenitor cells.30,31,33 There were extremely high levels of variability in the reports of mean cell concentration in the axial skeleton cohort. Mononuclear cell counts from axial sites ranged from means of 6.3–214.3 × 106 cells/mL. However, these values were in line with the mononuclear cell concentrations reported in appendicular cohort, with means ranging from 0.3–3.0 × 106 cells/mL.9,21,26

Understanding how the cell concentration of BMAC harvest influences recovery and patient outcomes may shed light on the importance of whether harvesting BMAC from the axial or appendicular skeleton provides clinically significant differences. A 2002 prospective study investigating BMAC for use in hip arthroplasty found that a greater number of transplanted progenitor cells was significantly correlated with a decrease in arthroplasty failure rates.42 Our results suggest that BMAC harvested from both the axial skeleton and appendicular skeleton had high variability in TNCs and CFUs and that no significant difference exists in TNC or CFU count between the axial and appendicular skeleton. Surgeons may elect to harvest BMAC from a site that is close to the operative site, which would reduce patient morbidity and decrease time of surgery without sacrificing cell count. The high levels of objective heterogeneity as measured by I-squared value in this study are indicative of a need for further nuanced studies with large sample sizes and more robust study designs that explicitly compare TNC and CFU within axial and appendicular harvest sites. Further prospective studies should be conducted to better identify differences in patient reported outcomes and clinical complication rates when BMAC is harvested from the axial versus appendicular skeleton.

4.1

4.1 Limitations

This study is not without limitations. There are large ranges in cell concentration and type of cell count reported across each of the studies included. Furthermore, ranges and standard deviations are not reported for all types of cells across all included studies, and there was heterogeneity among included studies with regards to specific harvest site within the axial or appendicular skeletons. These factors limit the definitive comparisons that can be made regarding TNC, CFU, MSC, and mononuclear cell counts on the basis of axial versus appendicular harvest site. In particular, many studies that reported TNC or CFU concentrations could not be included in the subgroup analysis performed in this study because they did not report standard deviation or ranges, which could have affected the pooled mean cell counts and the comparison between the axial and appendicular cohorts. Additionally, there was insufficient data to perform subgroup analysis of MSC and mononuclear cell counts on the basis of axial versus appendicular harvest site. While prior literature has identified differences in BMAC cell composition on the basis of age, sex, and medical comorbidities, these factors were not evaluated in the scope of our systematic review and meta-analysis. We also included studies which utilized various BMAC collection and preparation techniques, which undoubtedly have a large impact on MSC quantity and viability.

4.2

4.2 Conclusions

BMAC harvested from the axial and appendicular skeletons demonstrate significant variability in progenitor cell concentration. Harvesting at appendicular sites near the operative location allows the surgeon to extract sufficient quality BMAC as compared to harvest sites within the axial skeleton, such as the iliac crest.

CRediT authorship contribution statement

Udit Dave: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing. Jared Rubin: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing. Harshal Shah: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing. Cameron Gerhold: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing. Johnathon R. McCormick: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing. Andrew S. Bi: Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing. Catherine Yuh: Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing. Luciano A. Rossi: Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing. Jorge Chahla: Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing.

Submission declaration

This study has not been previously published, is not under consideration for publication elsewhere, is approved by all authors and tacitly or explicitly by the responsible authorities where the work was carried out, and that, if accepted, it will not be published elsewhere in the same form, in English or in any other language, including electronically without the written consent of the copyright-holder.

Data availability statement

There is no supplemental data or online material pertaining to this manuscript. We have included the search terms utilized in the manuscript.

Ethical statement

This study is a systematic review and so no research was done with human or animal subjects, not applicable.

Guardian/Patient's consent statement

This study is a systematic review, this is not applicable.

Funding statement

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

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