Assessment of immune cells and function of the residual spleen after subtotal splenectomy due to splenomegaly in cirrhotic patients

BMC Immunology

Xiao-Ji Zhu⁴  Wen-Jun Guo¹  Kun Li⁴  Hong-Jie Sun³  Jin-Yuan Tang⁴  Min Wang⁴  Tao Wang²  Yong-Bo Xu⁴  Feng-Guo Jian³  Jian-Hua Zhao⁴  Ting-Guo Zhang¹  Hai-Bo Chu⁴ 

[1] Department of Pathology, Weifang Medical University, Weifang, China;Departments of Pathology, The 89th Hospital of PLA, Weifang, China;Department of General Surgery, Changyi People’s Hospital, Weifang, China;Center of General Surgery, The 89th Hospital of PLA, West Beigong Road 256, Weifang 261021, China

关键词: Immune;    Macrophage;    T, B lymphocytes;    Portal hypertension;    Splenomegaly;    Residual spleen;   

Others  :  1077694
DOI  :  10.1186/s12865-014-0042-3

 received in 2014-05-15, accepted in 2014-09-22,  发布年份 2014

【 摘 要 】

Background

The spleen is thought to be central in regulating the immune system, a metabolic asset involved in endocrine function. Overwhelming postsplenectomy infection leads to a mortality rate of up to 50%. However, there is still controversy on performing subtotal splenectomy as treatment of splenomegaly due to portal hypertension in cirrhotic patients. In the present study, immunocytes and the indexes of splenic size, hemodynamics, hematology and immunology in the residual spleen were analyzed to support subtotal splenectomy due to splenomegaly.

Results

In residual spleen, T lymphocytes mainly were focal aggregation in the periarterial lymphatic sheath. While B lymphocytes densely distributed in splenic corpuscle. In red pulp, macrophages were equally distributed in the xsplenic cord and adhered to the wall of splenic sinus with high density. The number of unit area T and B lymphocytes of splenic corpuscle and marginal zone as well as macrophages of red pulp were obviously increased in the residual spleen, while the number of macrophages didn’t be changed among the three groups in white pulp. While there were some beneficial changes (i.e., Counts of platelet and leucocyte as well as serum proportion of CD3+ T cells, CD4+ T cells, CD8+ T cells were increased markedly; serum levels of M-CSF and GM-CSF were decreased significantly; The proportion of granulocyte, erythrocyte, megakaryocyte in bone marrow were changed obviously; But serum IgA, IgM, IgG, Tuftsin level, there was no significant difference; splenic artery flow volume, portal venous diameter and portal venous flow volume, a significant difference was observed in residual spleen) in the clinical indices.

Conclusion

After subtotal splenectomy with splenomegaly due to portal hypertension in cirrhotic patients, the number of unit area T and B lymphocytes, and MØ in red pulp of residual spleen increased significantly. However, whether increase of T, B lymphocytes and MØs in residual splenic tissue can enhance the immune function of the spleen, still need further research to confirm.

【 授权许可】

   
2014 Chu et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Tarantino G, Savastano S, Capone D, Colao A: Spleen: a new role for an old player? World J Gastroenterol 2011, 17:3776-3784.
• [2]Jones P, Leder K, Woolley I, Cameron P, Cheng A, Spelman D: Postsplenectomy infection-strategies for prevention in general practice. Aust Fam Physician 2010, 39:383-386.
• [3]Petroianu A, Resende V, Silva R: Late postoperative follow-up of patients undergoing subtotal splenectomy. Clinics (Sao Paulo) 2005, 60:473-478.
• [4]Coignard-Biehler H, Lanternier F, Hot A, Salmon D, Berger A, de Montalembert M, Suarez F, Launay O, Lecuit M, Lortholary O: Adherence to preventive measures after splenectomy in the hospital setting and in the community. J Infect Public Health 2011, 4:187-194.
• [5]BIerring F, Grunnet I: Quantitative bone marrow studies in the rat following a combination of subtotal splenectomy, total thymectomy and extensive removal of lymph nodes. Acta Anat (Basel) 1964, 59:182-187.
• [6]Morgenstern L, Kahn F, Weinstein I: Subtotal splenectomy in myelofibrosis. Surgery 1966, 60:336-339.
• [7]Goldthorn JF, New BA, Schwartz AD: The protection of small amounts of splenic tissue against intravenous pneumococcal challenge following subtotal splenectomy. J Surg Oncol 1981, 17:145-149.
• [8]Malangoni MA, Dawes LG, Droege EA, Rao SA, Collier BD, Almagro UA: Splenic phagocytic function after partial splenectomy and splenic autotransplantation. Arch Surg 1985, 120:275-278.
• [9]Dugan MC, Grogan TM, Witte MH, Rangel C, Richter L, Witte CL, Van Wyck DB: Immunoarchitecture of the regenerating rat spleen: effects of partial splenectomy and heterotopic autotransplantation. Scan Electron Microsc 1986, ᅟ(Pt 2):607-613.
• [10]Resende V, Petroianu A: Functions of the splenic remnant after subtotal splenectomy for treatment of severe splenic injuries. Am J Surg 2003, 185:311-315.
• [11]Bader-Meunier B, Gauthier F, Archambaud F, Cynober T, Miélot F, Dommergues JP, Warszawski J, Mohandas N, Tchernia G: Long-term evaluation of the beneficial effect of subtotal splenectomy for management of hereditary spherocytosis. Blood 2001, 97:399-403.
• [12]Petroianu A, Da Silva RG, Simal CJ, De Carvalho DG, da Silva RA: Late postoperative follow-up of patients submitted to subtotal splenectomy. Am Surg 1997, 63:735-740.
• [13]Andraus W, Pinheiro RS, Haddad LB, Herman P, D’Albuquerque LA: The best approach for splenectomy in portal hypertension. Surgery 2011, 149:853.
• [14]Li E, Zhao L, Zhu L, Lin A, Ge L, Wang F, Shi B: Treating portal hypertension by subtotal splenectomy with retroperitoneal splenic transposition and devascularization: clinical study. Zhonghua Wai Ke Za Zhi 1998, 36:333-335.
• [15]Petroianu A, Resende V, Da Silva RG: Late follow-up of patients submitted to subtotal splenectomy. Int Surg 2006, 4:172-178.
• [16]Elmore SA: Enhanced histopathology of the spleen. Toxicol Pathol 2006, 34:648-655.
• [17]Steiniger B, Barth P, Hellinger A: The perifollicular and marginal zones of the human splenic white pulp: do fibroblasts guide lymphocyte immigration? Am J Pathol 2001, 159:501-512.
• [18]Bajenoff M, Glaichenhaus N, Germain RN: Fibroblastic reticular cells guide T lymphocyte entry into and migration within the splenic T cell zone. J Immunol 2008, 181:3947-3954.
• [19]Pabst R, Westermann J: The role of the spleen in lymphocyte migration. Scanning Microsc 1991, 5:1075-1079.
• [20]Mina-Osorio P, Rosas-Ballina M, Valdes-Ferrer SI, Al-Abed Y, Tracey KJ, Diamond B: Neural signaling in the spleen controls B-cell responses to blood-borne antigen. Mol Med 2012, 18:618-627.
• [21]Brelińska R, Pilgrim C: Macrophages and interdigitating cells; their relationship to migrating lymphocytes in the white pulp of rat spleen. Cell Tissue Res 1983, 233:671-688.
• [22]Karlsson MC, Guinamard R, Bolland S, Sankala M, Steinman RM, Ravetch JV: Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone. J Exp Med 2003, 198:333-340.
• [23]McGaha TL, Chen Y, Ravishankar B, van Rooijen N, Karlsson MC: Marginal zone macrophages suppress innate and adaptive immunity to apoptotic cells in the spleen. Blood 2011, 117:5403-5412.
• [24]Mosser DM, Edwards JP: Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008, 8:958-969.
• [25]Tokushige K, Hirose S, Nishimura H, Fujimori M, Yamauchi K, Obata H, Futagawa S, Shirai T: Abnormal T cell activation and skewed T cell receptor V beta repertoire usage in Japanese patients with idiopathic portal hypertension. Clin Immunol Immunopathol 1995, 75:206-213.
• [26]Mejias M, Garcia-Pras E, Gallego J, Mendez R, Bosch J, Fernandez M: Relevance of the mTOR signaling pathway in the pathophysiology of splenomegaly in rats with chronic portal hypertension. J Hepatol 2010, 52:529-539.
• [27]Yamamoto K: Morphological studies of the spleen in idiopathic portal hypertension (so-called Banti’s syndrome without liver cirrhosis) using light microscopy, scanning electron microscopy and histometry. Acta Pathol Jpn 1979, 29:1-19.
• [28]Li ZF, Zhang S, Lv GB, Huang Y, Zhang W, Ren S, Yang J, Dang SS: Changes in count and function of splenic lymphocytes from patients with portal hypertension. World J Gastroenterol 2008, 14:2377-2382.
• [29]Tang WH, Wu FL, Huang MK, Friess H: Splenic tissue autotransplantation in rabbits: no restoration of host defense. Langenbecks Arch Surg 2003, 387:379-385.
• [30]Smith E, De Young NJ, Drew PA: Immune cell subpopulations in regenerated splenic tissue in rats. Aust N Z J Surg 1999, 69:522-525.
• [31]Li ZF, Gao J, Zhang S, Zhang Y, Sun Y, Su Q: The observation of quantity and phagocytosis of splenic macrophages in patients with portal hypertension-associated hypersplenism. Chin J Exp Surg 2006, 23:1288-1290.
• [32]Li ZF, Zhang S: Changes in splenic macrophage function of hypersplenism due to portal hypertension. Zhonghua Wai Ke Za Zhi 2009, 47:89-91.
• [33]Chen X, Chen S, Li C, Zhu Y, Peng B: Skewed T-cell subsets and enhanced macrophages phagocytosis in the spleen of patients with immune thrombocytopenia failing glucocorticoids. Int J Hematol 2011, 94:248-254.
• [34]Guisado Vasco P, Villar Rodriguez JL, Ibañez Martínez J, González Cámpora R, Galera Davidson H: Immunohistochemical organization patterns of the follicular dendritic cells, myofibroblasts and macrophages in the human spleen–new considerations on the pathological diagnosis of splenectomy pieces. Int J Clin Exp Pathol 2009, 3:189-202.
• [35]Humphrey JH, Grennan D: Different macrophage populations distinguished by means of fluorescent polysaccharides. Recognition and properties of marginal‐zone macrophages. Eur J Immunol 1981, 11:221-228.
• [36]Steiniger B, Barth P, Herbst B, Hartnell A, Crocker PR: The species-specific structure of microanatomical compartments in the human spleen: strongly sialoadhesin-positive macrophages occur in the perifollicular zone, but not in the marginal zone. Immunology 1997, 92:307-316.
• [37]Brozman M: Anatomical pathways from the white to the red pulp in the human spleen. Acta Anat (Basel) 1985, 121:189-193.
• [38]Gomez-Rubio M, Lopez-Cano A, Rendon P, Munoz-Benvenuty A, Macias M, Garre C, Segura-Cabral JM: Safety and diagnostic accuracy of percutaneous ultrasound-guided biopsy of the spleen: a multicenter study. J Clin Ultrasound 2009, 37:445-450.
• [39]Gannot G, Richardson AM, Rodriguez-Canales J, Pinto PA, Merino MJ, Chuaqui RF, Gillespie JW, Emmert-Buck MR: Decrease in CD8+ lymphocyte number and altered cytokine profile in human prostate cancer. Am J Cancer Res 2011, 1:120-127.
• [40]Rivera HM, Bethea CL: Ovarian steroids increase spinogenetic proteins in the macaque dorsal raphe. Neuroscience 2012, 208:27-40.