Cited by 39Lymphatic System and DiseasesLymphatic Disorders and TreatmentsParasitic Diseases Research and Treatment

The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.

Phenotypic modulation of smooth muscle cells in lymphoedema

Ogata, F., Fujiu, K., Koshima, I., Nagai, R., Manabe, I.·2015·British Journal of Dermatology

Abstract

Background Lymphoedema is a debilitating progressive condition that is frequently observed following cancer surgery and severely restricts quality of life. Although it is known that lymphatic dysfunction and obstruction underlie lymphoedema, the pathogenic mechanism is poorly understood. Smooth muscle cells (SMCs) play pivotal roles in the pathogenesis of various vascular diseases, including atherosclerosis. Objectives We analysed SMCs in lymphatic vessels from the lymphoedematous legs of 29 patients. Methods Expression of smooth muscle α-actin (SMαA) and smooth muscle myosin heavy chain (SM-MHC) isoforms SM1 and SM2 was investigated using immunohistochemistry. Results Compared with normal lymphatic vessels, all affected lymphatic vessels in chronic lymphoedema showed marked wall thickening. In addition to increases in the numbers of rows of SMαA(+) SM1(+) SMCs in the tunica media, SMCs were also observed in the subendothelial region (tunica intima). While most intimal and medial cells were positive for SMαA and SM1, staining for SM1 and particularly SM2, a marker of mature SMCs, progressively declined in lymphatic vessels in increasingly severe lymphoedema lesions. Consequently, the SM1(+) and SM2(+) cell fractions were significantly reduced in the tunica media and intima of lymphatic vessels. Conclusions These observations indicate that the lymphatic tunica media and tunica intima consist mainly of phenotypically modulated SMCs, and that SMCs play a key role in the developm…

Overview

Integrity signals

Registry

Crossref · 10.1111/bjd.13482

Cites

2 of 2 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Significant collecting LV remodeling occurs depending on the stage of lymphedema, with vessel morphology changes occurring as lymphedema progresses.

    “and recent histological characterizations have uncovered significant collecting LV remodeling, depending on the stage of lymphedema, with vessel morphology changes occurring as lymphedema progresses (144).”

    From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [144]

  • LMCs dedifferentiate and proliferate, with some collecting LVs undergoing inward remodeling, which further increases resistance to flow and reduces lymph transport.

    “Eventually, LMCs dedifferentiate and proliferate, with some collecting LVs undergoing inward remodeling (144), which further increases resistance to flow and reduces lymph transport.”

    From Transport and Immune Functions of the Lymphatic System. (2025) · cites this paper as [144]

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 30

  1. Szuba, 1998, Lymphedema: classification, diagnosis and therapy, Vasc Med, 3, 145, 10.1177/1358836X9800300209 · DOI
  2. Fitzpatrick, 1969, Lymphangiosarcoma and breast cancer, Can J Surg, 12, 172
  3. Schirger, 1962, Idiopathic lymphedema. Review of 131 cases, J Am Med Assoc, 182, 14, 10.1001/jama.1962.03050400016004 · DOI
  4. Williams, 2005, Lymphoedema: estimating the size of the problem, Palliat Med, 19, 300, 10.1191/0269216305pm1020oa · DOI
  5. Ryan, 2003, Aetiology and prevalence of lower limb lymphoedema following treatment for gynaecological cancer, Aust N Z J Obstet Gynaecol, 43, 148, 10.1046/j.0004-8666.2003.00040.x · DOI
  6. Carvalho, 1994, Wertheim-Meigs radical hysterectomy, Sao Paulo Med J, 112, 539, 10.1590/S1516-31801994000200003 · DOI
  7. Rockson, 2001, Lymphedema, Am J Med, 110, 288, 10.1016/S0002-9343(00)00727-0 · DOI
  8. Zampell, 2012, Regulation of adipogenesis by lymphatic fluid stasis: part I. Adipogenesis, fibrosis, and inflammation, Plast Reconstr Surg, 129, 825, 10.1097/PRS.0b013e3182450b2d · DOI
  9. Lee, 2011, Contemporary role of lymphoscintigraphy: we can no longer afford to ignore!, Phlebology, 26, 177, 10.1258/phleb.2011.011e01 · DOI
  10. Alitalo, 2005, Lymphangiogenesis in development and human disease, Nature, 438, 946, 10.1038/nature04480 · DOI
  11. Daroczy, 1995, Pathology of lymphedema, Clin Dermatol, 13, 433, 10.1016/0738-081X(95)00086-U · DOI
  12. Olszewski, 1990, Immune cells in peripheral lymph and skin of patients with obstructive lymphedema, Lymphology, 23, 23
  13. Koshima, 2004, Minimal invasive lymphaticovenular anastomosis under local anesthesia for leg lymphedema: is it effective for stage III and IV?, Ann Plast Surg, 53, 261, 10.1097/01.sap.0000120319.89926.07 · DOI
  14. Koshima, 2000, Supermicrosurgical lymphaticovenular anastomosis for the treatment of lymphedema in the upper extremities, J Reconstr Microsurg, 16, 437, 10.1055/s-2006-947150 · DOI
  15. Zawieja, 2009, Contractile physiology of lymphatics, Lymphat Res Biol, 7, 87, 10.1089/lrb.2009.0007 · DOI
  16. Ikomi, 2006, Recanalization of the collecting lymphatics in rabbit hind leg, Microcirculation, 13, 365, 10.1080/10739680600745810 · DOI
  17. Koshima, 1996, Ultrastructural observations of lymphatic vessels in lymphedema in human extremities, Plast Reconstr Surg, 97, 397, 10.1097/00006534-199602000-00018 · DOI
  18. Manabe, 2003, Regulation of smooth muscle phenotype, Curr Atheroscler Rep, 5, 214, 10.1007/s11883-003-0027-9 · DOI
  19. Ross, 1999, Atherosclerosis - an inflammatory disease, N Engl J Med, 340, 115, 10.1056/NEJM199901143400207 · DOI · Paper page
  20. Darby, 1990, Alpha-smooth muscle actin is transiently expressed by myofibroblasts during experimental wound healing, Lab Invest, 63, 21
  21. Aikawa, 1993, Human smooth muscle myosin heavy chain isoforms as molecular markers for vascular development and atherosclerosis, Circ Res, 73, 1000, 10.1161/01.RES.73.6.1000 · DOI
  22. International Society of Lymphology, 2009, The diagnosis and treatment of peripheral lymphedema. 2009 Concensus Document of the International Society of Lymphology, Lymphology, 42, 51
  23. Perrotta, 2013, Ultrastructural features of human atherosclerosis, Ultrastruct Pathol, 37, 43, 10.3109/01913123.2011.592721 · DOI
  24. Gebousky, 2009, Staging of upper limb lymphedema from routine lymphoscintigraphic examinations, Comput Biol Med, 39, 1, 10.1016/j.compbiomed.2008.10.003 · DOI
  25. Szuba, 2002, Quantitative radionuclide lymphoscintigraphy predicts outcome of manual lymphatic therapy in breast cancer-related lymphedema of the upper extremity, Nucl Med Commun, 23, 1171, 10.1097/00006231-200212000-00004 · DOI
  26. Ogata, 2007, Intraoperative lymphography using indocyanine green dye for near-infrared fluorescence labeling in lymphedema, Ann Plast Surg, 59, 180, 10.1097/01.sap.0000253341.70866.54 · DOI
  27. Iwata, 2013, Lineage of bone marrow-derived cells in atherosclerosis, Circ Res, 112, 1634, 10.1161/CIRCRESAHA.113.301384 · DOI
  28. Wang, 2014, Flow-regulated lymphatic vasculature development and signaling, Vasc Cell, 6, 14, 10.1186/2045-824X-6-14 · DOI
  29. Gordon, 1990, Cell proliferation in human coronary arteries, Proc Natl Acad Sci USA, 87, 4600, 10.1073/pnas.87.12.4600 · DOI · Paper page
  30. Yu, 2011, Smooth muscle cell apoptosis promotes vessel remodeling and repair via activation of cell migration, proliferation, and collagen synthesis, Arterioscler Thromb Vasc Biol, 31, 2402, 10.1161/ATVBAHA.111.235622 · DOI

Cited by

Sorted by citations

Metadata

Authors
Ogata, F., Fujiu, K., Koshima, I., Nagai, R., & Manabe, I.
Affiliations
  • The University of Tokyo (JP)
  • Jichi Medical University (JP)
Corresponding author
Manabe, I.
Venue
British Journal of Dermatology
Published
2015-03-09
Volume
172
Issue
5
Pages
1286-1293
ISSN
0007-0963 (ISSN-L)
OpenAlex
W2062331608
Cited by
39
References
2
Citations by year
2026: 1 · 2025: 1 · 2024: 5 · 2023: 5 · 2022: 4 · 2021: 2 · 2020: 3 · 2019: 3 · 2018: 6 · 2017: 3 · 2016: 5 · 2015: 1
FWCI
1.45
Type
journal article
Language
en
Open access
closed
Locations
  • British Journal of Dermatology (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Japan Society for the Promotion of Science
  • Ministry of Education, Culture, Sports, Science, and Technology
  • Council for Science and Technology Policy
Topics
  • Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
  • Health Sciences › Medicine › Surgery › Lymphatic Disorders and Treatments
  • Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
Keywords
lymphedema, smooth muscle cells, lymphatic vessels, smooth muscle actin, smooth muscle myosin heavy chain, tunica media, tunica intima, lymphatic dysfunction
MeSH terms
Actins, Adult, Aged, Aged, 80 and over, Chronic Disease, Female, Fibrosis, Humans, Immunohistochemistry, Lymphedema, Male, Middle Aged, Phenotype, Myosin Heavy Chains, Smooth Muscle Myosins, Myocytes, Smooth Muscle, Lymphatic Vessels, Microscopy, Electron, Transmission

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review