Annals of Surgical Oncology

, Volume 14, Issue 2, pp 286–298 | Cite as

Lymphatic Drainage of the Peritoneal Space: A Pattern Dependent on Bowel Lymphatics

  • Cherie P. Parungo
  • David I. Soybel
  • Yolonda L. Colson
  • Sang-Wook Kim
  • Shunsuke Ohnishi
  • Alec M. De Grand
  • Rita G. Laurence
  • Edward G. Soltesz
  • Fredrick Y. Chen
  • Lawrence H. Cohn
  • Moungi G. Bawendi
  • John V. FrangioniEmail author
Resident/Fellow Essay Award Winner for the Best Clinical Research Paper Basic Science and Special Investigator Award Winners



Understanding lymph drainage patterns of the peritoneum could assist in staging and treatment of gastrointestinal and ovarian malignancies. Sentinel lymph nodes (SLNs) have been identified for solid organs and the pleural space. Our purpose was to determine whether the peritoneal space has a predictable lymph node drainage pattern.


Rats received intraperitoneal injections of near-infrared (NIR) fluorescent tracers: namely, quantum dots (designed for retention in SLNs) or human serum albumin conjugated with IRDye800 (HSA800; designed for lymphatic flow beyond the SLN). A custom imaging system detected NIR fluorescence at 10 and 20 minutes and 1, 4, and 24 hours after injection. To determine the contribution of viscera to peritoneal lymphatic flow, additional cohorts received bowel resection before NIR tracer injection. Associations with appropriate controls were assessed with the χ2 test.


Quantum dots drained to the celiac, superior mesenteric, and periportal lymph node groups. HSA800 drained to these same groups at early time points but continued flowing to the mediastinal lymph nodes via the thoracic duct. After bowel resection, both tracers were found in the thoracic, not abdominal, lymph node groups. Additionally, HSA800 was no longer found in the thoracic duct but in the anterior chest wall and diaphragmatic lymphatics.


The peritoneal space drains to the celiac, superior mesenteric, and periportal lymph node groups first. Lymph continues via the thoracic duct to the mediastinal lymph nodes. Bowel lymphatics are a key determinant of peritoneal lymph flow, because bowel resection shifts lymph flow directly to the intrathoracic lymph nodes via chest wall lymphatics.


Peritoneal space Lymph node Lymphatic drainage Near-infrared fluorescence Carcinomatosis Metastasis 



The authors thank Peter Kang, MD, and Tomislav Mihaljevic, MD, for helpful discussion; Barbara L. Clough for editing; and Grisel Vazquez for administrative assistance. Supported by National Institutes of Health National Research Service Award F32 HL72568-01 (C.P.P.), the National Science Foundation Materials Research Science and Engineering Center Program under Grant DMR-0213282 (M.G.B.), National Institutes of Health Grants R01-CA-115296 (J.V.F.) and R33-EB-000673 (J.V.F. and M.G.B.), and an Application Development Award (J.V.F.) from the Center for Integration of Medicine and Innovative Technology.


  1. 1.
    Uren RF, Hoefnagel CA. Lymphoscintigraphy. In: Thompson JF, Morton DM, Kroon BBR, eds. Textbook of Melanoma. London, Martin Dunitz, 2003, 339–64Google Scholar
  2. 2.
    Parungo CP, Colson YL, Kim S, et al. Sentinel lymph node mapping of the pleural space. Chest 2005;127:1799–804PubMedCrossRefGoogle Scholar
  3. 3.
    Parungo CP, Ohnishi S, De Grand AM, et al. In vivo optical imaging of pleural space drainage to lymph nodes of prognostic significance. Ann Surg Oncol 2004;11:1085–92PubMedCrossRefGoogle Scholar
  4. 4.
    Fritz DL, Waag DM. Transdiaphragmatic lymphatic transport of intraperitoneally administered marker in hamsters. Lab Anim Sci 1999;49:522–9PubMedGoogle Scholar
  5. 5.
    Abu-Hijleh MF, Habbal OA, Moqattash ST. The role of the diaphragm in lymphatic absorption from the peritoneal cavity. J Anat 1995;186(Pt 3):453–67PubMedGoogle Scholar
  6. 6.
    Abernethy NJ, Chin W, Hay JB, Rodela H, Oreopoulos D, Johnston MG. Lymphatic drainage of the peritoneal cavity in sheep. Am J Physiol 1991;260:F353–8PubMedGoogle Scholar
  7. 7.
    Cardenas A, Kelleher T, Chopra S. Review article: hepatic hydrothorax. Aliment Pharmacol Ther 2004;20:271–9PubMedCrossRefGoogle Scholar
  8. 8.
    Kim S, Lim YT, Soltesz EG, et al. Near-infrared fluorescent type II quantum dots for sentinel lymph node mapping. Nat Biotechnol 2004;22:93–7PubMedCrossRefGoogle Scholar
  9. 9.
    Ohnishi S, Lomnes SJ, Laurence RG, Gogbashian A, Mariani G, Frangioni JV. Organic alternatives to quantum dots for intraoperative near-infrared fluorescent sentinel lymph node mapping. Mol Imaging 2005;4:172–81PubMedGoogle Scholar
  10. 10.
    De Grand AM, Frangioni JV. An operational near-infrared fluorescence imaging system prototype for large animal surgery. Technol Cancer Res Treat 2003;2:553–62PubMedGoogle Scholar
  11. 11.
    Yuan Z, Rodela H, Hay JB, Oreopoulos D, Johnston MG. Lymph flow and lymphatic drainage of inflammatory cells from the peritoneal cavity in a casein-peritonitis model in sheep. Lymphology 1994;27:114–28PubMedGoogle Scholar
  12. 12.
    Tran L, Rodela H, Abernethy NJ, et al. Lymphatic drainage of hypertonic solution from peritoneal cavity of anesthetized and conscious sheep. J Appl Physiol 1993;74:859–67PubMedGoogle Scholar
  13. 13.
    Greene FL, Balch CM, Page DL, et al. AJCC Cancer Staging Manual. 6th ed. New York: Springer-Verlag, 2002Google Scholar
  14. 14.
    Begossi G, Gonzalez-Moreno S, Ortega-Perez G, Fon LJ, Sugarbaker PH. Cytoreduction and intraperitoneal chemotherapy for the management of peritoneal carcinomatosis, sarcomatosis and mesothelioma. Eur J Surg Oncol 2002;28:80–7PubMedCrossRefGoogle Scholar
  15. 15.
    Verwaal VJ, van Ruth S, de Bree E, et al. Randomized trial of cytoreduction and hyperthermic intraperitoneal chemotherapy versus systemic chemotherapy and palliative surgery in patients with peritoneal carcinomatosis of colorectal cancer. J Clin Oncol 2003;21:3737–43PubMedCrossRefGoogle Scholar
  16. 16.
    Verwaal VJ, van Tinteren H, van Ruth S, Zoetmulder FA. Predicting the survival of patients with peritoneal carcinomatosis of colorectal origin treated by aggressive cytoreduction and hyperthermic intraperitoneal chemotherapy. Br J Surg 2004;91:739–46PubMedCrossRefGoogle Scholar
  17. 17.
    Witkamp AJ, de Bree E, Kaag MM, van Slooten GW, van Coevorden F, Zoetmulder FA. Extensive surgical cytoreduction and intraoperative hyperthermic intraperitoneal chemotherapy in patients with pseudomyxoma peritonei. Br J Surg 2001;88:458–63PubMedCrossRefGoogle Scholar
  18. 18.
    Lambrou NC, Gomez-Marin O, Mirhashemi R, et al. Optimal surgical cytoreduction in patients with stage III and stage IV endometrial carcinoma: a study of morbidity and survival. Gynecol Oncol 2004;93:653–8PubMedCrossRefGoogle Scholar
  19. 19.
    Parungo CP, Ohnishi S, Kim SW, et al. Intraoperative identification of esophageal sentinel lymph nodes using near-infrared fluorescence imaging.J Thorac Cardiovasc Surg 2005;129:844–50PubMedCrossRefGoogle Scholar
  20. 20.
    Soltesz EG, Kim S, Laurence RG, et al. Intraoperative sentinel lymph node mapping of the lung using near-infrared fluorescent quantum dots. Ann Thorac Surg 2005;79:269–77, discussion 269–77PubMedCrossRefGoogle Scholar
  21. 21.
    Soltesz EG, Kim S, Kim SW, et al. Sentinel lymph node mapping of the gastrointestinal tract by using invisible light. Ann Surg Oncol 2006;13:386–96PubMedCrossRefGoogle Scholar
  22. 22.
    Abernethy NJ, Chin W, Hay JB, Rodela H, Oreopoulos D, Johnston MG. Lymphatic removal of dialysate from the peritoneal cavity of anesthetized sheep. Kidney Int 1991;40:174–81PubMedCrossRefGoogle Scholar
  23. 23.
    Noguchi M. Sentinel lymph node biopsy and breast cancer. Br J Surg 2002;89:21–34PubMedCrossRefGoogle Scholar
  24. 24.
    Watanabe T, Kimijima I, Ohtake T, Tsuchiya A, Shishido F, Takenoshita S. Sentinel node biopsy with technetium-99m colloidal rhenium sulphide in patients with breast cancer. Br J Surg 2001;88:704–7PubMedCrossRefGoogle Scholar
  25. 25.
    Wong SL, Edwards MJ, Chao C, Simpson D, McMasters KM. The effect of lymphatic tumor burden on sentinel lymph node biopsy results. Breast J 2002;8:192–8PubMedCrossRefGoogle Scholar
  26. 26.
    Marco AJ, Domingo M, Ruberte J, Carretero A, Briones V, Dominguez L. Lymphatic drainage of Listeria monocytogenes and Indian ink inoculated in the peritoneal cavity of the mouse. Lab Anim 1992;26:200–5PubMedCrossRefGoogle Scholar
  27. 27.
    McMasters KM, Reintgen DS, Ross MI, et al. Sentinel lymph node biopsy for melanoma: how many radioactive nodes should be removed? Ann Surg Oncol 2001;8:192–7PubMedCrossRefGoogle Scholar
  28. 28.
    Wong SL, Edwards MJ, Chao C, et al. Sentinel lymph node biopsy for breast cancer: impact of the number of sentinel nodes removed on the false-negative rate. J Am Coll Surg 2001;192:684–9, discussion 689–91PubMedCrossRefGoogle Scholar

Copyright information

© Society of Surgical Oncology 2006

Authors and Affiliations

  • Cherie P. Parungo
    • 1
  • David I. Soybel
    • 1
  • Yolonda L. Colson
    • 1
  • Sang-Wook Kim
    • 2
  • Shunsuke Ohnishi
    • 3
  • Alec M. De Grand
    • 3
  • Rita G. Laurence
    • 1
  • Edward G. Soltesz
    • 1
  • Fredrick Y. Chen
    • 1
  • Lawrence H. Cohn
    • 1
  • Moungi G. Bawendi
    • 2
  • John V. Frangioni
    • 3
    Email author
  1. 1.Department of SurgeryBrigham & Women’s HospitalBostonUSA
  2. 2.Department of ChemistryMassachusetts Institute of TechnologyCambridgeUSA
  3. 3.Division of Hematology/Oncology and Department of RadiologyBeth Israel Deaconess Medical CenterBostonUSA

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