Skip to main content
Top
Published in: Osteoporosis International 4/2013

01-04-2013 | Original Article

Osteoporosis/osteopenia as an independent factor associated with periodontitis in postmenopausal women: a case–control study

Authors: J. S. Passos, M. I. P. Vianna, I. S. Gomes-Filho, S. S. Cruz, M. L. Barreto, L. Adan, C. K. Rösing, E. M. M. Cerqueira, S. C. Trindade, J. M. F. Coelho

Published in: Osteoporosis International | Issue 4/2013

Login to get access

Abstract

Summary

This study investigated whether osteoporosis/osteopenia has an influence on the progression of periodontitis in postmenopausal women. The findings highlight that postmenopausal women with osteoporosis/osteopenia had a greater chance of presenting periodontitis than those with normal bone mineral density, particularly among nonusers of osteoporosis medications and women with a greater number of remaining teeth, showing that osteoporosis/osteopenia has had an influence on the progression of periodontitis.

Introduction

This study investigated whether osteoporosis/osteopenia has an influence on the progression of periodontitis in postmenopausal women and explored the effects of use of osteoporosis medication and tooth loss on this association.

Methods

This case–control study involved 521 postmenopausal women, with minimum age of 50 years, in Feira de Santana, Bahia, Brazil. Sociodemographic characteristics, health conditions/medications, and lifestyle habits were recorded. A complete periodontal examination was performed and periodontitis was diagnosed. Bone mineral density was evaluated through lumbar spine and femoral bone densitometry, obtained using dual-energy X-ray absorptiometry. Logistic regression was used to calculate the strength of association between the occurrences of osteoporosis/osteopenia and periodontitis.

Results

Women with osteoporosis/osteopenia were twice as likely to present periodontitis, as were those with normal bone mineral density, even after adjusting for smoking, age, family income, and last visit to dentist (odds ratios (OR)adjusted = 2.24, 95 % CI [1.24–4.06], p = 0.008). Among nonusers of osteoporosis medication (ORadjusted = 2.51, 95 % CI [1.33–4.73], p = 0.004) and women with at least 10 remaining teeth (ORadjusted = 2.50 95 % CI [1.18–5.27], p = 0.02), the odds ratio was higher and statistically significant.

Conclusions

These findings highlight that postmenopausal women with osteoporosis/osteopenia had a greater chance of presenting periodontitis than those with normal bone mineral density, particularly among nonusers of osteoporosis medications and women with a greater number of remaining teeth.
Literature
2.
go back to reference Lener UH (2006) Inflammation-induced bone remodeling in periodontal disease and the influence of post-menopausal osteoporosis. J Dent Res 85:596–607CrossRef Lener UH (2006) Inflammation-induced bone remodeling in periodontal disease and the influence of post-menopausal osteoporosis. J Dent Res 85:596–607CrossRef
3.
go back to reference Wactawski-Wende J, Hausmann E, Hovey K, Trevisan M, Grossi S, Genco RJ (2005) The association between osteoporosis and alveolar crestal height in postmenopausal women. J Periodontol 76:2116–2124PubMedCrossRef Wactawski-Wende J, Hausmann E, Hovey K, Trevisan M, Grossi S, Genco RJ (2005) The association between osteoporosis and alveolar crestal height in postmenopausal women. J Periodontol 76:2116–2124PubMedCrossRef
4.
go back to reference Brennan-Calanan RM, Genco RJ, Wilding GE, Hovey KM, Trevisan M, Wactawski-Wende J (2008) Osteoporosis and oral infection: independent risk factors for oral bone loss. J Dent Res 87:323–327PubMedCrossRef Brennan-Calanan RM, Genco RJ, Wilding GE, Hovey KM, Trevisan M, Wactawski-Wende J (2008) Osteoporosis and oral infection: independent risk factors for oral bone loss. J Dent Res 87:323–327PubMedCrossRef
5.
go back to reference Payne JB, Reinhardt RA, Nummikoski PV, Patil KD (1999) Longitudinal alveolar bone loss in postmenopausal osteoporotic/osteopenic women. Osteoporos Int 10:34–40PubMedCrossRef Payne JB, Reinhardt RA, Nummikoski PV, Patil KD (1999) Longitudinal alveolar bone loss in postmenopausal osteoporotic/osteopenic women. Osteoporos Int 10:34–40PubMedCrossRef
6.
go back to reference Borrell LN, Papapanou PN (2005) Analytical epidemiology of periodontitis. J Clin Periodontol 32:132–158PubMedCrossRef Borrell LN, Papapanou PN (2005) Analytical epidemiology of periodontitis. J Clin Periodontol 32:132–158PubMedCrossRef
7.
go back to reference Norderyd OM, Grossi SG, Machtei EE, Zambon JJ, Hausmann E, Dunford RG, Genco RJ (1993) Periodontal status of women taking postmenopausal estrogen supplementation. J Periodontol 64:957–962PubMedCrossRef Norderyd OM, Grossi SG, Machtei EE, Zambon JJ, Hausmann E, Dunford RG, Genco RJ (1993) Periodontal status of women taking postmenopausal estrogen supplementation. J Periodontol 64:957–962PubMedCrossRef
8.
go back to reference Reinhardt RA, Payne JB, Maze CA, Patil KD, Gallagher SJ, Mattson JS (1999) Influence of estrogen and osteopenia/osteoporosis on clinical periodontitis in postmenopausal women. J Periodontol 70:823–828PubMedCrossRef Reinhardt RA, Payne JB, Maze CA, Patil KD, Gallagher SJ, Mattson JS (1999) Influence of estrogen and osteopenia/osteoporosis on clinical periodontitis in postmenopausal women. J Periodontol 70:823–828PubMedCrossRef
9.
go back to reference Jabbar S, Drury J, Fordham J, Datta HK, Francis RM, Tuck SP (2011) Plasma vitamin D and cytokines in periodontal disease and postmenopausal osteoporosis. J Periodontal Res 46:97–104PubMedCrossRef Jabbar S, Drury J, Fordham J, Datta HK, Francis RM, Tuck SP (2011) Plasma vitamin D and cytokines in periodontal disease and postmenopausal osteoporosis. J Periodontal Res 46:97–104PubMedCrossRef
10.
go back to reference Pilgram TK, Hildebolt CF, Dotson M, Cohen SC, Hauser JF, Kardaris E, Civitelli R (2002) Relationships between clinical attachment level and spine and hip bone mineral density: data from healthy postmenopausal women. J Periodontol 73:298–301PubMedCrossRef Pilgram TK, Hildebolt CF, Dotson M, Cohen SC, Hauser JF, Kardaris E, Civitelli R (2002) Relationships between clinical attachment level and spine and hip bone mineral density: data from healthy postmenopausal women. J Periodontol 73:298–301PubMedCrossRef
11.
go back to reference Famili P, Cauley J, Suzuki JB, Weyant R (2005) Longitudinal study of periodontal disease and edentulism with rates of bone loss in older women. J Periodontol 76:11–15PubMedCrossRef Famili P, Cauley J, Suzuki JB, Weyant R (2005) Longitudinal study of periodontal disease and edentulism with rates of bone loss in older women. J Periodontol 76:11–15PubMedCrossRef
12.
go back to reference Bullon P, Goberna B, Guerrero JM, Segura JJ, Perez-Cano R, Martinez-Sahuquillo A (2005) Serum, saliva, and gingival crevicular fluid osteocalcin: their relation to periodontal status and bone mineral density in postmenopausal women. J Periodontol 76:513–519PubMedCrossRef Bullon P, Goberna B, Guerrero JM, Segura JJ, Perez-Cano R, Martinez-Sahuquillo A (2005) Serum, saliva, and gingival crevicular fluid osteocalcin: their relation to periodontal status and bone mineral density in postmenopausal women. J Periodontol 76:513–519PubMedCrossRef
13.
go back to reference Sultan N, Rao J (2011) Association between periodontal disease and bone mineral density in postmenopausal women: a cross sectional study. Med Oral Patol Oral Circ Bucal 16:e440–e447CrossRef Sultan N, Rao J (2011) Association between periodontal disease and bone mineral density in postmenopausal women: a cross sectional study. Med Oral Patol Oral Circ Bucal 16:e440–e447CrossRef
14.
go back to reference Nicopoulou-Karayianni K, Tzoutzoukos P, Mitsea A, Karayiannis A, Tsiklakis K, Jacobs R, Lindh C, van der Stelt P, Allen P, Graham J, Horner K, Devlin H, Pavitt S, Yuan J (2009) Tooth loss and osteoporosis: the osteodent study. J Clin Period ontol 36:190–197CrossRef Nicopoulou-Karayianni K, Tzoutzoukos P, Mitsea A, Karayiannis A, Tsiklakis K, Jacobs R, Lindh C, van der Stelt P, Allen P, Graham J, Horner K, Devlin H, Pavitt S, Yuan J (2009) Tooth loss and osteoporosis: the osteodent study. J Clin Period ontol 36:190–197CrossRef
15.
go back to reference Haas AN, Rösing CK, Oppermann RV, Albandar JM, Susin C (2009) Association among menopause, hormone replacement therapy, and periodontal attachment loss in southern Brazilian women. J Periodontol 80:1380–1387PubMedCrossRef Haas AN, Rösing CK, Oppermann RV, Albandar JM, Susin C (2009) Association among menopause, hormone replacement therapy, and periodontal attachment loss in southern Brazilian women. J Periodontol 80:1380–1387PubMedCrossRef
16.
go back to reference Renvert S, Berglund J, Persson RE, Persson GR (2011) Osteoporosis and periodontitis in older subjects participating in the Swedish National Survey on Aging and Care (SNAC-Blekinge). Acta Odontol Scand 69(4):201–207PubMedCrossRef Renvert S, Berglund J, Persson RE, Persson GR (2011) Osteoporosis and periodontitis in older subjects participating in the Swedish National Survey on Aging and Care (SNAC-Blekinge). Acta Odontol Scand 69(4):201–207PubMedCrossRef
17.
go back to reference Inagaki K, Kurosu Y, Yoshinari N, Noguchi T, Krall EA, Garcia RI (2005) Efficacy of periodontal disease and tooth loss to screen for low bone mineral density in Japanese women. Calcif Tissue Int 77:9–14PubMedCrossRef Inagaki K, Kurosu Y, Yoshinari N, Noguchi T, Krall EA, Garcia RI (2005) Efficacy of periodontal disease and tooth loss to screen for low bone mineral density in Japanese women. Calcif Tissue Int 77:9–14PubMedCrossRef
18.
go back to reference Pihlstrom BL, Ortiz-Campos C, McHugh RB (1981) A randomized four-year study of periodontal therapy. J Periodontol 52:227–242PubMedCrossRef Pihlstrom BL, Ortiz-Campos C, McHugh RB (1981) A randomized four-year study of periodontal therapy. J Periodontol 52:227–242PubMedCrossRef
19.
go back to reference Ainamo J, Bay I (1975) Problems and proposals for recording gingivitis and plaque. Int Dent J 25:229–235PubMed Ainamo J, Bay I (1975) Problems and proposals for recording gingivitis and plaque. Int Dent J 25:229–235PubMed
20.
go back to reference Page RC, Eke PI (2007) Case definitions for use in population-based surveillance of periodontitis. J Periodontol 78:1387–1399PubMedCrossRef Page RC, Eke PI (2007) Case definitions for use in population-based surveillance of periodontitis. J Periodontol 78:1387–1399PubMedCrossRef
21.
go back to reference World Health Organization (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Geneva: WHO (technical reports series) World Health Organization (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Geneva: WHO (technical reports series)
22.
go back to reference Rothman KJ, Greenland S (1998) Modern epidemiology, 2nd edn. Lippincott, Philadelphia Rothman KJ, Greenland S (1998) Modern epidemiology, 2nd edn. Lippincott, Philadelphia
23.
go back to reference Al Habashneh R, Alchalabi H, Khader YS, Hazza’a AM, Odat Z, Johnson GK (2010) Association between periodontal disease and osteoporosis in postmenopausal women in Jordan. J Periodontol 81:1613–1621PubMedCrossRef Al Habashneh R, Alchalabi H, Khader YS, Hazza’a AM, Odat Z, Johnson GK (2010) Association between periodontal disease and osteoporosis in postmenopausal women in Jordan. J Periodontol 81:1613–1621PubMedCrossRef
24.
go back to reference Golub LM, Payne JB, Reinhardt RA, Nieman G (2006) Can systemic diseases co-induce (not just exacerbate) periodontitis? A hypothetical “two-hit” model. J Dent Res 85:102–105PubMedCrossRef Golub LM, Payne JB, Reinhardt RA, Nieman G (2006) Can systemic diseases co-induce (not just exacerbate) periodontitis? A hypothetical “two-hit” model. J Dent Res 85:102–105PubMedCrossRef
25.
go back to reference Golub LM, Ramamurthy NS, Llavaneras A, Ryan ME, Lee HM, Liu Y, Bain S, Sorsa T (1999) A chemically modified nonantimicrobial tetracycline (CMT-8) inhibits gingival matrix metalloproteinases, periodontal breakdown, and extra-oral bone loss in ovariectomized rats. Ann NY Acad Sci 878:290–310PubMedCrossRef Golub LM, Ramamurthy NS, Llavaneras A, Ryan ME, Lee HM, Liu Y, Bain S, Sorsa T (1999) A chemically modified nonantimicrobial tetracycline (CMT-8) inhibits gingival matrix metalloproteinases, periodontal breakdown, and extra-oral bone loss in ovariectomized rats. Ann NY Acad Sci 878:290–310PubMedCrossRef
26.
go back to reference Reinhardt RA, Stoner JA, Golub LM, Wolff MS, Lee HM, Meinberg TA, Lynch JC, Ryan ME, Sorsa T, Payne JB (2007) Efficacy of sub-antimicrobial dose doxycycline in post-menopausal women: clinical outcomes. J Clin Periodontol 34:768–775PubMedCrossRef Reinhardt RA, Stoner JA, Golub LM, Wolff MS, Lee HM, Meinberg TA, Lynch JC, Ryan ME, Sorsa T, Payne JB (2007) Efficacy of sub-antimicrobial dose doxycycline in post-menopausal women: clinical outcomes. J Clin Periodontol 34:768–775PubMedCrossRef
27.
go back to reference Rutger Persson G, Ohlsson O, Pettersson T, Renvert S (2003) Chronic periodontitis, a significant relationship with acute myocardial infarction. Eur Heart J 24:2108–2115PubMedCrossRef Rutger Persson G, Ohlsson O, Pettersson T, Renvert S (2003) Chronic periodontitis, a significant relationship with acute myocardial infarction. Eur Heart J 24:2108–2115PubMedCrossRef
28.
go back to reference Scannapieco FA, Dasanayake AP, Chhun N (2010) Does periodontal therapy reduce the risk for systemic diseases? Dent Clin North Am 54:163–181PubMedCrossRef Scannapieco FA, Dasanayake AP, Chhun N (2010) Does periodontal therapy reduce the risk for systemic diseases? Dent Clin North Am 54:163–181PubMedCrossRef
29.
go back to reference Wells G, Tugwell P, Shea B, Guyatt G, Peterson J, Zytaruk N, Robinson V, Henry D, O’Connell D, Cranney A, Osteoporosis Methodology Group and The Osteoporosis Research Advisory Group (2002) Meta-analysis of the efficacy of hormone replacement therapy in treating and preventing osteoporosis in postmenopausal women. Endoc Rev 23:529–539CrossRef Wells G, Tugwell P, Shea B, Guyatt G, Peterson J, Zytaruk N, Robinson V, Henry D, O’Connell D, Cranney A, Osteoporosis Methodology Group and The Osteoporosis Research Advisory Group (2002) Meta-analysis of the efficacy of hormone replacement therapy in treating and preventing osteoporosis in postmenopausal women. Endoc Rev 23:529–539CrossRef
30.
go back to reference Ciria-Recasens M, Blanch-Rubió J, Coll-Batet M, Del Pilar Lisbona-Pérez M, Díez-Perez A, Carbonell-Abelló J, Manasanch J, Pérez-Edo L (2011) Comparison of the effects of ossein-hydroxyapatite complex and calcium carbonate on bone metabolism in women with senile osteoporosis: a randomized, open-label, parallel-group, controlled, prospective study. Clin Drug Investig 31:817–824PubMedCrossRef Ciria-Recasens M, Blanch-Rubió J, Coll-Batet M, Del Pilar Lisbona-Pérez M, Díez-Perez A, Carbonell-Abelló J, Manasanch J, Pérez-Edo L (2011) Comparison of the effects of ossein-hydroxyapatite complex and calcium carbonate on bone metabolism in women with senile osteoporosis: a randomized, open-label, parallel-group, controlled, prospective study. Clin Drug Investig 31:817–824PubMedCrossRef
31.
go back to reference Rocha ML, Malacara JM, Sánchez-Marin FJ, Vazquez de la Torre CJ, Fajardo ME (2004) Effect of alendronate on periodontal disease in postmenopausal women: a randomized placebo-controlled trial. J Periodontol 75:1579–1585PubMedCrossRef Rocha ML, Malacara JM, Sánchez-Marin FJ, Vazquez de la Torre CJ, Fajardo ME (2004) Effect of alendronate on periodontal disease in postmenopausal women: a randomized placebo-controlled trial. J Periodontol 75:1579–1585PubMedCrossRef
32.
go back to reference Pizzo G, Guiglia R, Licata ME, Pizzo I, Davis JM, Giuliana G (2011) Effect of hormone replacement therapy (HRT) on periodontal status of postmenopausal women. Med Sci Monit 17:PH23–PH27PubMedCrossRef Pizzo G, Guiglia R, Licata ME, Pizzo I, Davis JM, Giuliana G (2011) Effect of hormone replacement therapy (HRT) on periodontal status of postmenopausal women. Med Sci Monit 17:PH23–PH27PubMedCrossRef
33.
go back to reference Palomo L, Buencamino-Francisco MC, Carey JJ, Sivanandy M, Thacker H (2011) Is long-term bisphosphonate therapy associated with benefits to the periodontium in postmenopausal women? Menopause 18:164–170PubMed Palomo L, Buencamino-Francisco MC, Carey JJ, Sivanandy M, Thacker H (2011) Is long-term bisphosphonate therapy associated with benefits to the periodontium in postmenopausal women? Menopause 18:164–170PubMed
34.
go back to reference Taguchi A, Sanada M, Suei Y, Ohtsuka M, Nakamoto T, Lee K, Tsuda M, Ohama K, Tanimoto K, Bollen AM (2004) Effect of estrogen use on tooth retention, oral bone height, and oral bone porosity in Japanese postmenopausal women. Menopause 11:556–562PubMedCrossRef Taguchi A, Sanada M, Suei Y, Ohtsuka M, Nakamoto T, Lee K, Tsuda M, Ohama K, Tanimoto K, Bollen AM (2004) Effect of estrogen use on tooth retention, oral bone height, and oral bone porosity in Japanese postmenopausal women. Menopause 11:556–562PubMedCrossRef
35.
go back to reference Civitelli R, Pilgram TK, Dotson M, Muckerman J, Lewandowski N, Armamento-Villareal R, Yokoyama-Crothers N, Kardaris EE, Hauser J, Cohen S, Hildebolt CF (2002) Alveolar and postcranial bone density in postmenopausal women receiving hormone/estrogen replacement therapy: a randomized, double-blind, placebo-controlled trial. Arch Intern Med 162:1409–1415PubMedCrossRef Civitelli R, Pilgram TK, Dotson M, Muckerman J, Lewandowski N, Armamento-Villareal R, Yokoyama-Crothers N, Kardaris EE, Hauser J, Cohen S, Hildebolt CF (2002) Alveolar and postcranial bone density in postmenopausal women receiving hormone/estrogen replacement therapy: a randomized, double-blind, placebo-controlled trial. Arch Intern Med 162:1409–1415PubMedCrossRef
36.
go back to reference Krall EA, Dawson-Hughes B, Hannan MT, Wilson PW, Kiel DP (1997) Postmenopausal estrogen replacement and tooth retention. Am J Med 102:536–542PubMedCrossRef Krall EA, Dawson-Hughes B, Hannan MT, Wilson PW, Kiel DP (1997) Postmenopausal estrogen replacement and tooth retention. Am J Med 102:536–542PubMedCrossRef
37.
go back to reference Susin C, Oppermann RV, Haugejorden O, Albandar JM (2005) Tooth loss and associated risk indicators in an adult urban population from south Brazil. Acta Odontol Scand 63:85–93PubMed Susin C, Oppermann RV, Haugejorden O, Albandar JM (2005) Tooth loss and associated risk indicators in an adult urban population from south Brazil. Acta Odontol Scand 63:85–93PubMed
38.
go back to reference Hugo FN, Hilgert JB, de Sousa ML, da Silva DD, Pucca GA Jr (2007) Correlates of partial tooth loss and edentulism in the Brazilian elderly. Community Dent Oral Epidemiol 35:224–232PubMedCrossRef Hugo FN, Hilgert JB, de Sousa ML, da Silva DD, Pucca GA Jr (2007) Correlates of partial tooth loss and edentulism in the Brazilian elderly. Community Dent Oral Epidemiol 35:224–232PubMedCrossRef
39.
go back to reference Albandar JM (2002) Global risk factors and risk indicators for periodontal diseases. J Periodontol 2000(29):177–206 Albandar JM (2002) Global risk factors and risk indicators for periodontal diseases. J Periodontol 2000(29):177–206
40.
go back to reference Hugoson A, Rolandsson MJ (2011) Periodontal disease in relation to smoking and the use of Swedish snus: epidemiological studies covering 20 years (1983–2003). Clin Periodontol 38:809–816CrossRef Hugoson A, Rolandsson MJ (2011) Periodontal disease in relation to smoking and the use of Swedish snus: epidemiological studies covering 20 years (1983–2003). Clin Periodontol 38:809–816CrossRef
41.
go back to reference Vestergaard P, Mosekilde L (2003) Fracture risk associated with smoking: a meta-analysis. J Intern Med 254:572–583PubMedCrossRef Vestergaard P, Mosekilde L (2003) Fracture risk associated with smoking: a meta-analysis. J Intern Med 254:572–583PubMedCrossRef
42.
go back to reference Buttros Dde A, Nahas-Neto J, Nahas EA, Cangussu LM, Barral AB, Kawakami MS (2011) Risk factors for osteoporosis in postmenopausal women from southeast Brazilian. Rev Bras Ginecol Obstet 33:295–302 (In Portuguese)PubMedCrossRef Buttros Dde A, Nahas-Neto J, Nahas EA, Cangussu LM, Barral AB, Kawakami MS (2011) Risk factors for osteoporosis in postmenopausal women from southeast Brazilian. Rev Bras Ginecol Obstet 33:295–302 (In Portuguese)PubMedCrossRef
43.
go back to reference Brennan RM, Genco RJ, Hovey KM, Trevisan M, Wactawski-Wende J (2007) Clinical attachment loss, systemic bone density, and subgingival calculus in postmenopausal women. J Periodontol 78:2104–2111PubMedCrossRef Brennan RM, Genco RJ, Hovey KM, Trevisan M, Wactawski-Wende J (2007) Clinical attachment loss, systemic bone density, and subgingival calculus in postmenopausal women. J Periodontol 78:2104–2111PubMedCrossRef
44.
go back to reference Hujoel PP, Cunha-Cruz J, Selipsky H, Saver BG (2005) Abnormal pocket depth and gingival recession as distinct phenotypes. Periodontol 39:22–29CrossRef Hujoel PP, Cunha-Cruz J, Selipsky H, Saver BG (2005) Abnormal pocket depth and gingival recession as distinct phenotypes. Periodontol 39:22–29CrossRef
45.
go back to reference Krall EA, Wehler C, Garcia RI, Harris SS, Dawson Hughes B (2001) Calcium and vitamin D supplements reduce tooth loss in the elderly. Am J Med 111:452–456PubMedCrossRef Krall EA, Wehler C, Garcia RI, Harris SS, Dawson Hughes B (2001) Calcium and vitamin D supplements reduce tooth loss in the elderly. Am J Med 111:452–456PubMedCrossRef
Metadata
Title
Osteoporosis/osteopenia as an independent factor associated with periodontitis in postmenopausal women: a case–control study
Authors
J. S. Passos
M. I. P. Vianna
I. S. Gomes-Filho
S. S. Cruz
M. L. Barreto
L. Adan
C. K. Rösing
E. M. M. Cerqueira
S. C. Trindade
J. M. F. Coelho
Publication date
01-04-2013
Publisher
Springer-Verlag
Published in
Osteoporosis International / Issue 4/2013
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-012-2130-7

Other articles of this Issue 4/2013

Osteoporosis International 4/2013 Go to the issue