Download PDF
J Reconstr Microsurg 2018; 34(01): 041-046
DOI: 10.1055/s-0037-1606320
Original Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Quantity of Lymph Nodes in the Vascularized Lymph Node Transfer Influences Its Lymphaticovenous Drainage

Grzegorz J. Kwiecien
1   Department of Plastic Surgery, Cleveland Clinic, Cleveland, Ohio
,
Bahar Bassiri Gharb
1   Department of Plastic Surgery, Cleveland Clinic, Cleveland, Ohio
,
Kashyap K. Tadisina
1   Department of Plastic Surgery, Cleveland Clinic, Cleveland, Ohio
,
Maria Madajka
1   Department of Plastic Surgery, Cleveland Clinic, Cleveland, Ohio
,
Judith Drazba
2   Imaging Core, Lerner Research Institute, Cleveland Clinic, Cleveland, Ohio
,
James E. Zins
1   Department of Plastic Surgery, Cleveland Clinic, Cleveland, Ohio
,
Graham S. Schwarz
1   Department of Plastic Surgery, Cleveland Clinic, Cleveland, Ohio
› Author Affiliations
Further Information

Publication History

09 April 2017

20 July 2017

Publication Date:
15 October 2017 (online)

    Permissions and Reprints

Abstract

Background The purpose of this study was to: (1) evaluate the mechanism of lymph drainage through a vascularized lymph node (VLN) flap, and (2) investigate if the number of VLNs impacts lymph transit time through the flap.

Methods Twenty-seven axillary VLN flaps were elevated in 14 Sprague-Dawley rats and divided into three groups (n = 9 each) based on the number of lymph nodes present: group 1 (0-VLNs), group 2 (2-VLNs), and group 3 (4-VLNs). Indocyanine green (n = 8/group) and Alexa680-albumin (n = 1/group) were injected into the edge of flaps and the latency period between injection and fluorescence in the axillary vein was recorded. Stereomicroscopic fluorescent lymphography was performed to directly visualize lymphatic transit through VLNs.

Results Fluorescence was detected in the axillary vein after 229s [47–476], 79s [15–289], and 56s [16–110] in group 1, 2, and 3, respectively (p < 0.01). There was a negative correlation between the number of VLNs in the flap and the latency period (r = -0.59; p < 0.05). Median flap weights were comparable in group 1, 2, and 3 (258 mg [196–349], 294 mg [212–407], 315 mg [204–386], respectively; p = 0.54). Stereoscopic lymphography allowed direct visualization of lymphatic fluid transit through VLNs.

Conclusion Lymphatic fluid in VLN flaps drains into the venous system mainly by passing through the afferent lymphatics and lymph nodes. A secondary mechanism appears to be the diffusion of fluid into the venous system via intratissue lymphaticovenous connections created during flap elevation. Increasing the number of lymph nodes in the flap is associated with a more rapid transit of fluid.

Keywords

vascularized lymph node transfer - lymphedema - microsurgery - lymphatic transit - mechanism of action
 

  • References

  • 1 Becker C, Assouad J, Riquet M, Hidden G. Postmastectomy lymphedema: long-term results following microsurgical lymph node transplantation. Ann Surg 2006; 243 (03) 313-315
    CrossrefPubMedGoogle Scholar
  • 2 Saaristo AM, Niemi TS, Viitanen TP, Tervala TV, Hartiala P, Suominen EA. Microvascular breast reconstruction and lymph node transfer for postmastectomy lymphedema patients. Ann Surg 2012; 255 (03) 468-473
    CrossrefPubMedGoogle Scholar
  • 3 Cheng MH, Huang JJ, Wu CW, Yang CY, Lin CY, Henry SL. , et al. The mechanism of vascularized lymph node transfer for lymphedema: natural lymphaticovenous drainage. Plast Reconstr Surg 2014; 133 (02) 192e-198e
    CrossrefPubMedGoogle Scholar
  • 4 Cheng MH, Chen SC, Henry SL, Tan BK, Lin MC, Huang JJ. Vascularized groin lymph node flap transfer for postmastectomy upper limb lymphedema: flap anatomy, recipient sites, and outcomes. Plast Reconstr Surg 2013; 131 (06) 1286-1298
    CrossrefPubMedGoogle Scholar
  • 5 Lin CH, Ali R, Chen SC, Wallace C, Chang YC, Chen HC. , et al. Vascularized groin lymph node transfer using the wrist as a recipient site for management of postmastectomy upper extremity lymphedema. Plast Reconstr Surg 2009; 123 (04) 1265-1275
    CrossrefPubMedGoogle Scholar
  • 6 Cheng MH, Huang JJ, Nguyen DH, Saint-Cyr M, Zenn MR, Tan BK. , et al. A novel approach to the treatment of lower extremity lymphedema by transferring a vascularized submental lymph node flap to the ankle. Gynecol Oncol 2012; 126 (01) 93-98
    CrossrefPubMedGoogle Scholar
  • 7 Sapountzis S, Ciudad P, Lim SY, Chilgar RM, Kiranantawat K, Nicoli F. , et al. Modified Charles procedure and lymph node flap transfer for advanced lower extremity lymphedema. Microsurgery 2014; 34 (06) 439-447
    CrossrefPubMedGoogle Scholar
  • 8 Gharb BB, Rampazzo A, Spanio di Spilimbergo S, Xu ES, Chung KP, Chen HC. Vascularized lymph node transfer based on the hilar perforators improves the outcome in upper limb lymphedema. Ann Plast Surg 2011; 67 (06) 589-593
    CrossrefPubMedGoogle Scholar
  • 9 Mehrara BJ, Zampell JC, Suami H, Chang DW. Surgical management of lymphedema: past, present, and future. Lymphat Res Biol 2011; 9 (03) 159-167
    CrossrefPubMedGoogle Scholar
  • 10 Ciudad P, Manrique OJ, Date S. , et al. Double gastroepiploic vascularized lymph node tranfers to middle and distal limb for the treatment of lymphedema. Microsurgery 2017; DOI: 10.1002.
    PubMedGoogle Scholar
  • 11 Inbal A, Teven CM, Chang DW. Latissimus dorsi flap with vascularized lymph node transfer for lymphedema treatment: Technique, outcomes, indications and review of literature. J Surg Oncol 2017; 115 (01) 72-77
    CrossrefPubMedGoogle Scholar
  • 12 Gratzon A, Schultz J, Secrest K, Lee K, Feiner J, Klein RD. Clinical and Psychosocial Outcomes of Vascularized Lymph Node Transfer for the Treatment of Upper Extremity Lymphedema After Breast Cancer Therapy. Ann Surg Oncol 2017; 24 (06) 1475-1481
    CrossrefPubMedGoogle Scholar
  • 13 Tourani SS, Taylor GI, Ashton MW. Vascularized Lymph Node Transfer: A Review of the Current Evidence. Plast Reconstr Surg 2016; 137 (03) 985-993
    CrossrefPubMedGoogle Scholar
  • 14 Kung TA, Champaneria MC, Maki JH, Neligan PC. Current concepts in the surgical management of lymphedema. Plast Reconstr Surg 2017; 139 (04) 1003e-1013e
    CrossrefPubMedGoogle Scholar
  • 15 Carl HM, Walia G, Bello R, Clarke-Pearson E, Hassanein AH, Cho B. et al. Systematic review of the surgical treatment of extremity lymphedema. J Reconstr Microsurg 2017 Jul;33(6):412–425. doi: 10.1055/s-0037-1599100. Epub 2017 Feb 24.
    PubMedGoogle Scholar
  • 16 Raju A, Chang DW. Vascularized lymph node transfer for treatment of lymphedema: a comprehensive literature review. Ann Surg 2015; 261 (05) 1013-1023
    CrossrefPubMedGoogle Scholar
  • 17 Ito R, Zelken J, Yang CY, Lin CY, Cheng MH. Proposed pathway and mechanism of vascularized lymph node flaps. Gynecol Oncol 2016; 141 (01) 182-188
    Google Scholar
  • 18 Hayashida K, Yoshida S, Yoshimoto H, Fujioka M, Saijo H, Migita K. , et al. Adipose-Derived Stem Cells and Vascularized Lymph Node Transfers Successfully Treat Mouse Hindlimb Secondary Lymphedema by Early Reconnection of the Lymphatic System and Lymphangiogenesis. Plast Reconstr Surg 2017; 139 (03) 639-651
    CrossrefPubMedGoogle Scholar
  • 19 Chen WF, Zhao H, Yamamoto T, Hara H, Ding J. Indocyanine Green Lymphographic Evidence of Surgical Efficacy Following Microsurgical and Supermicrosurgical Lymphedema Reconstructions. J Reconstr Microsurg 2016; 32 (09) 688-698
    Article in Thieme ConnectPubMedGoogle Scholar
  • 20 Miranda Garcés M, Pons G, Mirapeix R, Masià J. Intratissue lymphovenous communications in the mechanism of action of vascularized lymph node transfer. J Surg Oncol 2017; 115 (01) 27-31
    CrossrefPubMedGoogle Scholar
  • 21 Nguyen DH, Chou PY, Hsieh YH, Momeni A, Fang YH, Patel KM. , et al. Quantity of lymph nodes correlates with improvement in lymphatic drainage in treatment of hind limb lymphedema with lymph node flap transfer in rats. Microsurgery 2016; 36 (03) 239-245
    CrossrefPubMedGoogle Scholar
  • 22 Dayan JH, Dayan E, Smith ML. Reverse lymphatic mapping: a new technique for maximizing safety in vascularized lymph node transfer. Plast Reconstr Surg 2015; 135 (01) 277-285
    CrossrefPubMedGoogle Scholar
  • 23 Kwiecien GJ, Uygur S, Korn J, Gharb BB, Madajka M, Djohan R. , et al. Vascularized axillary lymph node transfer: A novel model in the rat. Microsurgery 2015; 35 (08) 662-667
    CrossrefPubMedGoogle Scholar
  • 24 Tilney NL. Patterns of lymphatic drainage in the adult laboratory rat. J Anat 1971; 109 (Pt 3): 369-383
    PubMedGoogle Scholar
  • 25 Cemal Y, Pusic A, Mehrara BJ. Preventative measures for lymphedema: separating fact from fiction. J Am Coll Surg 2011; 213 (04) 543-551
    CrossrefPubMedGoogle Scholar
  • 26 Miranda Garcés M, Mirapeix R, Pons G, Sadri A, Masià J. A comprehensive review of the natural lymphaticovenous communications and their role in lymphedema surgery. J Surg Oncol 2016; 113 (04) 374-380
    CrossrefPubMedGoogle Scholar
  • 27 Kariya S, Komemushi A, Nakatani M, Yoshida R, Kono Y, Tanigawa N. Intranodal lymphangiogram: technical aspects and findings. Cardiovasc Intervent Radiol 2014; 37 (06) 1606-1610
    CrossrefPubMedGoogle Scholar
  • 28 Koehler PR, Schaffer B. Peripheral lymphatico-venous anastomoses. Report of two cases. Circulation 1967; 35 (02) 401-404
    CrossrefPubMedGoogle Scholar
  • 29 Stanton AW, Modi S, Mellor RH, Levick JR, Mortimer PS. Recent advances in breast cancer-related lymphedema of the arm: lymphatic pump failure and predisposing factors. Lymphat Res Biol 2009; 7 (01) 29-45
    CrossrefPubMedGoogle Scholar
  • 30 Threefoot SA, Kossover MF, Kent WT, Hatchett BF, Pearson Jr JE, Cabrera-Gil C. Factors stimulating function of lymphaticovenous communications. Angiology 1967; 18 (11) 682-698
    CrossrefPubMedGoogle Scholar
  • 31 Threefoot SA, Kossover MF. Lymphaticovenous communications in man. Arch Intern Med 1966; 117 (02) 213-223
    CrossrefPubMedGoogle Scholar
  • 32 Threefoot SA. The clinical siginifcance of lymphaticovenous communications. Ann Intern Med 1970; 72 (06) 957-958
    CrossrefPubMedGoogle Scholar
  • 33 Edwards JM, Kinmonth JB. Lymphovenous shunts in man. BMJ 1969; 4 (5683): 579-581
    CrossrefPubMedGoogle Scholar
  • 34 Heymans O, Fallais C, Hustinx R. Intratissular lymphaticovenous anastomoses demonstrated by perioperative intramuscular injection of 99mTC-colloids. Lymphat Res Biol 2006; 4 (01) 29-33
    CrossrefPubMedGoogle Scholar
  • 35 Shao L, Takeda K, Kato S, Mori S, Kodama T. Communication between lymphatic and venous systems in mice. J Immunol Methods 2015; 424: 100-105
    CrossrefPubMedGoogle Scholar
  • 36 Tammela T, Saaristo A, Holopainen T, Lyytikkä J, Kotronen A, Pitkonen M. , et al. Therapeutic differentiation and maturation of lymphatic vessels after lymph node dissection and transplantation. Nat Med 2007; 13 (12) 1458-1466
    CrossrefPubMedGoogle Scholar
  • 37 Scallan JP, Huxley VH. In vivo determination of collecting lymphatic vessel permeability to albumin: a role for lymphatics in exchange. J Physiol 2010; 588 (Pt 1): 243-254
    CrossrefPubMedGoogle Scholar
  • 38 Aschen SZ, Farias-Eisner G, Cuzzone DA. , et al. Lymph node transplantation results in spontaneous lymphatic reconnection and restoration of lymphatic flow. Plast Reconstr Surg 2014; 133 (02) 301-310
    CrossrefPubMedGoogle Scholar
  • 39 Ohtani O, Ohtani Y. Recent developments in morphology of lymphatic vessels and lymph nodes. Ann Vasc Dis 2012; 5 (02) 145-150
    PubMedGoogle Scholar
  • 40 Wiig H, Swartz MA. Interstitial fluid and lymph formation and transport: physiological regulation and roles in inflammation and cancer. Physiol Rev 2012; 92 (03) 1005-1060
    CrossrefPubMedGoogle Scholar