1 Introduction
ED is the persistent or repeated inability to achieve or maintain sufficient penile erection to sustain a satisfying sexual life.[1] [2] [3–11] [12–16] [17–20]
The ischiocavernosus muscle (ICM) is a pair of short pinnate muscles attached to the pelvic ring. The ICM arises from the ischial tuberosity and attaches to the pubic ramus, and some muscle fibers enclose the root of the penis.[21–23] [23] [21] [21] [21] [21]
We found that ED patients with pelvic fractures had imaging manifestations of ICMI by reviewing their computed tomography (CT)/magnetic resonance imaging (MRI) scans. In this study, we analyzed the correlation and deduced the internal relationship between ICMI and different types of pelvic fractures and ED after pelvic fractures in male patients. This study will provide new ideas for the clinical diagnosis and treatment of ICMI and ED after pelvic fracture.
2 Materials and methods
2.1 Patients
This study was a retrospective case control study. A consecutive series of data covering 776 male patients with pelvic fractures during the period of January 2010 to December 2018 were collected from the Affiliated Hospital of Zunyi Medical University in China. The inclusion criteria were as follows: male; traumatic pelvic fracture; age range of 18 to 70 years; normal secondary sexual characteristics; normal erectile function before pelvic fracture; complete and accurate clinical records (hospitalizations from January 1, 2010, to December 31, 2018); and follow-up visits lasting for 1 to 10 years. The exclusion criteria were as follows: pelvic fracture with brain trauma; pelvic fracture with spinal trauma; death from a fractured pelvis; pelvic fractures associated with hypertension, diabetes, prostatic hyperplasia, and delayed gonadal dysfunction; pathological pelvic fracture; incomplete clinical records; and patients with pelvic fracture who refused follow-up visits. The institutional review board of the Affiliated Hospital of Zunyi Medical University approved the present study in September 2018, and all procedures performed in the present study involving human participants were in accordance with the ethical standards of the institutional committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
2.2 Blood tests
To exclude hormonal factors related to ED, the following testosterone levels were measured in peripheral blood plasma by radioimmunoassay: serum total testosterone (TT) and free testosterone (FT), estradiol (E2), luteinizing hormone (LH), and follicle-stimulating hormone (FSH). To exclude metabolic factors related to ED, fasting plasma glucose (FPG), triglyceride (TG), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C), and total cholesterol (TC) levels were determined with a fully automatic biochemical analyzer.
2.3 International index of erectile function-5 (IIEF-5) questionnaires
IIEF-5 questionnaires were completed by all patients. The method was used to categorize ED as follows: no ED (scores of 22–25) or ED (scores of 5–21) according to the literature.[24]
2.4 Diagnosis of pelvic fracture
Pelvic fracture was diagnosed by X-ray and CT.
2.5 Diagnosis and evaluation criteria of ICMI
CT/MRI/MUP was used to diagnose ICMI. The diagnostic criteria of ICMI include at least 2 of the following 4 indicators: Avulsion of the starting tendon of the ICM; ICM swelling, hematoma formation, starting tendon avulsion injury, and the fracture end embedded into the ICM; In the chronic phase, the impaired ICM demonstrated a speckle formation on T2WI showing low signal, and muscle atrophy and fat infiltration on T1WI showing high signal; ICM showed a shortened mean time limit, decreased amplitude and increased multiphase wave at the motor unit potential, or showed a shortened average time limit, decreased amplitude and increased multiphase waves at the motor unit potential.
2.6 Evaluation criteria of reversible/irreversible ED
Evaluation criteria of reversible ED: the course of ED recovered spontaneously within 12 months or with conventional medication within 12 months.
Evaluation criteria of irreversible ED: ED lasted longer than 12 months or did not recover after conventional medication.
2.7 Data extraction
The following parameters were obtained from each participant: age (year); blood pressure; TT, FT, E2, FSH, LH, FPG, TG, TC, and HDL-C levels; IIEF-5 score; presence of ED; type of ED, including reversible and irreversible ED; duration time of ED; presence of ICMI; type of ICMI, including unilateral injury and bilateral injury; type of pelvic fracture and treatment of pelvic fracture; and presence of posterior urethral injury, bladder injury and rectal injury.
2.8 Statistical analyses
Statistical analyses were performed using Statistical Package for the Social Sciences (SPSS Inc, Chicago, Illinois) version 18.0 for windows. The selected characteristics are expressed as the mean and standard deviation (mean ± SD) as well as the percentage (%). Multivariate logistic regression analysis and chi-square test were used, and the multivariate-adjusted odds ratios (ORs) and 95% confidence intervals (CIs) were simultaneously estimated. Differences were considered statistically significant with a P value of < .05.
3 Results
3.1 Clinical baseline characteristics of male patients with pelvic fractures
All of the patients had normal levels of blood hormones, including TT, FT, E2, LH, and FSH. Blood lipids, including TG, TC, LDL-C and HDL-C, blood glucose (FPG), and blood pressure levels, were also normal in these patients (data not shown). The principal characteristics of our study population of male patients with pelvic fractures are listed in Table 1 . A total of 776 men were analyzed, and the mean follow-up period was 67 (range, 12–120) months. The average age was 46 ± 13 (range, 18–67) years. The IIEF-5 score was 19.7 ± 5.9 (range, 5–25). The incidence of ED was 27.3% (212/776), the duration time of ED was 30 ± 23 months, and the incidence of reversible ED was 39.6% (84/212) and of irreversible ED was 60.4% (128/212). The incidence of ICMI was 29.4% (228/776), among which the incidence of unilateral injury was 57.9% (132/228) and of bilateral injury was 42.1% (96/228). Among all pelvic fractures, the incidence of pubic ramus fracture was 88.1% (684/776), pubic body fracture was 12.1% (94/776), ilium fracture was 37.4% (290/776), coccyx fracture was 0.3% (2/776), fracture of the ischium was 8.5% (66/776), fracture of ischial ramus was 10.7% (83/776), pubic symphysis separation was 9.2% (71/776), sacrum fracture was 36.5% (283/776), simple fracture was 1.8% (14/776), and complex fracture was 98.2% (762/776). Furthermore, 73.7% (572/776) of male patients with pelvic fractures were treated conservatively, while 26.3% (204/776) were treated surgically. Posterior urethral injury accounted for 7.1% (55/776), bladder injury accounted for 2.4% (19/776), and rectal injury accounted for 0.8% (6/776).
Table 1: The baseline characteristics of 776 male patients with pelvic fractures.
3.2 The analysis of the related factors of erectile dysfunction after pelvic fracture
In this study, we conducted a correlation analysis of the effects of different types of pelvic fractures, treatment options of pelvic fractures, ICMI, posterior urethral injury, bladder injury, and rectal injury on erectile dysfunction. As shown in Table 2 , we found that bilateral pubic ramus fractures (OR = 15.1, 95% CI: 6.4–35.6, P < .001), bilateral fractures of the ischium (OR = 1.2, 95% CI: 1.1–1.6, P = .006), bilateral fractures of the ischial ramus (OR = 17.9, 95% CI: 2.7–19.2, P = .003), pubic symphysis separation (OR = 2.7, 95% CI: 1.0–7.2, P = .038), unilateral ICMI (OR = 16.8, 95% CI: 2.9–48.4, P < .001), bilateral ICMI (OR = 26.0, 95% CI: 5.5–122.9, P < .001), and posterior urethral injury (OR = 3.7, 95% CI: 1.3–10.5, P = .015) were correlated with the occurrence of ED after pelvic fractures and were independent risk factors for ED after pelvic fractures. However, the presence of ED after pelvic fracture was not significantly correlated with unilateral pubic ramus fracture (OR = 0.4, 95% CI: 0.2–1.0, P = .058), unilateral pubic body fracture (OR = 0.5, 95% CI: 0.3–1.0, P = .067), bilateral pubic body fracture (OR = 0.4, 95% CI: 0.1–1.2, P = .095), unilateral ilium fracture (OR = 1.6, 95% CI: 1.1–2.2, P = .112), bilateral ilium fracture (OR = 1.9, 95% CI: 0.7–5.0, P = .189), coccyx fracture (OR = 2.4, 95% CI: 0.1–38.7, P = .545), unilateral fracture of the ischium (OR = 0.4, 95% CI: 0.1–3.3, P = .429), unilateral fracture of the ischial ramus (OR = 0.6, 95% CI: 0.3–1.5, P = .290), sacrum fracture (OR = 1.0, 95% CI: 0.5–1.7, P = .884), surgical treatment of pelvic fractures (OR = 1.7, 95% CI: 0.9–3.4, P = .127), bladder injury or rectal injury.
Table 2: The analysis of the related factors of erectile dysfunction after pelvic fracture.
3.3 The analysis of the related factors of ischiocavernosus muscle injury after pelvic fracture
In this study, we conducted correlation analyses of the effects of different types of pelvic fractures, treatment options for pelvic fractures, ED, posterior urethral injury, bladder injury, and rectal injury on ICMI. As shown in Table 3 , we found that bilateral pubic ramus fractures (OR = 43.8, 95% CI: 9.3–206.5, P < .001), bilateral pubic body fractures (OR = 20.6, 95% CI: 4.6–92.5, P < .001), pubic symphysis separation (OR = 10.4, 95% CI: 4.4–24.8, P < .001), the surgical treatment of pelvic fracture (OR = 4.1, 95% CI: 2.5–6.7, P < .001), the occurrence of ED (OR = 14.8, 95% CI: 5.9–43.3, P < .001), the occurrence of reversible ED (OR = 15.9, 95% CI: 5.7–43.4, P < .001), and the occurrence of irreversible ED (OR = 25.5, 95% CI: 5.5–112.4, P < .001) were correlated with ICMI and were independent risk factors for ICMI. However, ICMI was not significantly correlated with unilateral pubic ramus fracture (OR = 4.1, 95% CI: 0.9–19.3, P = .079), unilateral pubic body fracture (OR = 0.7, 95% CI: 0.1–5.5, P = .706), unilateral ilium fracture (OR = 1.4, 95% CI: 1.1–2.2, P = .122), bilateral ilium fracture (OR = 0.4, 95% CI: 0.1–1.2, P = .085), coccyx fracture (OR = 2.4, 95% CI: 0.1–37.8, P = .545), unilateral fracture of the ischium (OR = 0.5, 95% CI: 0.2–1.4, P = .171), bilateral fractures of the ischium (OR = 0.5, 95% CI: 0.1–4.0, P = .488), unilateral fracture of the ischial ramus (OR = 1.5, 95% CI: 0.8–3.0, P = .229), bilateral fractures of the ischial ramus (OR = 0.3, 95% CI: 0.0–1.8, P = .182), sacrum fracture (OR = 1.0, 95% CI: 0.6–1.6, P = .963), posterior urethral injury (OR = 0.9, 95% CI: 0.3–2.3, P = .790), bladder injury or rectal injury.
Table 3: The analysis of the related factors of ischiocavernosus muscle injury after pelvic fracture.
3.4 The correlation analysis of different types of ischiocavernosus muscle injuries and different types of erectile dysfunction after pelvic fracture
In this study, we conducted a correlation analysis of different types of ischiocavernosus muscle injuries and different types of erectile dysfunction after pelvic fracture. As shown in Table 4 , we found that unilateral ICMI was correlated with reversible ED, and unilateral ICMI (OR = 2.9, 95% CI: 1.3–6.3, P = .009) was an independent risk factor for reversible ED, while bilateral ICMI was correlated with irreversible ED, and bilateral ICMI (OR = 25.4, 95% CI: 7.2–89.6, P < .001) was an independent risk factor for irreversible ED.
Table 4: The correlation analysis of different types of ischiocavernosus muscle injuries and different types of erectile dysfunction after pelvic fracture.
4 Discussion
In this study, we evaluated the correlation among ICMI, pelvic fracture types, and ED after pelvic fracture. The results showed that the incidence of ED was 27.3%, the duration time of ED was 30 ± 23 months, and the incidence of reversible ED was 39.6% and of irreversible ED was 60.4%. The incidence of ICMI was 29.4%, among which the incidence of unilateral injury was 57.9%, and the incidence of bilateral injury was 42.1%. Among all pelvic fractures, the incidence of pubic ramus fracture was 88.1%, and the incidence of complex fracture was 98.2%. In addition, we found that bilateral pubic ramus fractures, bilateral fractures of the ischial ramus, pubic symphysis separation, unilateral ICMI, bilateral, and posterior urethral injury were correlated with the occurrence of ED after pelvic fractures and were independent risk factors for ED after pelvic fractures. At the same time, we also found that bilateral pubic ramus fractures, bilateral pubic body fractures, pubic symphysis separation, the surgical treatment of pelvic fracture, and the occurrence of ED/reversible ED/irreversible ED were correlated with ICMI and were independent risk factors for ICMI. Through further analysis, we found that unilateral ICMI was correlated with reversible ED, and unilateral ICMI was an independent risk factor for reversible ED, while bilateral ICMI was correlated with irreversible ED, and bilateral ICMI was an independent risk factor for irreversible ED. Therefore, we believe that ICMI is associated with ED and may be a cause for ED, while pubic ramus fracture and pubic symphysis separation may be the main causes of ICMI.
The above results obtained by us are quite different from previous research results of other scholars. Previous studies have shown that ED after pelvic fractures is mainly caused by nerve injury and blood vessel injury. Of course, there are also psychogenic factors.[5,25–27] [23,28,29] [21] [21] Fig. 1 ) and performed ICM electromyography examination on some patients, which resulted in abnormal electromyography evidence (see Fig. 2 ). Meanwhile, in this study, nerve evoked potential detection was performed on the adjacent muscles of ICM, including the bulbar spongiform muscle and the muscles of the medial thigh, and the results indicated no significant nerve damage (data not shown). This is the main reason why we conducted this study, and indeed, through this study, we proved the possibility of our view on the relationship between ICMI and different types of pelvic fractures and ED after pelvic fractures. Our findings are expected to attract the attention of colleagues, and in clinical work, we expect to focus on the diagnosis of ICMI-induced ED in male patients with pelvic fractures and conduct further research with follow-up treatment.
Figure 1: The appearance of ischiocavernosus muscle injury is shown by computed tomography/magnetic resonance imaging after pelvic fracture. (A) The normal ICM; (B, C) avulsion of the starting tendon of the ICM; (D) ICM swelling, hematoma formation, starting tendon avulsion injury, and the fracture end embedded into the ICM; (E, F) in the chronic phase, the impaired ICM demonstrated a speckle formation on T2WI showing low signal, and muscle atrophy and fat infiltration on T1WI showing high signal (→ was shown in). The area indicated by the red arrow is ICM injuries.
Figure 2 The present study has some limitations. In this study, we did not perform a nocturnal penile tumescence test, duplex ultrasonography of the penis, or cavernography of the penis. These examinations are currently recommended etiological examination methods for determining ED, and we only analyzed the correlation between all types of ED after pelvic fracture and ICMI. This results in a certain deficiency that needs to be further explained. However, this also gives us a direction for our future research.
In conclusion, in this study, we systematically analyzed the correlation among ICMI, types of pelvic fractures and ED after pelvic fractures through large clinical sample data. Our results showed that pubic ramus fracture, ischial ramus fracture, and pubic symphysis separation were strongly correlated with ICMI, and ICMI was strongly correlated with ED after pelvic fracture. Moreover, pubic ramus fracture, ischial ramus fracture, and pubic symphysis separation were independent risk factors for ICMI, and ICMI was an independent risk factor for ED after pelvic fracture. Therefore, we conclude that ICMI is associated with ED and may be a cause for ED, while pubic ramus fracture, ischial ramus fracture, and pubic symphysis separation may be the main causes of the high credibility and high clinical value of ICMI.
Acknowledgments
The authors acknowledge the efforts of the participants and investigators of the study.
References
1. Rew KT, Heidelbaugh JJ. Erectile dysfunction. Am Fam Physician. 2016;94: 820–827.
2. Shenfeld OZ, Kiselgorf D, Gofrit ON, et al. The incidence and causes of erectile dysfunction after pelvic fractures associated with posterior urethral disruption. J Urol. 2003;169:2173–2176.
3. Cai L, Jiang M, Wen Y, et al. Forensic identification for erectile dysfunction: experience of a single center. Urology. 2015;86:68–71.
4. Blaschko SD, Sanford MT, Schlomer BJ, et al. The incidence of erectile dysfunction after pelvic fracture urethral injury: a systematic review and meta-analysis. Arab J Urol. 2015;13:68–74.
5. Sangkum P, Levy J, Yafi FA, et al. Erectile dysfunction in urethral stricture and pelvic fracture urethral injury patients: diagnosis, treatment, and outcomes. Andrology. 2015;3:443–449.
6. El-Assmy A, Harraz AM, Benhassan M, et al. Erectile dysfunction post-perineal anastomotic urethroplasty for traumatic urethral injuries: analysis of incidence and possibility of recovery. Int Urol Nephrol. 2015;47:797–802.
7. Peng J, Zhang Z, Cui W, et al. Role of nocturnal penile erection test on response to daily sildenafil in patients with erectile dysfunction due to pelvic fracture urethral disruption: a single-center experience. Urology. 2014;84:1389–1394.
8. Morey AF. Re: predictors of erectile dysfunction post pelvic fracture urethral injuries: a multivariate analysis. J Urol. 2014;191:383.
9. Koraitim MM. Predictors of erectile dysfunction post pelvic fracture urethral injuries: a multivariate analysis. Urology. 2013;81:1081–1085.
10. Tang CY, Fu Q, Cui RJ, et al. Erectile dysfunction in patients with traumatic urethral strictures treated with anastomotic urethroplasty: a single-factor analysis. Can J Urol. 2012;19:6548–6553.
11. Zuckerman JM, McCammon KA, Tisdale BE, et al. Outcome of penile revascularization for arteriogenic erectile dysfunction after pelvic fracture urethral injuries. Urology. 2012;80:1369–1373.
12. Hefzy MS, Ebraheim N, Mekhail A, et al. Kinematics of the human pelvis following open book injury. Med Eng Phys. 2003;25:259–274.
13. Harvey-Kelly KF, Kanakaris NK, Eardley I, et al. Sexual function impairment after high energy pelvic fractures: evidence today. J Uml. 2011;185:2027–2034.
14. Feng C, Xu YM, Yu JJ, et al. Risk factors for erectile dysfunction in patients with urethral strictures secondary to blunt trauma. J Sex Med. 2008;5:2656–2661.
15. Malavand B, Mouzin M, Trieoire JL, et al. Evaluation of male sexual function after pelvic trauma by the international index of erectile function. Urology. 2000;55:842–846.
16. Metze M, Tiemann AH, Josten C. Male sexual dysfunction after pelvic fracture. J Trauma. 2007;63:394–401.
17. Gibbons KJ, Soloniuk DS, Razack N. Neurological injury and patterns of sacral fractures. J Neurosurg. 1990;72:889–893.
18. Bushnell BD, Dirschl DR. Small bowel obstruction from entrapment in a sacral fracture stabilized with iliosacral screws: case report and review of the literature. J Trauma. 2008;65:933–937.
19. Koraitim MM, Marzouk ME, Atta MA, et al. Risk factors and mechanism of urethral njury in pelvic fractures. Brit J Urol. 1996;71:876.
20. Mark SD, Keane TE, Vandermark RM, et al. Impotence following pelvic fracture urethral injury: incidence, aetiology and management. Br J Urol. 1995;75:62–64.
21. Liu T, Chen Z-P, Deng J-C, et al. Influence of different cutting combinations of cavernous nerves, cavernous vessels, and ischiocavernosus muscles on erectile dysfunction in rat models. Int J Clin Exp Med. 2019;12:5622–5629.
22. Peikert K, May CA. Muscle spindles in the human bulbospongiosus and ischiocavernosus muscles. Muscle Nerve. 2015;52:55–62.
23. Shafik A, Shafik I, El-Sibai O, et al. Effect of external anal sphincter contraction on the ischiocavernosus muscle and its suggested role in the sexual act. J Androl. 2006;27:40–44.
24. van Kollenburg RAA, de Bruin DM, Wijkstra H. Validation of the electronicversion of the international index of erectile function (IIEF-5 and IIEF-15): a crossover study. J Med Internet Res. 2019;21:e13490.
25. Guan Y, Wendong S, Zhao S, et al. The vascular and neurogenic factors associated with erectile dysfunction in patients after pelvic fractures. Int Braz J Urol. 2015;41:959–966.
26. Wong NC, Allard CB, Dason S, et al. Management of pelvic fracture-associated urethral injuries: a survey of Canadian urologists. Can Urol Assoc J. 2017;11:E74–E78.
27. Hosseini J, Soleimanzadeh Ardebili F, Fadavi B, et al. Effects of anastomotic posterior urethroplasty (simple or complex) on erectile function: a prospective study. Urol J. 2018;15:33–37.
28. Hsieh CH, Liu SP, Hsu GL, et al. Advances in understanding of mammalian penile evolution, human penile anatomy and human erection physiology: clinical implications for physicians and surgeons. Med Sci Monit. 2012;18:RA118–RA125.
29. Shafik A, Shafik AA, El Sibai O, et al. The response of the corporal tissue and cavernosus muscles to urethral stimulation: an effect of penile buffeting of the vaginal introitus. J Androl. 2007;28:853–857.
