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Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component
Open accessAbstract
Recently, macrophages have been characterized as having an M1 or M2 phenotype based on receptor expression, cytokine and effector molecule production, and function. The effects of macrophage phenotype upon tissue remodeling following the implantation of a biomaterial are largely unknown. The objectives of this study were to determine the effects of a cellular component within an implanted extracellular matrix (ECM) scaffold upon macrophage phenotype, and to determine the relationship between macrophage phenotype and tissue remodeling. Partial-thickness defects in the abdominal wall musculature of Sprague-Dawley rats were repaired with autologous body wall tissue, acellular allogeneic rat body wall ECM, xenogeneic pig urinary bladder tissue, or acellular xenogeneic pig urinary bladder ECM. At 3, 7, 14, and 28 days the host tissue response was characterized using histologic, immunohistochemical, and RT-PCR methods. The acellular test articles were shown to elicit a predominantly M2 type response and resulted in constructive remodeling, while those containing a cellular component, even an autologous cellular component, elicited a predominantly M1 type response and resulted in deposition of dense connective tissue and/or scarring. We conclude that the presence of cellular material within an ECM scaffold modulates the phenotype of the macrophages participating in the host response following implantation, and that the phenotype of the macrophages participating in the host response appears to be related to tissue remodeling outcome.
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“What is more, it is widely accepted that during the degradation of implanted ECM bioscaffolds, ECM components are released into the environment and promote the transition to a remodeling phase [18,44,74,78].”
From Immune Response to Extracellular Matrix Bioscaffolds: A Comprehensive Review (2025) · cites this paper as [74]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Mechanistically, inadequate decellularization retains high amounts of damage-associated molecular patterns (DAMPs) or endotoxin, and excessive crosslinking biases macrophages toward pro-inflammatory phenotypes that drive fibrosis and poor remodeling [73,74].”
From Immune Response to Extracellular Matrix Bioscaffolds: A Comprehensive Review (2025) · cites this paper as [74]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Immunohistochemical and gene expression analysis using CCR7 and iNOS for M1 and CD163 and Arg for M2 macrophages revealed that cellular scaffolds had a majority of M1 phenotype and provided a dense, poorly organized collagenous FBC, while decellularized scaffolds favored the M2 phenotype, and displayed both neomatrix formation and early angiogenesis.”
From Unraveling and Harnessing the Immune Response at the Cell–Biomaterial Interface for Tissue Engineering Purposes (2024) · cites this paper as [180]
Experimental — accuracy not yet measuredIn the citing paper
“Recognition of the predominant MΦ phenotypic profile can provide a tool by which a tissue regenerative outcome can be predicted and possibly promoted [4].”
From Macrophage functional polarization (M1/M2) in response to varying fiber and pore dimensions of electrospun scaffolds (2013) · cites this paper as [4]
In the citing paper
“Brown et al. [83], who demonstrated that the presence of even an autologous cellular component attracted M1 cells, which was not observed in cell free constructs.”
From Biomaterial based modulation of macrophage polarization: a review and suggested design principles (2015) · cites this paper as [83]
In the citing paper
“Briefly, scaffold materials composed of extracellular matrix (ECM) have been shown to promote a switch from a predominantly M1 cell population immediately following implantation to a population enriched in M2 cells by 7–14 days post implantation [154–156].”
From Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine (2012) · cites this paper as [156]
In the citing paper
“This constructive remodeling response has been directly linked to the ability of the material to modulate macrophage phenotype [154–157].”
From Macrophage polarization: an opportunity for improved outcomes in biomaterials and regenerative medicine (2012) · cites this paper as [156]
In the citing paper
“Here we find that MΦ activation depends on biomaterial architecture in addition to previously implicated biomaterial chemistry and bioactivity (34–36).”
From Proangiogenic scaffolds as functional templates for cardiac tissue engineering (2010) · cites this paper as [34]
In the citing paper
“Previous in vivo studies demonstrated concurrent expression of M1 and M2 markers (37), and enhanced expression of M2 markers has been associated with improved outcomes for implanted biologic scaffolds (34).”
From Proangiogenic scaffolds as functional templates for cardiac tissue engineering (2010) · cites this paper as [34]
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Citations
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Self-citationBubaline Diaphragm Matrix: Development and Clinical Assessment into Cattle Abdominal Hernia Repair
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“Effective removal of the antigen associated with cell membranes and intracellular components of tissues is necessary to avoid or minimize an adverse immunologic response by xenogenic recipients [4,5].”
Backgrounddo Amaral, D. L. A. S., Zanette, R. D. S. S., de Souza, G. T., da Silva, S. A., de Aguiar, J. A. K., Marcomini, R. F., do Carmo, A. M. R., Nogueira, B. V., Barros, R. J. D. S., Silva, F. D. S., et al. (2020) · Biologicals · doi:10.1016/j.biologicals.2020.06.003 · Cited by 9
Bone Tissue Engineering: Latest Trends and Future Perspectives
Pathak, R. (2015) · Advances in Animal and Veterinary Sciences · doi:10.14737/journal.aavs/2015/3.4s.9.22 · Cited by 9
Fusaro, L., Gualandi, C., Antonioli, D., Soccio, M., Liguori, A., Laus, M., Lotti, N., Boccafoschi, F., & Focarete, M. L. (2020) · Biomolecules · doi:10.3390/biom10121620 · Cited by 9
“The primary requirement to be satisfied is the minimization of the risk of rejection or failure in order to avoid inflammatory responses [2,3].”
BackgroundGroth, D., Poplawska, I., Tynecka, M., Grubczak, K., Holl, J., Starosz, A., Janucik, A., Borkowska, K., Juchniewicz, D., Hady, H. R., et al. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13122118 · Cited by 9
Miyachi, H., Tara, S., Nakayama, H., Hama, R., Sugiura, T., Reinhardt, J. W., Yi, T., Lee, Y., Lee, A. Y., Miyamoto, S., et al. (2024) · Acta Biomaterialia · doi:10.1016/j.actbio.2024.05.055 · Cited by 8
Numerical modelling of osteocyte growth on different bone tissue scaffolds
Paz, C., Suárez, E., Gil, C., & Parga, O. (2021) · Computer Methods in Biomechanics & Biomedical Engineering · doi:10.1080/10255842.2021.1972290 · Cited by 8
“…et al. 2015) Qm 1.86 10 18mol/(cells s) (Ho and Chung Ca 2009) Cm 0.006mol/m 3 (Babensee et al. 1998) #maxcell 1.5281 10 5 s 1 (Estrada et al. 2006; Brown et al. 2009) Kc 0.006 (Estrada et al. 2006; Brown et al. 2009) qc 1020 kg/m 3 (Estrada et al. 2006) Vcell 2.5 10 18 m3 (Brown et al.…”
InfluentialBanerjee, D., Nayakawde, N. B., Antony, D., Deshmukh, M. V., Ghosh, S., Sihlbom, C., Berger, E., Haq, U. U., & Olausson, M. (2021) · Tissue Engineering Part A · doi:10.1089/ten.tea.2021.0146 · Cited by 8
Nguyen, H.-Q.-D., Kao, C., Chiang, C., Hung, Y.-H., & Lo, C. (2022) · Gels · doi:10.3390/gels8030187 · Cited by 8
“indicated that, compared to cellular autografts, decellularized urinary bladder matrix (UBM) allografts promoted anti-inflammatory macrophage polarization and reduced fibrotic response to abdominal wall implants in rats [17].”
ResultDurand, M., Oger, M., Nikovics, K., Venant, J., Guillope, A.-C., Jouve, E., Barbier, L., Bégot, L., Poirier, F., Rousseau, C., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10123017 · Cited by 8
Majidi, M., Pakzad, S., Salimi, M., Azadbakht, A., Hajighasemlou, S., Amoupour, M., Nokhbedehghan, Z., Bonakdar, S., Sepehr, K. S., Chauhan, N. P. S., et al. (2023) · Biotechnology and Bioengineering · doi:10.1002/bit.28546 · Cited by 8
“…al., 2013; Tay et al., 2013) that play an essential role in the success or failure of biomaterial implantation and more importantly wound healing (Brown et al., 2009; Greisler, 1987, 1988; Greisler et al., 1988, 1989, 1991; Koh & DiPietro, 2011; Roh et al., 2008; Valentin et al., 2009; Wu et…”
BackgroundGothard, D., Rotherham, M., Smith, E. L., Kanczler, J. M., Henstock, J. R., Wells, J. A., Roberts, C., Qutachi, O., Peto, H., Rashidi, H., et al. (2024) · Mechanobiology in Medicine · doi:10.1016/j.mbm.2024.100096 · Cited by 8
“32,33 Hydrogel constructs in the present study were prepared as previously described.”
Wang, R. M., He, J., Xu, Y., & Christman, K. L. (2017) · Drug Discovery Today Disease Models · doi:10.1016/j.ddmod.2018.06.002 · Cited by 7
Role of Stem Cells and Extracellular Matrix in the Regeneration of Skeletal Muscle
Dunn, A. J., Marcinczyk, M., Talovic, M., Patel, K., Haas, G. J., & Garg, K. (2018) · InTech eBooks · doi:10.5772/intechopen.75828 · Cited by 8
Extracellular matrix hydrogel derived from bovine bone is biocompatible in vitro and in vivo
Ayala-Ham, A., Aguilar‐Medina, M., León-Félix, J., Romero-Quintana, J. G., Bermúdez, M., López-Gutierrez, J., Jiménez-Gastélum, G., Avendaño-Félix, M., Lizárraga-Verdugo, E. R., Castillo-Ureta, H., et al. (2022) · Bio-Medical Materials and Engineering · doi:10.3233/bme-211387 · Cited by 8
“The presence of cellular remanents has been linked with macrophage polarization profile to M1 and pro-inflammatory phenotype [27].”
New advances in liver decellularization and recellularization: innovative and critical technologies
Lin, Y.-Q., Wang, L., Wang, J., Pan, L., Zhu, G., Liu, W., Braddock, M., & Zheng, M. (2015) · Expert Review of Gastroenterology & Hepatology · doi:10.1586/17474124.2015.1058155 · Cited by 9
Sex as a determinant of age-related changes in rat spinal cord inflammation-oxidation state
Nacka-Aleksić, M., Stojanović, M., Simic, L., Bufan, B., Kotur‐Stevuljević, J., Stojić-Vukanić, Z., Dimitrijević, M., Ražić, S., & Leposavić, G. (2017) · Biogerontology · doi:10.1007/s10522-017-9726-4 · Cited by 9
“…of two target genes in a sample was compared according to the following equation: 2 dCtgene X 2 dCtgene Y Values were then plotted on a log scale such that values [1.0 represented a predominance of X gene expression and values\1.0 represented a predominance of Y gene expression (Brown et al. 2009).”
InfluentialChambers, K. L., Myerscough, M. R., Watson, M. G., & Byrne, H. M. (2024) · Bulletin of Mathematical Biology · doi:10.1007/s11538-024-01342-9 · Cited by 7
Recent Advances and Applications of Chitin and Chitosan Hydrogel Scaffolds in Tissue Engineering
Abdel-Mohsen, A. M., Abdel-Rahman, R. M., & Skotnicová, K. (2026) · Gels · doi:10.3390/gels12050427 · Cited by 7
Anand, M., Bhagania, M. K., & Kaur, K. (2023) · Archives of Aesthetic Plastic Surgery · doi:10.14730/aaps.2022.00710 · Cited by 8
Effectiveness of Biologic Factors in Shoulder Disorders
Giotis, D., Aryaei, A., Vasilakakos, T., & Paschos, N. K. (2017) · The Open Orthopaedics Journal · doi:10.2174/1874325001711010163 · Cited by 7
“[169] Brown BN, Valentin JE, Stewart-Akers AM, McCabe GP, Badylak SF.”
Functionalization of soft materials for cardiac repair and regeneration
Kuraitis, D., Hosoyama, K., Blackburn, N. J. R., Deng, C., Zhong, Z., & Suuronen, E. J. (2019) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2019.1572587 · Cited by 7
“grated into the functional tissue [85].”
Scleral defect repair using decellularized porcine sclera in a rabbit model
Wang, F., Zhao, L., Li, H., Li, D., Zhou, M., Zhou, Q., & Xie, L. (2020) · Xenotransplantation · doi:10.1111/xen.12633 · Cited by 8
Al‐Maawi, S., Wang, X., Sader, R., Götz, W., Motta, A., Migliaresi, C., Kirkpatrick, C. J., & Ghanaati, S. (2021) · Materials · doi:10.3390/ma14144038 · Cited by 8
“Macrophages and lymphocytes, as part of the immune system, play a crucial role in wound healing and the biomaterial-based regeneration process [17,18].”
BackgroundBiomaterials from Decellularized Tissues
Londoño, R., & Badylak, S. F. (2016) · Wiley eBooks · doi:10.1002/9781119126218.ch12 · Cited by 7
Self-citationImmune Response to Extracellular Matrix Bioscaffolds: A Comprehensive Review
Romero, D. J., Hussey, G., & Capella-Monsonís, H. (2025) · Biologics · doi:10.3390/biologics5030028 · Cited by 7
“They have demonstrated therapeutic potential across a variety of clinical and preclinical applications, including abdominal wall reconstruction [57,74,82], musculoskeletal repair [64,83,84], cardiac tissue regeneration [84–86], bladder augmentation [87,88], and esophageal repair [89–91], among…”
Bioengineering liver tissue by repopulation of decellularised scaffolds
Afzal, Z., & Huguet, E. (2023) · World Journal of Hepatology · doi:10.4254/wjh.v15.i2.151 · Cited by 6
Wang, T., Liao, S., Lu, P., He, Z., Cheng, S., Wang, T., Cheng, Z., An, Y., Wang, M., & Shu, C. (2024) · Materials Today Bio · doi:10.1016/j.mtbio.2024.101402 · Cited by 6
“Macrophages may stimulate cell migration into the grafts and regulate cell function and graft remodeling [25,75,76].”
Palai, D., Yasue, H., Ito, S., Komatsu, H., Taguchi, T., & Nishiguchi, A. (2025) · Biomaterials Science · doi:10.1039/d5bm00394f · Cited by 7
Zelus, E. I., Grime, J., Saviola, A. J., McCabe, M. C., Hansen, K. C., Alperin, M., & Christman, K. L. (2025) · Advanced Materials · doi:10.1002/adma.202419977 · Cited by 5
Immunomodulatory role of decellularized extracellular matrix in skin wound healing
Savitri, C., Park, H. S., Kim, Y., Jang, Y.-J., Hyun, J., Lee, D., Kang, M., Park, K. M., Bhang, S. H., & Park, K. (2025) · Materials Today Bio · doi:10.1016/j.mtbio.2025.102672 · Cited by 7
“…(ECM) has gained attention for its structural and bioactive components, which modulate immune responses and guide cell behavior [5 – 11 , 42 – 49 To overcome this, researchers have loaded nanofibers with growth factors such as vascular endothelial growth factor (VEGF), platelet-derived…”
InfluentialBebiano, L. B., Presa, R., Silva, I. V., Oliveira, A. L., Costa, J. B., & Pereira, R. F. (2023) · Journal of 3D Printing in Medicine · doi:10.2217/3dp-2023-0011 · Cited by 7
Sarangi, A. K., Salem, M. A., Younus, M. D., El-Haroun, H., Mahal, A., Tripathy, L., Mishra, R., Shabil, M., Alhumaydhi, F. A., Khatib, M. N., et al. (2024) · International Journal of Surgery · doi:10.1097/js9.0000000000002110 · Cited by 9
“An unfavourable host remodelling response occurs when the cellular material from the source tissue does not remove completely [263 – 266] .”
Biomaterial Strategies of Macrophage Behaviour in Bone Regeneration
Chocholata, P. K., Dvořáková, J., Babuška, V., & Čedíková, M. (2025) · Regenerative Engineering and Translational Medicine · doi:10.1007/s40883-025-00443-8 · Cited by 7
Bone Marrow-Derived Macrophages Enhance Vessel Stability in Modular Engineered Tissues
West, M. E. D., Sefton, E., & Sefton, M. (2019) · Tissue Engineering. Part A · doi:10.1089/ten.tea.2018.0222 · Cited by 5
Sahoo, S., Ma, J., Tastaldi, L. G., Baker, A. R., Loftis, J., Rosen, M. J., & Derwin, K. A. (2019) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.34357 · Cited by 6
Bioengineering and regeneration of gastrointestinal tissue: where are we now and what comes next?
Zakhem, E., Raghavan, S. A., Suhar, R. A., & Bitar, K. N. (2019) · Expert Opinion on Biological Therapy · doi:10.1080/14712598.2019.1595579 · Cited by 6
“their ability to promote reconstructive remodeling [51].”
Kanda, H., Ando, D., Oya, K., Diono, W., & Goto, M. (2021) · Arabian Journal of Chemistry · doi:10.1016/j.arabjc.2021.103280 · Cited by 6
Jiménez-Gastélum, G., Ramos‐Payán, R., López-Gutiérrez, J., Ayala-Ham, A. D. R., Silva-Benítez, E. D. L., Bermúdez, M., Romero-Quintana, J. G., Sánchez‐Schmitz, G., & Aguilar‐Medina, M. (2023) · Bio-Medical Materials and Engineering · doi:10.3233/bme-221450 · Cited by 6
Current Trends in the Development of Materials for Bone Grafting and Spinal Fusion (Review)
Bokov, A., Mlyavykh, S. G., Shirokova, N. Y., Davydenko, D. V., & Orlinskaya, N. Y. (2018) · Современные технологии в медицине · doi:10.17691/stm2018.10.4.24 · Cited by 6
“Such an immune response leads to rejection of the bone-substituting material [34, 35].”
Background
Metadata
- Authors
- Brown, B. N., Valentin, J. E., Stewart-Akers, A. M., McCabe, G. P., & Badylak, S. F.
- Affiliations
- University of Pittsburgh (US)
- Purdue University West Lafayette (US)
- Corresponding author
- Badylak, Stephen F.
- Venue
- Biomaterials
- Publisher
- Elsevier BV
- Published
- 2009-03
- Volume
- 30
- Issue
- 8
- Pages
- 1482-1491
- ISSN
- 0142-9612 (ISSN-L)
- PMC
- PMC2805023
- OpenAlex
- W1999579326
- Cited by
- 896
- References
- 38
- Citations by year
- 2026: 23 · 2025: 28 · 2024: 37 · 2023: 46 · 2022: 61 · 2021: 73 · 2020: 47 · 2019: 69 · 2018: 63 · 2017: 73 · 2016: 59 · 2015: 70 · 2014: 76 · 2013: 60 · 2012: 38
- FWCI
- 36.84
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biomaterials (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Biomedical Imaging and Bioengineering (F31EB007914)
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Health Sciences › Medicine › Surgery › Wound Healing and Treatments
- Physical Sciences › Engineering › Biomedical Engineering › Bone Tissue Engineering Materials
- Keywords
- macrophage phenotype, macrophage polarization, tissue remodeling, extracellular matrix scaffolds, acellular scaffolds, cellular scaffolds, host tissue response, scar formation, connective tissue deposition
- MeSH terms
- Animals, Cell Nucleus, Gene Expression Regulation, Immunohistochemistry, Indoles, Macrophages, Phenotype, Transplantation, Autologous, Transplantation, Heterologous, Transplantation, Homologous, Rats, Sprague-Dawley, Muscle, Skeletal, Prosthesis Implantation, Sus scrofa, Rats, Tissue Scaffolds
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