Hepatitis B Reactivation in Rheumatic Diseases: Screening and Prevention

Rheumatic Disease Clinics of North America

Volumn 43, Issue 1, 2017, Pages 133-149

  Koutsianas, Christos ^a,b   Thomas, Konstantinos ^a   Vassilopoulos, Dimitrios ^a  

^a UNIVERSITY OF ATHENS   (Greece)

^b RUSSELLS HALL HOSPITAL   (United Kingdom)

Author keywords

Abatacept; Biologics; Disease modifying antirheumatic drugs; Hepatitis B; Reactivation; Rheumatic diseases; Rituximab; TNF inhibitors; Tocilizumab

Indexed keywords

ABATACEPT; ADEFOVIR; ANTIRHEUMATIC AGENT; ANTIVIRUS AGENT; AZATHIOPRINE; BIOLOGICAL PRODUCT; CALCINEURIN INHIBITOR; CORTICOSTEROID; CYCLOPHOSPHAMIDE; DISEASE MODIFYING ANTIRHEUMATIC DRUG; DOXORUBICIN; ENTECAVIR; HYDROXYCHLOROQUINE; IMATINIB; LAMIVUDINE; LEFLUNOMIDE; METHOTREXATE; NILOTINIB; PREDNISOLONE; RITUXIMAB; SALAZOSULFAPYRIDINE; SECUKINUMAB; TELBIVUDINE; TENOFOVIR; TOCILIZUMAB; TOFACITINIB; TUMOR NECROSIS FACTOR INHIBITOR; UNINDEXED DRUG; USTEKINUMAB; VINCRISTINE; IMMUNOSUPPRESSIVE AGENT;

ALGORITHM; ANCA ASSOCIATED VASCULITIS; BREAST CANCER; CLINICAL PRACTICE; DRUG MEGADOSE; HEMATOLOGIC DISEASE; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; INFECTION RISK; JUVENILE RHEUMATOID ARTHRITIS; LYMPHOMA; MORBIDITY; MORTALITY; PATIENT MONITORING; PREVALENCE; PRIORITY JOURNAL; PSORIASIS; PSORIATIC ARTHRITIS; REVIEW; RHEUMATIC DISEASE; RHEUMATOID ARTHRITIS; SCREENING; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC SCLEROSIS; VASCULITIS; VIRUS REACTIVATION; HEPATITIS B, CHRONIC; IMMUNOLOGY; MASS SCREENING; RHEUMATIC DISEASES; VIRUS ACTIVATION;

ANTIRHEUMATIC AGENTS; ANTIVIRAL AGENTS; HEPATITIS B, CHRONIC; HUMANS; IMMUNOSUPPRESSIVE AGENTS; MASS SCREENING; RHEUMATIC DISEASES; VIRUS ACTIVATION;

EID: 85002410897     PISSN: 0889857X     EISSN: 15583163     Source Type: Journal    
DOI: 10.1016/j.rdc.2016.09.012     Document Type: Review

References (92)

1. 1 Lok, A.S., Ward, J.W., Perrillo, R.P., et al. Reactivation of hepatitis B during immunosuppressive therapy: potentially fatal yet preventable. Ann Intern Med 156 (2012), 743–745.
2. 2 Vassilopoulos, D., Calabrese, L.H., Management of rheumatic disease with comorbid HBV or HCV infection. Nat Rev Rheumatol 8 (2012), 348–357.
3. 3 Hadziyannis, S.J., Vassilopoulos, D., Hadziyannis, E., The natural course of chronic hepatitis B virus infection and its management. Adv Pharmacol 67 (2013), 247–291.
4. 4 Trepo, C., Chan, H.L., Lok, A., Hepatitis B virus infection. Lancet 384 (2014), 2053–2063.
5. 5 Dienstag, J.L., Hepatitis B virus infection. N Engl J Med 359 (2008), 1486–1500.
6. 6 Iqbal, K., Klevens, R.M., Kainer, M.A., et al. Epidemiology of acute hepatitis B in the United States from population-based surveillance, 2006-2011. Clin Infect Dis 61 (2015), 584–592.
7. 7 Roberts, H., Kruszon-Moran, D., Ly, K.N., et al. Prevalence of chronic hepatitis B virus (HBV) infection in U.S. households: National Health and Nutrition Examination Survey (NHANES), 1988-2012. Hepatology 63 (2016), 388–397.
8. 8 Ioannou, G.N., Hepatitis B virus in the United States: infection, exposure, and immunity rates in a nationally representative survey. Ann Intern Med 154 (2011), 319–328.
9. 9 Molto, A., Etcheto, A., van der Heijde, D., et al. Prevalence of comorbidities and evaluation of their screening in spondyloarthritis: results of the international cross-sectional ASAS-COMOSPA study. Ann Rheum Dis 75:6 (2016), 1016–1023.
10. 10 Dougados, M., Soubrier, M., Antunez, A., et al. Prevalence of comorbidities in rheumatoid arthritis and evaluation of their monitoring: results of an international, cross-sectional study (COMORA). Ann Rheum Dis 73 (2014), 62–68.
11. 11 Giardina, A.R., Ferraro, D., Ciccia, F., et al. No detection of occult HBV-DNA in patients with various rheumatic diseases treated with anti-TNF agents: a two-year prospective study. Clin Exp Rheumatol 31 (2013), 25–30.
12. 12 Vassilopoulos, D., Apostolopoulou, A., Hadziyannis, E., et al. Long-term safety of anti-TNF treatment in patients with rheumatic diseases and chronic or resolved hepatitis B virus infection. Ann Rheum Dis 69 (2010), 1352–1355.
13. 13 Urata, Y., Uesato, R., Tanaka, D., et al. Prevalence of reactivation of hepatitis B virus replication in rheumatoid arthritis patients. Mod Rheumatol 21 (2011), 16–23.
14. 14 Mori, S., Past hepatitis B virus infection in rheumatoid arthritis patients receiving biological and/or nonbiological disease-modifying antirheumatic drugs. Mod Rheumatol 21 (2011), 621–627.
15. 15 Tan, J., Zhou, J., Zhao, P., et al. Prospective study of HBV reactivation risk in rheumatoid arthritis patients who received conventional disease-modifying antirheumatic drugs. Clin Rheumatol 31 (2012), 1169–1175.
16. 16 Mori, S., Fujiyama, S., Hepatitis B virus reactivation associated with antirheumatic therapy: risk and prophylaxis recommendations. World J Gastroenterol 21 (2015), 10274–10289.
17. 17 Terrault, N.A., Bzowej, N.H., Chang, K.M., et al. AASLD guidelines for treatment of chronic hepatitis B. Hepatology 63 (2016), 261–283.
18. 18 Koutsianas, C., Thomas, K., Vassilopoulos, D., Prevention of HBV reactivation in patients treated with biologic agents. Expert Rev Clin Pharmacol, 2016, 1–11.
19. 19 Raimondo, G., Allain, J.P., Brunetto, M.R., et al. Statements from the Taormina expert meeting on occult hepatitis B virus infection. J Hepatol 49 (2008), 652–657.
20. 20 Kato, M., Atsumi, T., Reactivation of occult hepatitis B virus infection in patients with rheumatic diseases: pathogenesis, risk assessment and prevention. Rheumatol Int 36 (2016), 635–641.
21. 21 Squadrito, G., Spinella, R., Raimondo, G., The clinical significance of occult HBV infection. Ann Gastroenterol 27 (2014), 15–19.
22. 22 Phillips, S., Chokshi, S., Riva, A., et al. CD8(+) T cell control of hepatitis B virus replication: direct comparison between cytolytic and noncytolytic functions. J Immunol 184 (2010), 287–295.
23. 23 Bertoletti, A., Ferrari, C., Innate and adaptive immune responses in chronic hepatitis B virus infections: towards restoration of immune control of viral infection. Gut 61 (2012), 1754–1764.
24. 24 Hoofnagle, J.H., Reactivation of hepatitis B. Hepatology 49 (2009), S156–S165.
25. 25 Hwang, J.P., Lok, A.S., Management of patients with hepatitis B who require immunosuppressive therapy. Nat Rev Gastroenterol Hepatol 11 (2014), 209–219.
26. 26 Di Bisceglie, A.M., Lok, A.S., Martin, P., et al. Recent US Food and drug administration warnings on hepatitis B reactivation with immune-suppressing and anticancer drugs: just the tip of the iceberg?. Hepatology 61 (2015), 703–711.
27. 27 Hsu, C., Tsou, H.H., Lin, S.J., et al. Chemotherapy-induced hepatitis B reactivation in lymphoma patients with resolved HBV infection: a prospective study. Hepatology 59 (2014), 2092–2100.
28. 28 Hoofnagle, J.H., Davis, G.L., Pappas, S.C., et al. A short course of prednisolone in chronic type B hepatitis. Report of a randomized, double-blind, placebo-controlled trial. Ann Intern Med 104 (1986), 12–17.
29. 29 Perrillo, R.P., Schiff, E.R., Davis, G.L., et al. A randomized, controlled trial of interferon alfa-2b alone and after prednisone withdrawal for the treatment of chronic hepatitis B. The Hepatitis Interventional Therapy Group. N Engl J Med 323 (1990), 295–301.
30. 30 Cheng, A.L., Hsiung, C.A., Su, I.J., et al. Steroid-free chemotherapy decreases risk of hepatitis B virus (HBV) reactivation in HBV-carriers with lymphoma. Hepatology 37 (2003), 1320–1328.
31. 31 Kim, T.W., Kim, M.N., Kwon, J.W., et al. Risk of hepatitis B virus reactivation in patients with asthma or chronic obstructive pulmonary disease treated with corticosteroids. Respirology 15 (2010), 1092–1097.
32. 32 Nakanishi, K., Ishikawa, M., Nakauchi, M., et al. Antibody to hepatitis B e positive hepatitis induced by withdrawal of steroid therapy for polymyositis: response to interferon-alpha and cyclosporin A. Intern Med 37 (1998), 519–522.
33. 33 Zanati, S.A., Locarnini, S.A., Dowling, J.P., et al. Hepatic failure due to fibrosing cholestatic hepatitis in a patient with pre-surface mutant hepatitis B virus and mixed connective tissue disease treated with prednisolone and chloroquine. J Clin Virol 31 (2004), 53–57.
34. 34 Cheng, J., Li, J.B., Sun, Q.L., et al. Reactivation of hepatitis B virus after steroid treatment in rheumatic diseases. J Rheumatol 38 (2011), 181–182.
35. 35 Perrillo, R.P., Gish, R., Falck-Ytter, Y.T., American Gastroenterological Association Institute technical review on prevention and treatment of hepatitis B virus reactivation during immunosuppressive drug therapy. Gastroenterology 148 (2015), 221–244.
36. 36 Tang, K.T., Hung, W.T., Chen, Y.H., et al. Methotrexate is not associated with increased liver cirrhosis in a population-based cohort of rheumatoid arthritis patients with chronic hepatitis B. Sci Rep, 6, 2016, 22387.
37. 37 Laohapand, C., Arromdee, E., Tanwandee, T., Long-term use of methotrexate does not result in hepatitis B reactivation in rheumatologic patients. Hepatol Int 9 (2015), 202–208.
38. 38 Oshima, Y., Tsukamoto, H., Tojo, A., Association of hepatitis B with antirheumatic drugs: a case-control study. Mod Rheumatol 23 (2013), 694–704.
39. 39 Mo, Y.Q., Liang, A.Q., Ma, J.D., et al. Discontinuation of antiviral prophylaxis correlates with high prevalence of hepatitis B virus (HBV) reactivation in rheumatoid arthritis patients with HBV carrier state: a real-world clinical practice. BMC Musculoskelet Disord, 15, 2014, 449.
40. 40 Droz, N., Gilardin, L., Cacoub, P., et al. Kinetic profiles and management of hepatitis B virus reactivation in patients with immune-mediated inflammatory diseases. Arthritis Care Res (Hoboken) 65 (2013), 1504–1514.
41. 41 Carroll, M.B., Forgione, M.A., Use of tumor necrosis factor alpha inhibitors in hepatitis B surface antigen-positive patients: a literature review and potential mechanisms of action. Clin Rheumatol 29 (2010), 1021–1029.
42. 42 Perez-Alvarez, R., Diaz-Lagares, C., Garcia-Hernandez, F., et al. Hepatitis B virus (HBV) reactivation in patients receiving tumor necrosis factor (TNF)-targeted therapy: analysis of 257 cases. Medicine (Baltimore) 90 (2011), 359–371.
43. 43 Lan, J.L., Chen, Y.M., Hsieh, T.Y., et al. Kinetics of viral loads and risk of hepatitis B virus reactivation in hepatitis B core antibody-positive rheumatoid arthritis patients undergoing anti-tumour necrosis factor alpha therapy. Ann Rheum Dis 70 (2011), 1719–1725.
44. 44 Ryu, H.H., Lee, E.Y., Shin, K., et al. Hepatitis B virus reactivation in rheumatoid arthritis and ankylosing spondylitis patients treated with anti-TNF alpha agents: a retrospective analysis of 49 cases. Clin Rheumatol 31 (2012), 931–936.
45. 45 Ye, H., Zhang, X.W., Mu, R., et al. Anti-TNF therapy in patients with HBV infection–analysis of 87 patients with inflammatory arthritis. Clin Rheumatol 33 (2014), 119–123.
46. 46 Lee, Y.H., Bae, S.C., Song, G.G., Hepatitis B virus (HBV) reactivation in rheumatic patients with hepatitis core antigen (HBV occult carriers) undergoing anti-tumor necrosis factor therapy. Clin Exp Rheumatol 31 (2013), 118–121.
47. 47 Yeo, W., Chan, T.C., Leung, N.W., et al. Hepatitis B virus reactivation in lymphoma patients with prior resolved hepatitis B undergoing anticancer therapy with or without rituximab. J Clin Oncol 27 (2009), 605–611.
48. 48 Pei, S.N., Chen, C.H., Lee, C.M., et al. Reactivation of hepatitis B virus following rituximab-based regimens: a serious complication in both HBsAg-positive and HBsAg-negative patients. Ann Hematol 89 (2010), 255–262.
49. 49 Koo, Y.X., Tay, M., Teh, Y.E., et al. Risk of hepatitis B virus (HBV) reactivation in hepatitis B surface antigen negative/hepatitis B core antibody positive patients receiving rituximab-containing combination chemotherapy without routine antiviral prophylaxis. Ann Hematol 90 (2011), 1219–1223.
50. 50 Kim, S.J., Hsu, C., Song, Y.Q., et al. Hepatitis B virus reactivation in B-cell lymphoma patients treated with rituximab: analysis from the Asia Lymphoma Study Group. Eur J Cancer 49 (2013), 3486–3496.
51. 51 Pyrpasopoulou, A., Douma, S., Vassiliadis, T., et al. Reactivation of chronic hepatitis B virus infection following rituximab administration for rheumatoid arthritis. Rheumatol Int 31 (2011), 403–404.
52. 52 Mitroulis, I., Hatzara, C., Kandili, A., et al. Long-term safety of rituximab in patients with rheumatic diseases and chronic or resolved hepatitis B virus infection. Ann Rheum Dis 72 (2013), 308–310.
53. 53 Barone, M., Notarnicola, A., Lopalco, G., et al. Safety of long-term biologic therapy in rheumatologic patients with a previously resolved hepatitis B viral infection. Hepatology 62 (2015), 40–46.
54. 54 van Vollenhoven, R.F., Fleischmann, R.M., Furst, D.E., et al. Long-term safety of rituximab: final report of the rheumatoid arthritis global clinical trial program over 11 years. J Rheumatol 42 (2015), 1761–1766.
55. 55 Varisco, V., Vigano, M., Batticciotto, A., et al. Low risk of hepatitis B virus reactivation in HBsAg-negative/Anti-HBc-positive carriers receiving rituximab for rheumatoid arthritis: a retrospective multicenter Italian study. J Rheumatol 43:5 (2016), 869–874.
56. 56 Ghrenassia, E., Mekinian, A., Rouaghe, S., et al. Reactivation of resolved hepatitis B during rituximab therapy for rheumatoid arthritis. Joint Bone Spine 79 (2012), 100–101.
57. 57 Salman-Monte, T.C., Lisbona, M.P., Garcia-Retortillo, M., et al. Reactivation of hepatitis virus B infection in a patient with rheumatoid arthritis after treatment with rituximab. Reumatol Clin 10 (2014), 196–197.
58. 58 Kim, P.S., Ho, G.Y., Prete, P.E., et al. Safety and efficacy of abatacept in eight rheumatoid arthritis patients with chronic hepatitis B. Arthritis Care Res (Hoboken) 64 (2012), 1265–1268.
59. 59 Padovan, M., Filippini, M., Tincani, A., et al. Safety of abatacept in rheumatoid arthritis with serological evidence of past or present hepatitis B virus infection. Arthritis Care Res (Hoboken) 68:6 (2016), 738–743.
60. 60 Germanidis, G., Hytiroglou, P., Zakalka, M., et al. Reactivation of occult hepatitis B virus infection, following treatment of refractory rheumatoid arthritis with abatacept. J Hepatol 56 (2012), 1420–1421.
61. 61 Fanouriakis, A., Vassilopoulos, D., Repa, A., et al. Hepatitis B reactivation following treatment with abatacept in a patient with past hepatitis B virus infection. Rheumatology (Oxford) 53 (2014), 195–196.
62. 62 Nagashima, T., Minota, S., Long-term tocilizumab therapy in a patient with rheumatoid arthritis and chronic hepatitis B. Rheumatology (Oxford) 47 (2008), 1838–1840.
63. 63 Nakamura, J., Nagashima, T., Nagatani, K., et al. Reactivation of hepatitis B virus in rheumatoid arthritis patients treated with biological disease-modifying antirheumatic drugs. Int J Rheum Dis 19:5 (2016), 470–475.
64. 64 Chiu, H.Y., Chen, C.H., Wu, M.S., et al. The safety profile of ustekinumab in the treatment of patients with psoriasis and concurrent hepatitis B or C. Br J Dermatol 169 (2013), 1295–1303.
65. 65 Koskinas, J., Tampaki, M., Doumba, P.P., et al. Hepatitis B virus reactivation during therapy with ustekinumab for psoriasis in a hepatitis B surface-antigen-negative anti-HBs-positive patient. Br J Dermatol 168 (2013), 679–680.
66. 66 Lai, G.M., Yan, S.L., Chang, C.S., et al. Hepatitis B reactivation in chronic myeloid leukemia patients receiving tyrosine kinase inhibitor. World J Gastroenterol 19 (2013), 1318–1321.
67. 67 Walker, E.J., Simko, J.P., Ko, A.H., Hepatitis B viral reactivation secondary to imatinib treatment in a patient with gastrointestinal stromal tumor. Anticancer Res 34 (2014), 3629–3634.
68. 68 Wang, Y.D., Cui, G.H., Li, M., et al. Hepatitis B virus reactivation in a chronic myeloid leukemia patient treated with imatinib mesylate. Chin Med J (Engl) 125 (2012), 2636–2637.
69. 69 Weinbaum, C.M., Williams, I., Mast, E.E., et al. Recommendations for identification and public health management of persons with chronic hepatitis B virus infection. MMWR Recomm Rep 57 (2008), 1–20.
70. 70 Sarin, S.K., Kumar, M., Lau, G.K., et al. Asian-Pacific clinical practice guidelines on the management of hepatitis B: a 2015 update. Hepatol Int 10 (2016), 1–98.
71. 71 Lok, A.S., McMahon, B.J., Chronic hepatitis B: update 2009. Hepatology 50 (2009), 661–662.
72. 72 Zurawska, U., Hicks, L.K., Woo, G., et al. Hepatitis B virus screening before chemotherapy for lymphoma: a cost-effectiveness analysis. J Clin Oncol 30 (2012), 3167–3173.
73. 73 Wong, W.W., Hicks, L.K., Tu, H.A., et al. Hepatitis B virus screening before adjuvant chemotherapy in patients with early-stage breast cancer: a cost-effectiveness analysis. Breast Cancer Res Treat 151 (2015), 639–652.
74. 74 Day, F.L., Karnon, J., Rischin, D., Cost-effectiveness of universal hepatitis B virus screening in patients beginning chemotherapy for solid tumors. J Clin Oncol 29 (2011), 3270–3277.
75. 75 Saag, K.G., Teng, G.G., Patkar, N.M., et al. American College of Rheumatology 2008 recommendations for the use of nonbiologic and biologic disease-modifying antirheumatic drugs in rheumatoid arthritis. Arthritis Rheum 59 (2008), 762–784.
76. 76 Weinbaum, C.M., Mast, E.E., Ward, J.W., Recommendations for identification and public health management of persons with chronic hepatitis B virus infection. Hepatology 49 (2009), S35–S44.
77. 77 Motaparthi, K., Stanisic, V., Van Voorhees, A.S., et al. From the medical board of the National Psoriasis Foundation: recommendations for screening for hepatitis B infection prior to initiating anti-tumor necrosis factor-alfa inhibitors or other immunosuppressive agents in patients with psoriasis. J Am Acad Dermatol 70 (2014), 178–186.
78. 78 European Association for the Study of the Liver, EASL clinical practice guidelines: management of chronic hepatitis B virus infection. J Hepatol 57 (2012), 167–185.
79. 79 Dervite, I., Hober, D., Morel, P., Acute hepatitis B in a patient with antibodies to hepatitis B surface antigen who was receiving rituximab. N Engl J Med 344 (2001), 68–69.
80. 80 Singh, J.A., Saag, K.G., Bridges, S.L. Jr., et al. 2015 American College of Rheumatology guideline for the treatment of rheumatoid arthritis. Arthritis Rheumatol 68 (2016), 1–26.
81. 81 Sampedro, B., Hernandez-Lopez, C., Ferrandiz, J.R., et al. Computerized physician order entry-based system to prevent HBV reactivation in patients treated with biologic agents: the PRESCRIB project. Hepatology 60 (2014), 106–113.
82. 82 Mast, E.E., Weinbaum, C.M., Fiore, A.E., et al. A comprehensive immunization strategy to eliminate transmission of hepatitis B virus infection in the United States: recommendations of the Advisory Committee on Immunization Practices (ACIP) part II: immunization of adults. MMWR Recomm Rep 55 (2006), 1–33.
83. 83 Reddy, K.R., Beavers, K.L., Hammond, S.P., et al. American Gastroenterological Association Institute guideline on the prevention and treatment of hepatitis B virus reactivation during immunosuppressive drug therapy. Gastroenterology 148 (2015), 215–219.
84. 84 Kishida, D., Okuda, Y., Onishi, M., et al. Successful tocilizumab treatment in a patient with adult-onset Still's disease complicated by chronic active hepatitis B and amyloid A amyloidosis. Mod Rheumatol 21 (2011), 215–218.
85. 85 Tsuboi, H., Tsujii, A., Nampei, A., et al. A patient with rheumatoid arthritis treated with tocilizumab together with lamivudine prophylaxis after remission of infliximab-reactivated hepatitis B. Mod Rheumatol 21 (2011), 701–705.
86. 86 Raymundo, A.R., Facin, A.P., Silva de Castro, C.C., et al. Safety of ustekinumab in severe psoriasis with chronic hepatitis B. Indian J Dermatol Venereol Leprol 82 (2016), 326–328.
87. 87 Steglich, R.B., Meneghello, L.P., Carvalho, A.V., et al. The use of ustekinumab in a patient with severe psoriasis and positive HBV serology. An Bras Dermatol 89 (2014), 652–654.
88. 88 Lau, G.K., Yiu, H.H., Fong, D.Y., et al. Early is superior to deferred preemptive lamivudine therapy for hepatitis B patients undergoing chemotherapy. Gastroenterology 125 (2003), 1742–1749.
89. 89 Hsu, C., Hsiung, C.A., Su, I.J., et al. A revisit of prophylactic lamivudine for chemotherapy-associated hepatitis B reactivation in non-Hodgkin's lymphoma: a randomized trial. Hepatology 47 (2008), 844–853.
90. 90 Loomba, R., Rowley, A., Wesley, R., et al. Systematic review: the effect of preventive lamivudine on hepatitis B reactivation during chemotherapy. Ann Intern Med 148 (2008), 519–528.
91. 91 Huang, H., Li, X., Zhu, J., et al. Entecavir vs lamivudine for prevention of hepatitis B virus reactivation among patients with untreated diffuse large B-cell lymphoma receiving R-CHOP chemotherapy: a randomized clinical trial. JAMA 312 (2014), 2521–2530.
92. 92 Huang, Y.H., Hsiao, L.T., Hong, Y.C., et al. Randomized controlled trial of entecavir prophylaxis for rituximab-associated hepatitis B virus reactivation in patients with lymphoma and resolved hepatitis B. J Clin Oncol 31 (2013), 2765–2772.