Introduction

In 1987, Chamot, a French rheumatologist, described a special disease process characterized by skin lesions and joint damage co-existing in the affected individuals, and named it SAPHO syndrome with the initials of the words of synovitis, acne, pustulosis, hypertrophy and osteitis [1]. SAPHO and the disease spectrum it represents are considered rare. Due to the lag of its diagnosis and the uncertainty of clinical disease manifestations, its exact prevalence is still elusive [2]. According to published studies, there are reports of SAPHO diseases worldwide. The annual prevalence rate of European whites is less than 1/10,000, while the annual prevalence rate of Japanese is less than 0.00144/100,000. However, due to insufficient knowledge of the disease in China, there is no report on the exact incidence of SAPHO [3]. As of 2020, 1,000 SAPHO cases have been reported worldwide [4, 5]. The pathogenesis of SAPHO syndrome is unclear, and may be related to immune dysfunction [6], infection [7] and genetic susceptibility [8].There is no consensus on SAPHO’s treatment plan. The current main strategy is to ameliorate clinical symptoms and improve the quality of life of patients in the long time. The main therapeutic drugs include: non-steroidal anti-inflammatory drugs (NSAIDs), Disease-modifying antirheumatic drugs (DMARDs), Corticosteroids, Bisphosphonates and so on. TNF-α antagonists are also increasingly used in the treatment of SAPHO, and have achieved good clinical effects. Historically, SAPHO mainly affects young and middle-aged people [2], and the disease recurs [9]. So it may impair the quality of sexual life of patients.

Sexual dysfunction (SD) is characterized by desire, arousal, orgasm and pain, and its pathogenesis is more complicated, including a variety of physical and psychological factors. Historically, sexual dysfunction is attributed to the psychological field [10]. Sexual dysfunction is one of the common symptoms of Behçet’s disease (BD) [11]. But the data on SD occurrence in this particular group of patients is limited. As far as we know, the assessment of SAPHO patients’ anxiety, work status and quality of life has been the subject of numerous studies, no assessment of sexual dysfunction in patients with SAPHO syndrome has been carried out. This study is the first to assess sexual function of SAPHO syndrome patients and its purpose was to determine the prevalence of SD and to analyze the potential risk factors for SD.

Methods

Patient enrolment and study design

This study was approved by the ethics committee of PUMCH (Identifier: ZS-944) (Beijing, China). This study was conducted using a single-centre, cross-sectional design. The inclusion criteria included a diagnosis of SAPHO syndrome according to the diagnosis criteria proposed by Kahn [12] in 2003, and symptoms like bone pain persisting in the most recent one month. 18–60 years old, those who have had sex in the past 4 weeks. After obtaining the informed consent of PUMCH participants, they were asked to complete a questionnaire about the quality of sexual life. This study was funded by the National Key Research and Development Program of China (2016YFC0901500) and CAMS Innovation Fund for Medical Sciences (CIFMS) [2017-I2M-3-001].

The questionnaire completed by the patient includes demographic, quality of life, quality of sexual life data and mental state. Demographic and clinical data include gender, age, SAPHO duration, BMI, smoking, drinking, marital status, educational level, occupational status and work status. The disease related quality of life was measured with the help of the Short Form-36 quality of life questionnaire (SF-36 QoL). The SF-36 QoL questionnaire mainly involves the following areas: Physical-Functioning, role-limit-physical, role-limit-emotional, energy-fatigue, emotional-well-being, social-functioning, pain and general-health. The SF-36 QoL scale was in the supplementary material. The main variable “sexual dysfunction” in this study was evaluated differently in men and women. The Female Sexual Function Index (FSFI) has been validated as a reliable questionnaire to assess female sexual function in general Chinese population [13]. The FSFI scale involves six female sexual areas: Desire, Arousal, Lubrication, Orgasm, Satisfaction and Pain. It mainly contains 19 questions to investigate sexual problems in the past 4 weeks. The first two questions are scored 1–5, and the remaining questions are scored 0–5. A total score of less than 23 is defined as the critical value for distinguishing FSD. (FSD was defined as “lack or reduced sexual interest or excitement”). The FSFI scale was in the supplementary material. The International Index of Erectile Function (IIEF) is often used to assess the quality of sexual life of male patients [14]. Male SD is represented by erectile dysfunction (ED). The IIEF scale involves five sexual domains of men: Erectile function, Orgasmic function, Sexual desire, Intercourse satisfaction and Overall satisfaction. This is an erectile dysfunction questionnaire containing 15 questions. The first 9 questions are scored 0–5, and the rest are scored 1–5. Scores below 25 are considered ED. (The European Urological Association defined erectile dysfunction as “continuous failure to achieve and maintain sufficient erectile ability to obtain satisfactory sexual behavior.) The IIEF scale was in the supplementary material. At the same time, the self-esteem and relationship questionnaire (SEAR) questionnaire was used to assess the mental state of participants. The SEAR questionnaire is a questionnaire containing 14 questions. It explains the psychological state of participants in two major aspects: Sexual relationship (Q1-Q8) and Confidence (Q9-Q14). Among them, Confidence (Q9-Q14) includes two small aspects: Self-esteem (Q9- Q12) and Overall relationship (Q13-Q14). The SEAR scale was in the supplementary material.

Statistical analysis

The data are expressed as the mean, standard deviation, number and percentage of categorical variables of continuous variables. Continuous variables used t test or Mann-Whitney Utest, categorical variables used chi-square test or Fisher’s exact test. Statistical analysis was performed with SPSS (version 25.0), and a two-sided P value of less than 0.05 was considered statistically significant.

Results

Epidemiological characteristics of the participants in this study

249 patients completed all of the questionnaires and constituted the study population. Of the 249 patients in this cross-sectional study, 80 were males and 169 were females. The age of the patients is between 18 and 59 years old, and most of them are between 30 and 59 years old. Regarding BMI, the BMI of most patients was between 18.5 and 28. Only a small percentage of patients have the habit of smoking and drinking. Among all the participants, the vast majority were already married. The education level of the patients was evenly distributed from low to high. In the work status survey, “Employed” and “Retired / housewives” each account for half. As for the most important part-SAPHO duration: 52.6% of patients with SAPHO disease progression less than 5 years; 33.7% of patients with 5–10 years; and 13.7% of patients with more than 10 years. Demographic data from these couples was presented in Table 1.

Table 1 Epidemiological data of participants in this study (n = 249)
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Results of sexual function assessment using FSFI (for female) and IIEF (for male)

Among all the participants in this cross-sectional study, whether they suffered from SD was described in Table 2. The FSFI scale showed that among 169 female patients, 124 patients had FSD (73.4%); while 45 patients had no FSD (26.6%). The IIEF scale showed that among 80 male patients, 45 patients suffered from ED (56.3%); while 35 patients did not have ED (43.7%). In addition, in the FSFI scale, the scores of FSD and nFSD patients in the scale were significantly different (p < 0.01). The IIEF scale also described similar results (p < 0.01).

Table 2 Results of sexual function assessment using FSFI (for female) and IIEF (for male)
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Comparison of clinical characteristics between participants with and without sexual dysfunction

SF-36 QoL and SEAR were used to analyze the clinical status of all participants with or without SD. The specific data analysis was illustrated in Tables 3 and 4. Among the female participants in this study, there were no significant differences in BMI, age, smoking, drinking, marital status, educational level, occupational status and work status among female participants with or without SD. In the SF-36 QoL scale analysis, female participants with or without SD showed no significant differences in physical-functioning, role-limit-physical, role-limit-emotional, social-functioning pain and general-health; but participants with SD showed lower scores in energy-fatigue (p = 0.01) and emotional-well-being (p = 0.02). In the SEAR scale survey, compared with normal participants, participants with SD showed lower scores in the areas of Sexual relationship, Self-esteem, Confidence and Overall relationship (p < 0.001). Among all male participants, we found that there were no significant differences in demographic, quality of life (SF-36 QoL) and mental state (SEAR) among participants with or without SD. In addition, there was no significant difference in SAPHO duration between female and male participants, with or without SD.

Table 3 Comparison of clinical characteristics between females with and without sexual dysfunction
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Table 4 Comparison of clinical characteristics between males with and without sexual dysfunction
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Potential risk factors for participants sexual dysfunction using logistic regression

Finally, we conducted a logistic regression analysis of potential risk factors for SD in all participants. Potential risk factors mainly include somking, drinking, mental work dominant quality of life indicators, Sexual relationship, Confidence, Self-esteem, age and BMI. In addition, we also analyze the relationship between SAPHO duration and SD. The specific data analysis was illustrated in Tables 5 and 6. The final results showed that whether it is male or female SD patients, the logistic regression data show that the above factors are not potential risk factors for sexual dysfunction. Similarly, SAPHO duration is not a potential risk factor for sexual dysfunction.

Table 5 Potential risk factors for female sexual dysfunction using logistic regression
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Table 6 Potential risk factors for male erectile dysfunction using logistic regression
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Discussion

This study included 249 SAPHO syndrome patients, who were distributed across the country. Through the SF-36 QoL, FSFI, IIEF, and SEAR scales, we recorded the demographic, quality of life, quality of sexual life data and mental state of all participants (including 80 men and 169 women). Finally, we perform statistical analysis on all the data. In this article, we explored the connection between SAPHO and sexual dysfunction, and analyzed the potential risk factors that cause sexual dysfunction.

The incidence of sexual dysfunction is increasing year by year globally. SD affects the physical health of patients and reduces their quality of life. The cause of SD is unclear, but it may be multifactorial, involving biological, psychosocial, and disease-specific factors. SD is associated with many diseases, including IBD [15], chronic sinusitis [16], primary Sjögren’s syndrome (pSS) [17], rheumatoid arthritis (RA) [18], liver cirrhosis [19], diabetes [20], Behçet’s disease [11, 21] and so on. SAPHO syndrome is a chronic systemic inflammatory disease with external manifestations of skin involvement and internal manifestations of bone and joint involvement. The clinical presentation of the disease in SAPHO syndrome approximates that of seronegative arthritis. Since rheumatoid factor is negative in the early stages of rheumatoid arthritis, it can be called seronegative arthritis. Numerous studies have reported the relationship between rheumatoid arthritis and sexual dysfunction. Wojciech Tański et al. found that sexual dysfunction in patients with rheumatoid arthritis is closely related to their disease activity [22]. Patients with high disease activity had a higher proportion of sexual dysfunction. Interestingly, we found that SAPHO, as a disease similar to seronegative arthritis (early stage rheumatoid arthritis, low disease activity), also causes sexual dysfunction in patients. In this study, we found that out of 169 female patients, 124 patients (73.4%) had SD; among 80 male patients, 45 patients suffered from ED (56.3%); while 35 patients did not have ED (43.7%). Female patients suffer from SD more frequently than men. We then assessed the quality of life and mental state of all participants. We found that female SD patients had significantly lower scores in energy-fatigue, emotional-well-being, Sexual relationship, Self-esteem, Confidence and Overall relationship; among all male participants, we found that with or without SD There were no significant differences in the quality of life and mental state of the participants. This suggests that female SD patients are abnormal in their psychological state. It is worth noting that, with or without SD, there was no significant difference in the duration of SAPHO between female and male participants. Therefore, SAPHO duration will not have a significant impact on the patient’s SD.

The strength of this study is that this is the first report on the relationship between SAPHO syndrome and sexual dysfunction. At the same time, it included a relatively large sample size of 249 patients. Also, including 80 males is an advantage. However, the proportion of male participants was relatively low, and more male participants would make the conclusions more reliable. Study limitations include a significant risk of selection bias. Patients were consecutively recruited upon presentation to the outpatient department. Therefore, patients with low or very high disease activity may have been missed due to absence. Likewise, underresourced and noncompliant patients may also be spilled. However, this study did not classify the patients according to the site of disease involvement, which made it impossible for us to analyze the relationship between the site of disease involvement and sexual dysfunction in SAPHO patients. Sensitive questions about private and intimate matters involved in the questionnaire may make the experimental data of the survey research low quality. The cross-sectional study design did not allow for a dynamic lifetime approach [23]. In addition, since healthy participants were not included in this study, direct comparisons of sexual dysfunction data between healthy participants and patients with SAPHO syndrome could not be made. Therefore, a causal relationship between the various risk factors of SAPHO syndrome and sexual dysfunction cannot be drawn.

In conclusion, we found that the incidence of female SD in SAPHO patients is higher, and the main influence on female SD is psychological factors. This suggests that we are also very important to regulate the mental state of patients when treating SAPHO clinically. These promising findings prove that it is necessary to further design randomized controlled trials to further explore the relationship between SAPHO and SD.