HYPOSPLENISM AS A RISK FACTOR OF INFECTION, AUTOIMMUNITY AND COMPLICATIONS IN COELIAC DISEASE. Antonio Di Sabatino

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1 HYPOSPLENISM AS A RISK FACTOR OF INFECTION, AUTOIMMUNITY AND COMPLICATIONS IN COELIAC DISEASE Antonio Di Sabatino First Department of Medicine, University of Pavia, Fondazione IRCCS Policlinico S. Matteo, Pavia

2 Definition of hyposplenism In 1955, Dameshek coined the term hyposplenism to describe a patient with coeliac disease in whom Howell-Jolly bodies were detected on peripheral blood smear and an atrophic spleen was confirmed at post-mortem examination Since then, hyposplenism has been regarded as an acquired disorder, potentially associated with several diseases, sometimes accompanied by a reduction in spleen size, and burdened by the same complications occurring in surgical asplenia

3 Structure, function, and cell populations of the three functional compartments of the spleen COMPARTMENT HISTOLOGY STRUCTURE FUNCTION CELL White pulp PALS A Mn Follicle GC Follicle PALS A PALS Mn GC Adaptive response (antigenspecific) consequent to interaction between antigen presenting cells (dendritic cells or marginal zone B lymphocytes) and B or T lymphocytes PALS (T-dependent) Small CD4 + T lymphocytes Dendritic cells B lymphocytes Macrophages Plasma cells Follicle (B-dependent) B lymphocytes/plasma cells Dendritic cells Marginal zone MZ MZ MZ Innate response (first line defence, non-antigen specific) characterised by IgM-memory B lymphocyte production of natural antibodies Resident B lymphocytes Macrophages In transit CD4 + T lymphocytes CD27 + memory B lymphocytes Dendritic cells Red pulp Cords Sinus Sinus Cords Sinus Innate response characterised by activation of macrophages in cords Adaptive response characterised by plasma cell migration from the white pulp after antigen-specific differentiation in follicles Blood filter (pitting, culling) Cords of Billroth CD8 + T lymphocytes Fibroblasts Macrophages Natural killer cells Sinusoids CD8 + endothelial cells Di Sabatino & Corazza. Lancet 211

4 Function of CD27 + memory B cells in steady-state conditions IgM-memory B cells (IgM bright IgD dull ) Fetal liver? spleen B T-independent reaction Switched-memory B cells (IgM neg IgD neg ) Bone marrow spleen B Lymph node APC T B T-dependent reaction Carsetti et al. Immunol Rev 24

5 IgM memory B cells controlling Streptococcus pneumoniae infections are generated in the spleen CD27 IgD Splenectomized patient (SP) memory 4.8% IgM mem 3.6% mature Switched Control subject (CS) memory 54.3% IgM mem 21.5% mature CD22 Switched IgM % of total lymphocytes % of total B cells B cells SP IgM-mem p<.1 CS SP CS % of total B cells % of total B cells B Memory SP p<.1 CS Switched-mem SP CS Kruetzmann et al. J Exp Med 23

6 Clinical consequences of defective spleen function FUNCTION RESULT OF DEFECTIVE FUNCTION CLINICAL CONSEQUENCES Immune IgM-memory B cells Tuftsin/properdin activity Serious infections by encapsulated bacteria (Streptococcus pneumoniae, Neisseria meningitidis, Haemophylus influenzae) Marginal zone B cells Treg Autoimmunity Sequestration of platelets (Culling) Thromboembolism Filtering removal of pits from erythrocytes (Pitting) circulating pitted erythrocytes and Howell- Jolly bodies

7 Diagnostic techniques for spleen dysfunction 99 Tc Spleen scan Howell-Jolly bodies Pitted red cells Di Sabatino & Corazza. Lancet 211

8 Flow cytometric analysis of IgM-memory B cells as a diagnostic tool for spleen dysfunction Pitted red cells (%) SPLENECTOMIZED PATIENTS p<.1 Pitted red cells (%) HYPOSPLENIC PATIENTS p= IgM-memory B cells (% total B cells) IgM-memory B cells (% total B cells) Di Sabatino et al. Am J Gastro 25

9 Natural history of splenic hypofunction REVERSIBLE HYPOSPLENISM IRREVERSIBLE HYPOSPLENISM SPLENIC ATROPHY Responder Crohn s disease pts 14 Non-responder Crohn s disease pts p<.1 12 Pitted red cells (%) Pitted red cells (%) Pre-ifx Post-ifx Di Sabatino et al. IBD 28 Pre-ifx Post-ifx Di Sabatino et al. IBD 28

10 Coeliac disease as the commonest cause of nonsurgical asplenia DISEASES ASSOCIATED WITH FUNCTIONAL HYPOSPLENISM/SPLENIC ATROPHY Di Sabatino A & Corazza GR. Lancet 211

11 Functional hyposplenism in untreated coeliac disease (CD) Pitted red cells (%) Untreated CD (Hypo=33%) Control subjects (Hypo=%) Asplenic subjects (Hypo=1%) Corazza et al. Am J Gastroenterol 1999

12 Pitted red cell counting correlates with IgM-memory B cells and serum tuftsin activity in untreated coeliac disease Untreated coeliac patients Pitted red cells (%) IgM memory B cells (% total B cells) p=.1 r s =-.34 Pitted red cells (%) p<.1 r s = Serum tuftsin activity (%) Corazza et al. Am J Gastro 1999; Di Sabatino et al. Clin Gastroenterol Hepatol 26

13 Effect of age at onset, age at diagnosis and gluten-free diet in patients with coeliac disease EFFECT OF AGE AT ONSET EFFECT OF AGE AT DIAGNOSIS EFFECT OF GLUTEN-FREE DIET Pitted red cells (%) Control subjects Coeliac children Asplenic subjects Hyposplenic coeliacs (%) Age at diagnosis Age at study 15/19 2/29 3/39 4/49 5/59 6/69 >69 Age (years) Pitted red cells (%) p< Months of gluten-free diet Corazza et al. Gut 1982 Corazza et al. Am J Gastro 1999 Corazza et al. Gut 1983

14 Splenic hypofunction and coeliac disease (CD)- associated autoimmune disorders (AID) 35 Healthy Volunteers (Hypo=%) CD patients without AID (Hypo=19%) CD patients with AID (Hypo=59%) Splenectomized patients (Hypo=1%) Pitted red cells (%) Di Sabatino et al. Clin Gastroenterol Hepatol 26

15 Circulating IgM-memory and switched-memory B cells in coeliac disease (CD)-associated autoimmune disorders (AID) CD27 Asplenic subject memory 8.1% Hyposplenic coeliac memory 22.6% Control subject memory 46.3% 2 MEMORY B CELLS IgM IgD mature IgM mem 2.1% mature mature IgM mem 3.8% IgM mem 15.4% CD22 % of total B cells p<.5 Switched Switched Switched Switched IgM SP CD + AID CD w/o AID HC Di Sabatino et al. Clin Gastroenterol Hepatol 26

16 Splenic hypofunction and the spectrum of malignant complications in adult coeliac disease 35 3 Compl. CD (Hypo=8%) Uncompl. CD (Hypo=19%) Pitted red cells (%) Di Sabatino et al. Clin Gastroenterol Hepatol 26

17 Splenic atrophy and mesenteric lymph node cavitation in a patient with refractory coeliac disease 99m Tc Splenic Scan Abdominal Bowel Sonography Posteroanterior Laterolateral Di Sabatino et al. Clin Gastroenterol Hepatol 26

18 Splenic atrophy and coeliac disease. Morphological and functional aspects Control-PBL CD-PBL Control subject Coeliac patient CD27 CD19 + Response to CpG-ODN CD45RO CD2 CD27 IgD Control-SPL CD-SPL CD19 + CD21 bright CD19 + CD27 + Immunoglobulins (µg/ml) Control subject IgM IgA IgG Coeliac patient IgM Di Sabatino et al. J Allergy Clin Immunol 27

19 Case reports of hyposplenism-related infections in patients with coeliac disease AUTHOR YEAR JOURNAL CASES TYPE OF INFECTION OTHER DETAILS Corazza GR 1984 Ital J Gastroenterol 1 Pneumoccoccal pneumonia Splenic atrophy Matuchansky C 1984 Gastroenterology 2 Pneumococcal pneumonia, infectious pericarditis Splenic atrophy (2) MLNC (2) O Donogue DJ 1986 Postgrad Med J 1 Pneumococcal septicemia Splenic atrophy Logan RFA 1989 Gastroenterology 2 Pneumococcal meningitis, septicemia by Salmonella Splenic atrophy (1) Stevens FM 199 Digestion 3 Lung abscesses bystaphyl, Klebsiella, MycoTBC Splenic atrophy (2) Hyposplenism (1) Howat AJ 1995 Histopathology 2 Fatal chest infection, septicemia Splenic atrophy (1) MLNC (2) Harmon GS 21 Clin Gastro Hep 1 Septicemia by Klebsiella Splenic atrophy

20 Risk for pneumococcal sepsis in coeliac disease 15,325 coeliac patients 14,494 hospitalized patients 2,44 coeliac patients 2,956 asplenic patients 5 vs hospitalized patients vs general population 5 Coeliac patients Asplenic patients 1 Sepsis Hip fracture Lymphoma Relative Risk Relative Risk Absolute Risk p<.1 p<.1 Ludvigsson et al. Gut 28 Thomas et al. EJGH 28 Walters et al. Gut 28

21 Septicemia and pneumonia as frequent causes of death in coeliac patients: the Swedish cohort (1,32 pts) Standardized Mortality Ratio All malignancies 2.9 All infections 7.1 Septicemia 2.8 Respiratory diseases 2.9 Pneumonia Peters et al. Arch Intern Med 23

22 Use of anti-pneumococcal vaccines in at risk populations in UK (Q-research database 21-25) 8 Splenectomy (n. 2,1) Coeliac disease / sickle cell anemia (n. 3,584) % vaccinated patients Pebody et al. Epidemiol Infect 28

23 Traditional polysaccharide and new conjugate anti-pneumococcal vaccines used in the prophylactic management of asplenic/hyposplenic patients VACCINE BRAND NAME STRUCTURE MECHANISM SEROTYPES INDICATIONS PPV23 Pneumovax Polysaccharide T-cell independent 1, 2, 3, 4, 5, 6B, 7F, 8, 9N, 9V, 1A, 11A, 12F, 14, 15B, 17F, 18C, 19A, 19F, 2, 22F, 23F, 33F - Asplenic or hyposplenic adults - Asplenic or hyposplenic children > 5 yrs PCV13 Prevnar Protein-conjugate (CRM197 protein) T-cell dependent 1, 3, 4, 5, 6A, 6B, 7F, 9V, 14, 18C, 19A, 19F, 23F - Asplenic or hyposplenic children < 5 yrs

24 Traditional polysaccharide and new conjugate anti-pneumococcal vaccines used in the prophylactic management of asplenic/hyposplenic patients VACCINE BRAND NAME STRUCTURE MECHANISM SEROTYPES INDICATIONS PPV23 Pneumovax Polysaccharide T-cell independent 1, 2, 3, 4, 5, 6B, 7F, 8, 9N, 9V, 1A, 11A, 12F, 14, 15B, 17F, 18C, 19A, 19F, 2, 22F, 23F, 33F - Asplenic or hyposplenic adults - Asplenic or hyposplenic children > 5 yrs PCV13 Prevnar Protein-conjugate (CRM197 protein) T-cell dependent 1, 3, 4, 5, 6A, 6B, 7F, 9V, 14, 18C, 19A, 19F, 23F - Asplenic or hyposplenic children < 5 yrs - Adult patients with major hyposplenism

25 Asplenia/hyposplenism-related thromboembolism Splenectomy Coeliac disease Inflammatory bowel disease Whipple s disease Pitted red cells (%) p=.7 r s =.66 Platelet count (x1 3 /µl) Di Sabatino et al. Am J Gastro 29

26 Risk of thromboembolism in 14,27 patients with coeliac disease versus 69,48 matched reference individuals Hazard ratios 2 1 p< p< Reference individuals Coeliac patients -15 yrs 16 yrs Age at diagnosis Ludvigsson et al. Br J Haematol 27

27 Critical issues in coeliac disease-associated hyposplenism 1. When to evaluate splenic function 2. How to measure splenic function 3. When to recommend prophylactic vaccination 4. What is the cause of hyposplenism

28 Critical issues in coeliac disease-associated hyposplenism 1. When to evaluate splenic function in CD Patients with complications (RCD, UJI, EATL, collagenous sprue) Patients with concomitant autoimmune disorders Patients with old age at diagnosis Patients with previous history of major infections/sepsis Patients with mesenteric lymph node cavitation and/or small sized spleen (φ F <7.5cm; φ M <8.cm) at abdominal US or CT

29 Two-thirds of individuals with small sized spleen (φ F <7.5cm; φ M <8.cm) incidentally detected at abdominal US are hyposplenic hyposplenic patients 24 Pitted red cells (%) Splenectomized patients (n=52) Patients with small sized spleen (n=128) Di Sabatino et al. Intern Emerg Med 211

30 Critical issues in coeliac disease-associated hyposplenism 2. How to measure splenic function Pitted red cell counting by phase-interference microscopy Flow cytometric analysis of circulating memory B cells Flow cytometric detection of circulating Howell-Jolly bodies % HJB (CD71 - /TOPRO + ) p=.128 r s =.73 Splenectomized % PITTED RED CELLS p=.2 r s =.83 Hyposplenic 1 15 % PITTED RED CELLS

31 Critical 3. When issues to in recommend coeliac disease-associated prophylactic vaccination hyposplenism Pitted red cells (%) SPLENECTOMIZED PATIENTS Pitted red cells (%) HYPOSPLENIC COELIAC PATIENTS IgM-memory B cells (% total B cells) IgM-memory B cells (% total B cells)

32 4. What is the cause of hyposplenism To clarify mutual connections between spleen and gut Spleen Gut

33 The spleen plays a major function in the protection of gut mucosa Asplenic Asplenic Control Di Sabatino et al. FISMAD, Naples, March 212 Rosado et al. Mucosal Immunol 29

34 Oral tolerance to deamidated gliadin in HLA-DQ2 transgenic mice is predominantly mounted in the spleen Deamidated gliadin Ovalbumine Du Pré et al. Gastroenterology 211

35

36 Response to pneumococcal vaccine in 1 patients with coeliac disease Eusplenic coeliac patients Hyposplenic coeliac patients 12 Number of serotypes in which pts achieved a 2-fold rise in antibody levels Pt.#1 Pt.#2 Pt.#3 Pt.#4 Pt.#5 Pt.#6 Pt.#7 Pt.#8 Pt.#9 Pt.#1 McKinley et al. J Clin Gastroenterol 1995

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