Ankylosing spondylitis (AS) is a chronic rheumatic

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1 SPINE Volume 41, Number 17, pp ß 2016 Wolters Kluwer Health, Inc. All rights reserved DEFORMITY Changes in Sexual Activity in Male Patients Surgically Treated for Kyphosis due to Ankylosing Spondylitis Ziming Yao, PhD, y Jianwei Du, PhD, Zheng Wang, PhD, y Guoquan Zheng, PhD, y Xuesong Zhang, PhD, y Geng Cui, PhD, y and Yan Wang, PhD y Study Design. A retrospective study. Objective. The aim of this study was to assess the changes in sexual activities in male patients surgically treated for ankylosing spondylitis (AS)-induced kyphosis and the correlation between these changes and spinal sagittal realignment. Summary of Background Data. Sexual function may be affected by AS. However, little is known about the effect of spinal surgery on the sexual activity of patients with AS-induced kyphosis. Methods. Data of 45 male patients who had been surgically treated for AS-induced kyphosis were retrospectively reviewed. Changes in sexual activity were evaluated by the international index of erectile function (IIEF), frequency of sexual activity, and time point at which sexual activity began postoperatively. We compared the above-mentioned parameters before and 24 months postoperatively and analyzed the correlation of the changes in the IIEF with the changes in radiological characteristics. Results. Each domain of the IIEF and the total IIEF were increased postoperatively. Improved sexual function was correlated with changes in spinal sagittal characteristics, among which lumbar lordosis (LL) and the chin-brow vertical angle (CBVA) were the most significant causes (P < 0.05). Most patients (71.1%) resumed their sexual activity 5 to 12 weeks after surgery. At the 24-month follow-up, the frequency of From the Yangzhou NO.1 People s Hospital, Yangzhou, China; and y Department of Orthopaedics, Chinese People s Liberation Army General Hospital (301 Hospital), Beijing, China. Acknowledgment date: September 1, First revision date: January 9, Acceptance date: February 1, Jianwei Du is the co-first author. The manuscript submitted does not contain information about medical device(s)/drug(s). No funds were received in support of this work. No relevant financial activities outside the submitted work. Address correspondence and reprint requests to Zheng Wang, PhD, Department of Orthopaedics, Chinese PLA, General Hospital (301 Hospital), 28 Fuxing Road, Beijing, China. wangzheng301@hotmail.com patients sexual activity was higher than that before surgery (P < 0.05). Conclusion. Surgical correction of spinal deformity may improve sexual function and increase the frequency of sexual activity in men with AS. Spinal sagittal realignment and pelvic rotation may be correlated with improvement of sexual function. Key words: ankylosing spondylitis, kyphosis, sexual function, surgery. Level of Evidence: 4 Spine 2016;41: Ankylosing spondylitis (AS) is a chronic rheumatic disorder that primarily affects the axial skeleton. 1 Throughout the course of the disease, joint stiffness, fatigue, and spinal kyphosis may increase in severity, and spinal mobility becomes increasingly limited. 1,2 Sexual activity is an important part of healthy life in adults. Many recent studies have proven that sexual function is impaired in male patients with AS because of back pain, decreased mobility of the axial skeleton, and high disease activity. 3 9 Both the prevalence and severity of sexual dysfunction in patients with AS are much higher than those observed in healthy individuals. 3,4 However, there is a paucity of information regarding sexual activity before and after surgical treatment of AS-induced kyphosis. Patients and surgeons often hesitate to talk about the effects of disease and surgery on sexuality, but it is imperative that sexuality issues be addressed. Therefore, in the present study, we assessed the effect of spinal surgery on the quality and frequency of sexual activity and the favorite coital position of male patients with AS. MATERIALS AND METHODS We collected and reviewed the data of 98 consecutive patients with AS who underwent primary one-stage spinal osteotomy surgery at our hospital from September 2010 to September All patients met the most recently modified New York criteria and were unable to lie down flat in bed with their heads touching the pillow because of severe kyphotic DOI: /BRS September 2016

2 TABLE 1. Inclusion and Exclusion Criteria Inclusion Criteria Diagnosed with AS according to the modified New York criteria Kyphosis in thoracolumbar and/or lumbar years old Signed informed consent Accepted treatment options Be married and could achieve sexual life before surgery Exclusion Criteria Female patients Had neurological symptoms before surgery Undertook hip joint surgery during follow-up or range of hip motion changed more than 108 Kyphosis in cervical or cervicothoracic spine Neurological complications occurred Reoperation Took anti-rheumatic drugs or tumor necrosis factor, or nonsteroidal anti-inflammatory drugs more than 3 months Inability to understand information because of abuse, psychological, or medical reasons. Patients with pulmonary, hepatic, hematologic, or renal diseases; endocrine disorders such as diabetes mellitus; thyroid function disorder or systemic disorders such as hormonal, neurogenic, and cardiovascular diseases that may affect the sexual function deformities. 10 According to our inclusion and exclusion criteria (Table 1), the data of 45 patients were included in this study and investigated in detail. The study protocol was fully approved by our institutional ethics board. Surgical Treatment Experienced spine surgeons in our hospital decided on the surgical plan and conducted all of the surgical operation. 11 A single-level pedicle subtraction osteotomy (PSO), a single-level PSO with a couple of Smith Petersen osteotomies, or a twolevel PSO was performed using a posterior approach according to the kyphosis severity. After surgery, the patients were asked to wear a removable brace for 6 months in daytime. Clinical and Imaging Characteristics The following demographic and clinical characteristics of the patients were collected and analyzed: sex, marital status, disease course (defined as the duration since onset of the first symptoms of AS), drug use, visual analog scale (VAS) score for back pain, and range of hip motion. The following parameters were measured on a plain lateral X-ray of the full spine preoperatively and 24 months postoperatively: global kyphosis (GK, the angle between the superior endplate of the maximally tilted upper end vertebra and the inferior endplate of the maximally tilted lower end vertebra), lumbar lordosis (LL), thoracic kyphosis (TK), pelvic incidence (PI), pelvic tilt (PT), sagittal vertical axis (SVA), and sacral slope (SS). The chin-brow vertical angle (CBVA), defined as the angle measured between a line from the brow to the chin to the vertical while the patient stood with hips and knees extended, 12 was measured on clinical photographs of the patients. position was chosen from pictures showing four common positions: the missionary position (man on top of woman, face to face), Amazon position (woman on top of man, face to face), spoons position (man behind woman with both lying on their sides), and dog position (woman in the quadruped position with man kneeling behind her). The questionnaires also assessed the international index of erectile function (IIEF), which comprises five domains: erection function (EF), orgasm function (OF), sexual desire (SD), intercourse satisfaction (IS), and overall satisfaction (OS). 13 Statistical Analysis Statistical calculations were performed using the Statistical Package for Social Sciences software version 17.0 for Windows (SPSS Inc, Chicago, IL). Continuous variables are presented as mean and standard deviation if normally distributed and as median and range if nonnormally distributed. Comparisons of the pre- and postoperative IIEF, VAS score, CBVA, and spinal sagittal parameters were performed with the Student t test. The rate of increase in the IIEF was calculated as follows: [(postoperative IIEF preoperative IIEF)/preoperative IIEF)] 100%. Spearman correlation analysis was used to test the association between changes in the IIEF with changes in the imaging parameters, and a multivariate linear regression analysis was performed to analyze the relationship between them. A stepwise method was used to construct multivariate regression models in relation to various dependent variables. The distribution of the frequency of sexual activity and the favorite pre- and postoperative sexual positions were compared using the Chi-square test. The level of statistical significance was set at P < Characteristics of Sexual Activity Before and 24 months after surgery, the patients completed questionnaires concerning the frequency of sexual activity, the time point at which they resumed their sexual activity after surgery, and their adjustment of coital position. Coital RESULTS Patient Demographics We initially assessed six (6.1%) women and 92 (93.9%) men. Only 60 of the 92 men had a sexual partner, and 10 Spine

3 TABLE 2. Outcomes of Clinical and Photographic Characteristics (n ¼ 45) Characteristics Preoperative 24-month Postoperative VAS CBVA (8) <0.001 TK (8) PI (8) PT (8) <0.001 SS (8) <0.001 SVA (cm) <0.001 LL (8) <0.001 GK (8) <0.001 CBVA indicates chin-brow vertical angle; GK, global kyphosis; LL, lumbar lordosis; PI, pelvic incidence; PT, pelvic tilt; SS, sacral slope; SVA, sagittal vertical axis; TK, thoracic Kyphosis; VAS, visual analog scale of back pain. patients did not participate in the survey regarding sexual activity. Finally, 45 patients (all male) were included in the study. The mean age of these 45 patients was years (range, yrs), and the median disease duration was 15 years (range, 5 30 yrs). Of all 45 patients, 21 (46.7%) underwent single-level PSO, 15 (33.3%) underwent two-level PSO, and nine (20.0%) underwent singlelevel PSO with Smith Petersen osteotomies. All patients back pain was slight (few patients complained of back pain during sexual activity), and there were no significant differences in the pre- and postoperative VAS scores among the patients (P > 0.05) (Table 2). None of the patients developed instrument failure during the 24-month follow-up. During follow-up, all of these 45 patients did not take antirheumatic drugs, tumor necrosis factor, or nonsteroidal anti-inflammatory drugs. Imaging Results The CBVA and radiographic results are listed in Table 2. Before surgery, the average CBVA, PT, SS, SVA, LL, and GK were , , , cm, , and , respectively. After surgery, the average CBVA, PT, SS, SVA, LL, and GK were , , , cm, , and , respectively. Significant differences were observed in each of these parameters P (P < 0.05), while no significant differences were observed in PI and TK before and after surgery (P > 0.05). Outcomes of Sexual Function Of the 45 patients, 40 (88.9%) reported an improvement in OS. Table 3 summarizes the IIEF before and after surgery. Each domain of the IIEF and the total IIEF were significantly higher after than before surgery (P < 0.05). The rate of increase varied from 8.33% to 14.75%, and the total score was increased by 9.86%. According to Spearman correlation analysis, there was a significant positive correlation between the change in the IIEF and the improvement in SVA, LL, and CBVA (P < 0.05). Moreover, the change in SS was positively correlated with the improvements of IS, OS, and TS of the IIEF and the change in PT was positively correlated with the improvements of OS, and TS of the IIEF (Table 4). The stepwise regression analysis results indicated that changes in LL and CBVA were independently associated with improvements in EF and the total IIEF, changes in OF and SD were independently associated with an improvement in the CBVA, and changes in IS and OS were independently associated with an improvement in LL (P < 0.05) (Table 5). Sexual activity was resumed within 5 to 8 postoperative weeks in 48.9% of patients and within 9 to 12 weeks in 22.2% (Figure 1). The frequency distribution of sexual activity before and 24 months after surgery is shown in Figure 2, and the Chi-square test result showed that patients had more frequent sexual activity 24 months after than before surgery (P < 0.05). Considering the limitations due to disease and the sexual positions chosen by the patients, the four positions depicted in the picture were assessed. Figure 3 shows that before surgery, the Amazon position (woman on top of man, face to face) was the most frequent (37.8%) and comfortable position. At the 24-month follow-up, the spoons position (man behind woman with both lying on their sides) was the most frequent (37.8%) and comfortable position. And the distributions of the favorite pre- and postoperative sexual positions were not significantly different (P > 0.05). DISCUSSION According to the result of this research, AS patients EF, OF, SD, IS, and OS are improved by spinal kyphosis surgery, and TABLE 3. Results of Sexual Function Before and 24 mnths After Surgery (n ¼ 45) IIEF Domains (range) Preoperative 24 mnths Follow-up Increase Rate (%) P EF (0 30) OF (0 10) SD (2 10) IS (0 15) OS (2 10) TS (4 75) <0.001 EF indicates erectile function; IIEF, International index of erectile function; IS, intercourse satisfaction; OF, orgasmic function; OS, overall satisfaction; SD, sexual desire; TS, total score of IIEF September 2016

4 TABLE 4. Correlation Between the Changes of IIEF Scores With the Changes of Imaging Characteristics Characteristics D EF (r) D OF (r) D SD (r) D IS (r) D OS (r) D TS (r) D GK D SS y y D PT y D SVA y y y y D LL y y y y y y D TK D CBVA y y y y CBVA indicates chin-brow vertical angle; EF, erectile function; GK, global kyphosis; IS, intercourse satisfaction; LL, lumbar lordosis; OF, orgasmic function; OS, overall satisfaction; PT, pelvic tilt; SD, sexual desire; SS, sacral slope; SVA, sagittal vertical axis; TK, thoracic kyphosis; TS, total score of IIEF. P y P D Means this value s change (e.g., D EF ¼ 24-month postoperative EF preoperative EF). TABLE 5. Stepwise Regression Analyses in Surgical Patients With AS Dependent Variables D EF D OF D SD D IS D OS D TS Variables Entered Coef. SE t P R Sig. D LL <0.001 D CBVA D CBVA D CBVA D LL < <0.001 D LL < <0.001 D LL < <0.001 D CBVA <0.001 Changes of IIEF domains as dependent variables, changes of radiological characteristics as independent variables. CBVA indicates chin-brow vertical angle; EF, erectile function; IS, intercourse satisfaction; LL, lumbar lordosis; OF, orgasmic function; OS, overall satisfaction; SD, sexual desire; TK, thoracic kyphosis; TS, total score of IIEF. D This value s change (e.g., D EF ¼ 24-month postoperative EF preoperative EF). these improvements are related to the spinal sagittal realignments and pelvic rotation. As is well known, sexuality is a substantial component of an adult s quality of life, and a healthy locomotor system and mood are necessary for normal sexual function. 14 Some researches recently reported an increased prevalence of sexual dysfunction among patients with AS. 7,15 A systematic review and meta-analysis including 11 studies reported that each domain of the IIEF was lower in men with AS than in controls. 6 Rostom et al. 16 claimed that fatigue and sleep disturbance resulted in perceived problems with sexual activity. Gallinaro et al. 5 found that the chronic nature of AS, with its associated poor functional capacity and high disease activity, interferes with sexual intercourse. According to Tristano, 17 pain and depression could be the main contributing factors in patients with sexual dysfunction. The sexual function of AS patients [%] [%] Preoperatively 24 months follow-up weeks 5-8 weeks 9-12 weeks >12 weeks Figure 1. The time point that patients resume the sexual activity after surgery >12 times month Figure 2. The frequency of sexual activity preoperatively and at 24 months follow-up. Spine

5 [%] Missionary Amazone Spoons Dog Preoperatively 24 months follow-up Figure 3. The most frequent and comfortable sexual positions in AS patients preoperatively and at 24 months follow-up. could also be affected by anti-rheumatic drugs, tumor necrosis factor, and nonsteroidal anti-inflammatory drugs as reported in literatures Thus, we excluded the patients who took these drugs more than 3 months in this study. In terms of the effect of spinal surgery on sex-related quality of life, some studies have evaluated patients with scoliosis or lumbar disc herniation. 21,22 Hagg et al. 23 found that among patients with chronic low back pain, those who underwent surgical treatment had a significantly better sexual life than did those who underwent nonsurgical treatment. However, these studies ignored the influence of spinal kyphosis on sexual function in the late stage of AS and the changes in sexual function in patients with AS after spinal surgery. The major finding of our study is that surgical treatment for AS-induced kyphosis improves the sexual activity in EF, OF, SD, IS, and OF as well as the total IIEF. And these improvements might be associated with spinal realignment, especially the increase in LL and the change in the CBVA; an association between them was identified by stepwise regression analyses. The late stage of AS is characterized by specific spinal deformities such as lumbar hypolordosis, thoracic hyperkyphosis, and thoracolumbar kyphosis 1 ; however, patients back pain is usually not as serious as that in the early stage, which is characterized by lower disease activity. According to the result, few patients complained of back pain during sexual activity and there was no significant difference in the pre- and postoperative VAS scores. Thus, we excluded the effect of back pain on sexual life and hypothesized that immovability of the spine, severe kyphotic deformity, and the resulting depression might be the main causes of worse functional capacity. Although surgery did not influence spinal motion, it contributed to the restoration of spinal sagittal alignment and pelvic rotation, which are still significantly associated with the improvement in sexual function. Therefore, we considered that maintenance of spinal sagittal parameters and pelvic rotation at near-normal levels could help to maintain or achieve satisfactory sexual function, while these parameters may also alter the general well-being of the patient, resulting in increased sexual satisfaction and performance. Improvement of IS and orgasmic function may be explained by the optimized alignment of spine and pelvic rotation, which makes the penis more prominent relative to the body. But it is difficult to explain the improvement of erectile function and SD. We conjectured that one of the reasons might be the mental health caused by the better physical appearance. Thus, we have to mention that one of the weak sides of our study is lack of mental assessment. Sidorkewicz et al. 24 reported that different coital positions require different spinal motion ranges. However, in patients with AS who have a fully inflexible spine, spinal surgery can still positively influence their ability to engage in their favorite coital position to some extent. Notably, coital positions are greatly affected by hip motion 25 ; thus, the coital positions of patients with AS might vary with hip stiffness. We took this into account in the present study in that we limited the cases to patients with a range of hip motion that changed by no more than 108. Although the difference in favorite coital positions was not significant, the Amazon and spoons positions were the most frequent and comfortable positions before and 24 months after surgery, respectively. Many patients are concerned about the time point at which they will be able to resume sexual activity after surgery. Kanayama et al. 22 found that in patients who underwent surgical treatment for lumbar disc herniation, sexual activity was resumed within 2 weeks postoperatively in 23% of patients (27% in men and 14% in women) and within 4 weeks in 53%. However, no researcher has reported the time point at which sexual activity begins after surgical treatment of AS. The current study demonstrated that most patients who underwent surgical treatment of AS resumed their sexual activity with their spouse within 5 to 12 postoperative weeks, and no complications occurred because of sexual activity. On the basis of our observations, we believe that resumption of sexual activity 5 to 12 weeks after an operation for AS is more likely safe and might be permitted. Although Ozkorumak et al. 15 reported that there was no difference in the frequency of sexual intercourse between patients with AS and a healthy group, the results of our study show that surgery increases the frequency of sexual activity in patients with AS. Although this study is an original report about the effect of kyphosis correction surgery on sexual activity, it has severallimitations.first,itwas a retrospective case series without a control group, which prevented us from evaluating the change in sexual activity of patients who did not receive surgical treatment. Second, it did not take psychological factors into account, making it difficult to distinguish whether spinal realignment improved the sexual activity directly or via an improvement in psychological well-being. Third, the small sample size hampered us to study the impact of age and sagittal correction on resuming sexual activity. In conclusion, surgical correction of spinal deformity may improve sexual function, increase the frequency of sexual activity, and influence the favorite coital position in male patients with AS. Changes in the CBVA and LL are the most significant factors correlated with improvements in sexual function. Resumption of sexual activity after 5 to 12 weeks postoperatively might be permitted September 2016

6 Key Points Surgical correction of kyphosis may improve sexual function in male patients with ankylosing spondylitis. Surgical correction of kyphosis may increase the frequency of sexual activity and influence the favorite coital position. Resumption of sexual activity 5 to 12 weeks postoperatively might cause no complications. References 1. Braun J, Sieper J. Ankylosing spondylitis. Lancet 2007;369: Chang KW, Chen YY, Lin CC, et al. Closing wedge osteotomy versus opening wedge osteotomy in ankylosing spondylitis with thoracolumbar kyphotic deformity. Spine 2005;30: Shen B, Zhang A, Liu J, et al. A primary analysis of sexual problems in Chinese patients with ankylosing spondylitis. Rheumatol Int 2013;33: Sariyildiz MA, Batmaz I, Dilek B, et al. Relationship of the sexual functions with the clinical parameters, radiological scores and the quality of life in male patients with ankylosing spondylitis. Rheumatol Int 2013;33: Gallinaro AL, Akagawa LL, Otuzi MH, et al. Sexual activity in ankylosing spondylitis. Rev Bras Reumatol 2012;52: Fan D, Liu L, Ding N, et al. Male sexual dysfunction and ankylosing spondylitis: a systematic review and metaanalysis. J Rheumatol 2015;42: Cakar E, Dincer U, Kiralp MZ, et al. Sexual problems in male ankylosing spondylitis patients: relationship with functionality, disease activity, quality of life, and emotional status. Clin Rheumatol 2007;26: Ostensen M. New insights into sexual functioning and fertility in rheumatic diseases. Best Pract Res Clin Rheumatol 2004;18: Panush RS, Mihailescu GD, Gornisiewicz MT, et al. Sex and arthritis. Bull Rheum Dis 2000;49: van der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 1984;27: Zheng GQ, Song K, Zhang YG, et al. Two-level spinal osteotomy for severe thoracolumbar kyphosis in ankylosing spondylitis. Experience with 48 patients. Spine 2014;39: Suk KS, Kim KT, Lee SH, Kim JM. Significance of chin-brow vertical angle in correction of kyphotic deformity of ankylosing spondylitis patients. Spine 2003;28: Rosen RC, Riley A, Wagner G, et al. The international index of erectile function (IIEF): a multidimensional scale for assessment of erectile dysfunction. Urology 1997;49: Tristano AG. Impact of rheumatoid arthritis on sexual function. World J Orthop 2014;5: Ozkorumak E, Karkucak M, Civil F, et al. Sexual function in male patients with ankylosing spondylitis. Int J Impot Res 2011;23: Rostom S, Mengat M, Mawani N, et al. Sexual activity in Moroccan men with ankylosing spondylitis. Rheumatol Int 2013;33: Tristano AG. The impact of rheumatic diseases on sexual function. Rheumatol Int 2009;29: Gleason JM, Slezak JM, Jung H, et al. Regular nonsteroidal antiinflammatory drug use and erectile dysfunction. J Urol 2011;185: Dong X, Zheng Y, Shi TY, Liu HY. Effects of tumor necrosis factor-alpha on sexual activity of male patients with ankylosing spondylitis. Clin Rheumatol 2015;34: Aguirre MA, Velez A, Romero M, Collantes E. Gynecomastia and sexual impotence associated with methotrexate treatment. J Rheumatol 2002;29: Danielsson AJ, Nachemson AL. Childbearing, curve progression, and sexual function in women 22 years after treatment for adolescent idiopathic scoliosis: a case-control study. Spine 2001;26: Kanayama M, Horio M, Umi Y, et al. How does surgery affect sexual desire and activities in patients with lumbar disc herniation? Spine 2010;35: Hagg O, Fritzell P, Nordwall A, Swedish Lumbar Spine Study G. Sexual function in men and women after anterior surgery for chronic low back pain. Eur Spine J 2006;15: Sidorkewicz N, McGill SM. Male spine motion during coitus: implications for the low back pain patient. Spine 2014;39: Charbonnier C, Chague S, Ponzoni M, et al. Sexual activity after total hip arthroplasty: a motion capture study. J Arthroplasty 2014;29: Spine