Multilevel Analysis of the Neovascularization and Integration Process of a Nonvascularized Rectus Fascia Transplantation

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Abstract

Background.

Failure to close the abdominal wall after intestinal transplantation (ITx) or multivisceral Tx remains a surgical challenge. An attractive method is the use of nonvascularized rectus fascia (NVRF) in which both layers of the donor abdominal rectus fascia are used as an inlay patch without vascular anastomosis. How this graft integrates over time remains unknown. The study aims to provide a multilevel analysis of the neovascularization and integration process of the NVRF.

Methods.

Three NVRF-Tx were performed after ITx. Clinical, radiological, histological, and immunological data were analyzed to get insights into the neovascularization and integration process of the NVRF. Moreover, cryogenic contrast-enhanced microfocus computed tomography (microCT) analysis was used for detailed reconstruction of the vasculature in and around the NVRF (3-dimensional histology).

Results.

Two men (31- and 51-y-old) and 1 woman (49-y-old) underwent 2 multivisceral Tx and 1 combined liver-ITx, respectively. A CT scan showed contrast enhancement around the fascia graft at 5 days post-Tx. At 6 weeks, newly formed blood vessels were visualized around the graft with Doppler ultrasound. Biopsies at 2 weeks post-Tx revealed inflammation around the NVRF and early fibrosis. At 6 months, classical 2-dimensional histological analysis of a biopsy confirmed integration of the fascia graft with strong fibrotic reaction without signs of rejection. A cryogenic contrast-enhanced microCT scan of the same biopsy revealed the presence of microvasculature, enveloping and penetrating the donor fascia.

Conclusions.

We showed clinical, histological, and microCT evidence of the neovascularization and integration process of the NVRF after Tx.

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Most cited references 29

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Simultaneous three-dimensional visualization of mineralized and soft skeletal tissues by a novel microCT contrast agent with polyoxometalate structure.

Greet Kerckhofs, Steve Stegen, Nick van Gastel … (2018)

Biological tissues have a complex and heterogeneous 3D structure, which is only partially revealed by standard histomorphometry in 2D. We here present a novel chemical compound for contrast-enhanced microfocus computed tomography (CE-CT), a Hafnium-based Wells-Dawson polyoxometalate (Hf-POM), which allows simultaneous 3D visualization of mineralized and non-mineralized skeletal tissues, such as mineralized bone and bone marrow vasculature and adipocytes. We validated the novel contrast agent, which has a neutral pH in solution, by detailed comparison with (immuno)histology on murine long bones as blueprint, and showed that Hf-POM-based CE-CT can be used for virtual 3D histology. Furthermore, we quantified the 3D structure of the different skeletal tissues, as well as their spatial relation to each other, during aging and diet-induced obesity. We discovered, based on a single CE-CT dataset per sample, clear differences between the groups in bone structure, vascular network organization, characteristics of the adipose tissue and proximity of the different tissues to each other. These findings highlight the complementarity and added value of Hf-POM-based CE-CT compared to standard histomorphometry. As this novel technology provides a detailed 3D simultaneous representation of the structural organization of mineralized bone and bone marrow vasculature and adipose tissue, it will enable to improve insight in the interactions between these three tissues in several bone pathologies and to evaluate the in vivo performance of biomaterials for skeletal regeneration.

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Transplantation of the abdominal wall.

Juan Madariaga, Allan Levi, Seigo Nishida … (2003)

Closure of the abdomen in patients undergoing intestinal transplantation can be extremely difficult, if not impossible. We describe our initial experience with abdominal wall allotransplantation to facilitate abdominal closure. We undertook nine cadaveric abdominal wall composite allograft transplants in eight patients. The graft's blood supply was based on the inferior epigastric vessels left in continuity with the donor femoral and iliac vessels. Skin biopsies were undertaken randomly and when rejection was suspected. Vessel patency was monitored by doppler ultrasound. Six patients have survived, five of whom have intact, viable abdominal wall grafts. Two patients have had a clinically mild episode of acute rejection of the skin of the abdominal wall that resolved with corticosteroid therapy. No clinically apparent graft-versus-host disease has been noted. Transplantation of an abdominal wall composite allograft can facilitate reconstruction and closure of the abdominal compartment in intestinal transplant recipients with complex abdominal wall defects.

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Negative pressure wound therapy promotes vessel destabilization and maturation at various stages of wound healing and thus influences wound prognosis

ZHANJUN MA, KANGQUAN SHOU, Zonghuan Li … (2016)

Negative pressure wound therapy (NPWT) has been observed to accelerate the wound healing process in humans through promoting angiogenesis. However, the potential biological effect and relevant molecular mechanisms, including microvessel destabilization, regression and endothelial cell proliferation in the early stage (1–3 days), and the neovascular stabilization and maturation in the later stage (7–15 days), have yet to be fully elucidated. The current study aimed to research the potential effect of NPWT on angiogenesis and vessel maturation, and investigate relevant association between mature microvessels and wound prognosis, as well as the regulatory mechanisms in human wound healing. Patients in the present study (n=48) were treated with NPWT or a petrolatum gauze, and relevant growth factors and vessel changes were detected using various experimental methods. NPWT increased the expression levels of angiogenin-2 (Ang-2), and decreased the expression levels of Ang-1 and ratios of Ang-1/Ang-2 in the initial stages of wound healing. However, in the latter stages of wound healing, NPWT increased the expression levels of Ang-1 and ratios of Ang-1/Ang-2, as well as the phosphorylation level of tyrosine kinase receptor-2. Consequently, microvessel pericyte coverage was gradually elevated, and the basement membrane was gradually supplied with new blood at the later stage of wound healing. In conclusion, NPWT may preferentially stimulate microvessel destabilization and regression in the early stage of wound healing, and as a consequence, increase angiogenesis. Subsequently, in the later stage of wound healing, NPWT may preferentially promote microvessel stabilization, thereby promoting microvessel maturation in human wounds through the angiogenin/tyrosine kinase receptor-2 signaling pathway. The results of the present study results demonstrated that NPWT was able to accelerate wound healing speed, and thus influence wound prognosis, as a result of an abundance of mature microvessels in human wounds.

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Author and article information

Contributors

Ewout Muylle:

ORCID: https://orcid.org/0000-0002-0646-2615

Arne Maes:

ORCID: https://orcid.org/0000-0002-1488-5079

Gert De Hertogh:

ORCID: https://orcid.org/0000-0001-8494-7725

Nele Van De Winkel:

ORCID: https://orcid.org/0000-0003-4862-478X

Greet Kerckhofs:

ORCID: https://orcid.org/0000-0002-1750-8324

Antoine Dubois:

ORCID: https://orcid.org/0000-0002-2839-8896

Vincent Vandecaveye:

ORCID: https://orcid.org/0000-0002-0800-3279

Lieven Thorrez:

ORCID: https://orcid.org/0000-0002-5896-6823

Ina Hennion:

ORCID: https://orcid.org/0000-0002-0360-5385

Marie-Paule Emonds:

ORCID: https://orcid.org/0000-0002-2653-8656

Steven Pans:

ORCID: https://orcid.org/0000-0003-0176-454X

Nathalie P. Deferm

Diethard Monbaliu:

ORCID: https://orcid.org/0000-0002-0506-1609

Emilio Canovai:

ORCID: https://orcid.org/0000-0003-4921-466X

Tim Vanuytsel:

ORCID: https://orcid.org/0000-0001-8728-0903

Jacques Pirenne:

ORCID: https://orcid.org/0000-0002-8147-8801

Journal

Journal ID (nlm-ta): Transplant Direct

Journal ID (iso-abbrev): Transplant Direct

Journal ID (publisher-id): TXD

Title: Transplantation Direct

Publisher: Lippincott Williams & Wilkins (Hagerstown, MD )

ISSN (Electronic): 2373-8731

Publication date (Electronic): 15 May 2024

Publication date Collection: June 2024

Volume: 10

Issue: 6

Electronic Location Identifier: e1624

Affiliations

[1 ] Leuven Intestinal Failure and Transplantation (LIFT) Center, University Hospitals Leuven, Leuven, Belgium.

[2 ] Department of Abdominal Transplant Surgery, University Hospitals Leuven, Leuven, Belgium.

[3 ] Department of Chronic Diseases and Metabolism, Laboratory of Respiratory Diseases and Thoracic Surgery (BREATHE), KU Leuven, Leuven, Belgium.

[4 ] Department of Materials Engineering, KU Leuven, Leuven, Belgium.

[5 ] Biomechanics Lab, Institute of Mechanics, Materials and Civil Engineering, UCLouvain, Louvain-la-Neuve, Belgium.

[6 ] Pole of Morphology, Institute of Experimental and Clinical Research, UCLouvain, Brussels, Belgium.

[7 ] Department of Pathology, University Hospitals Leuven, Leuven, Belgium.

[8 ] Unit of Translational Cell- and Tissue Research, Department of Imaging and Pathology, KU Leuven, Leuven, Belgium.

[9 ] Department of Abdominal Surgery, University Hospitals Leuven, Leuven, Belgium.

[10 ] Department of Development and Regeneration, Unit of Urogenital, Abdominal and Plastic Surgery, KU Leuven, Leuven, Belgium.

[11 ] Prometheus Division of Skeletal Tissue Engineering, KU Leuven, Leuven, Belgium.

[12 ] Department of Microbiology, Immunology and Transplantation, KU Leuven, Leuven, Belgium.

[13 ] Department of Radiology, University Hospitals Leuven, Leuven, Belgium.

[14 ] Translational MRI Unit, Department of Imaging and Pathology, KU Leuven, Leuven, Belgium.

[15 ] Tissue Engineering Lab, Department of Development and Regeneration, KU Leuven, KULAK campus Kortrijk, Kortrijk, Belgium.

[16 ] Histocompatibility and Immunogenetics Laboratory, Belgian Red Cross-Flanders, Mechelen, Belgium.

[17 ] Department of Abdominal Surgery, Sint-Franciscusziekenhuis, Heusden-Zolder, Belgium.

[18 ] Nuffield Department of Surgical Sciences, University of Oxford, Oxford, United Kingdom.

[19 ] Department of Gastroenterology and Hepatology, University Hospitals Leuven, Leuven, Belgium.

[20 ] Department of Chronic Diseases and Metabolism, Translational Research Center for Gastrointestinal Disorders (TARGID), KU Leuven, Leuven, Belgium.

[21 ] Department of Thoracic Surgery, University Hospitals Leuven, Leuven, Belgium.

Author notes

Correspondence: Laurens J. Ceulemans, MD, PhD, Department of Thoracic Surgery and Lung Transplantation, University Hospitals Leuven/KU Leuven, Herestraat 49, 3000 Leuven, Belgium. ( laurens.ceulemans@ 123456uzleuven.be ); LinkedIn: www.linkedin.com/in/laurens-ceulemans-1190a7a1; Twitter: @CeulemansLJ.

Author information

Ewout Muylle https://orcid.org/0000-0002-0646-2615

Arne Maes https://orcid.org/0000-0002-1488-5079

Gert De Hertogh https://orcid.org/0000-0001-8494-7725

Nele Van De Winkel https://orcid.org/0000-0003-4862-478X

Greet Kerckhofs https://orcid.org/0000-0002-1750-8324

Antoine Dubois https://orcid.org/0000-0002-2839-8896

Vincent Vandecaveye https://orcid.org/0000-0002-0800-3279

Lieven Thorrez https://orcid.org/0000-0002-5896-6823

Ina Hennion https://orcid.org/0000-0002-0360-5385

Marie-Paule Emonds https://orcid.org/0000-0002-2653-8656

Steven Pans https://orcid.org/0000-0003-0176-454X

Diethard Monbaliu https://orcid.org/0000-0002-0506-1609

Emilio Canovai https://orcid.org/0000-0003-4921-466X

Tim Vanuytsel https://orcid.org/0000-0001-8728-0903

Jacques Pirenne https://orcid.org/0000-0002-8147-8801

Laurens J. Ceulemans https://orcid.org/0000-0002-4261-7100

Article

Publisher ID: TXD-2024-0016 Accession ID: 00007

DOI: 10.1097/TXD.0000000000001624

PMC ID: 11098214

PubMed ID: 38757048

SO-VID: 03d9de83-1a5e-4eb3-a75c-d846cccbbc3c

License:

This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

History

Date received : 22 January 2024

Date accepted : 05 February 2024

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Multilevel Analysis of the Neovascularization and Integration Process of a Nonvascularized Rectus Fascia Transplantation

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Abstract

Background.

Methods.

Results.

Conclusions.

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Most cited references 29

Simultaneous three-dimensional visualization of mineralized and soft skeletal tissues by a novel microCT contrast agent with polyoxometalate structure.

Transplantation of the abdominal wall.

Negative pressure wound therapy promotes vessel destabilization and maturation at various stages of wound healing and thus influences wound prognosis

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Contributors

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Author notes

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