The human T-lymphotropic virus type 1 (HTLV-1) is a retrovirus that has infected 10 to 20 million people worldwide.[1,2] HTLV-1 is a lymphotropic virus that is related to two human lymphoma types, including adult T-cell lymphoma leukemia (ATLL) and HTLV-1- associated myelopathy/tropical spastic paraparesis (HAM/TSP).[1,2] HTLV-1 is transmitted through blood and sexual intercourse.[1,2] However, the disease becomes symptomatic in only 5% of the infected individuals.[3,4] HTLV-1 is endemic in some parts of the world including Japan, Brazil, North Palestine, and North and North-East Iran.[2,5] The prevalence of HTLV-1 in Mashhad City, which is located in North-East of Iran, is estimated to be as high as 12.2%.
The chronic nature of the disease and the high rate of asymptomatic carriers with an unknown estimation of disease activation can induce a great psychological burden for HTLV-1-infected patients. Few studies evaluated psychological disorders in HTLV-1. Based on the findings of these studies, regardless of being a carrier or having the disease, 42% of the infected patients have psychological abnormalities.[7,8] The reported psychological abnormalities included mood disorder (34%), anxiety (22%), and alcoholism (2%). The prevalence of psychological abnormalities was reported to be similar to its prevalence in other chronic diseases.[7,8] However, there is an inconsistency between the findings of the studies that evaluated psychological abnormalities among HTLV-1 patients. While some studies showed that the prevalence of psychiatric disorders was significantly higher among HTLV-1 asymptomatic carriers compared to the general population,[10–12] some other studies reported no significant difference in the prevalence of depression between HTLV-1 and healthy subjects.[13,14]
Sexual function is an important determinant of quality of life.[15,16] Sexual dysfunction is common among patients with chronic conditions.[17,18] Sexual dysfunction may affect patients in any of the desire, satisfaction, lubrication, orgasm, and pain domains. A study also showed that changes in female sexual function could be an indicator of an underlying condition. Therefore, considering the neurological involvement in HTLV-1 disease, sexual function can be hypothetically impaired in this disease. A few cross-sectional studies showed that the prevalence of sexual dysfunction among seropositive HTLV-1 patients who did not develop myelopathy was higher than in the general population.[21–23]
Considering the discrepancies between the findings of previous studies, the high prevalence of HTLV-1 in the North-East of Iran, and the importance of sexual dysfunction in life, this study was conducted to evaluate the prevalence of sexual dysfunction in asymptomatic men and women with HTLV-1 infection and to identify the relationship between sexual dysfunction and psychological disorders.
MATERIALS AND METHODS
The study protocol was approved by the Ethical Committee of the Mashhad University of Medical Sciences (Code: IR.MUMS.MEDICAL.REC 1398.885).
This cross-sectional study was performed on patients with HTLV-1 disease referred to the Neurology Clinic of the Ghaem Hospital, Mashhad, Iran. HTLV-1 infection was confirmed by Western blot or polymerase chain reaction (PCR). Written informed consent was obtained from all patients before participating in the study. All patients were evaluated by a neurologist. An expanded disability status scale (EDSS) was used to rate patient disability by the neurologist.
Inclusion criteria were documented HTLV-1 diagnosis based on the enzyme-linked immune assay (ELISA) and then confirmed with a Western blot or PCR, willingness to participate in the study, being within the age range of 18 to 80 years old for men and 18 to 55 years old for women, being married, having sexual intercourse in the past four years, the EDSS below 2. Exclusion criteria were having spastic paraparesis based on neurologist evaluation, having uveitis or leukemia, having penile prosthesis, history of prostatectomy, any history of surgery on ovaries, uterus or vagina, positive history for cancer, having neurologic diseases, renal or liver failure, menopause, consumption of medications that affect the central nervous system or genitourinary system.
The sample size was calculated based on the formula for estimating a qualitative variable in the population considering a type 1 error of 5%. Based on the findings of the study by Castro et al., the sample size was calculated as 114. Considering the 10% dropout, the sample size was increased to 127 patients.
Expanded disability status scale (EDSS): This scale is used to evaluate the functional systems of the central nervous system (CNS) by clinicians. EDSS questionnaire items are scored based on a 10-point ordinal scale ranging from 0 indicating normal neurological findings to 10 indicating death due to neurological involvement.
Brief male sexual function inventory (BMFSI): This 15-item questionnaire is used to evaluate male sexual dysfunction in five domains. The domains include erection, ejaculation, sexual drive, problem assessment, and overall satisfaction. Each item is scored based on a five-point Likert scale with a score of 1 indicating worst and a score of 5 indicating best condition. The sum of the score for each domain and the total score was calculated for the patients. Therefore, the total score would range from 15 to 75. Scores between 15 and 25 indicate low sexual function, scores between 25 and 50 indicate moderate sexual function and scores higher than 50 indicate high sexual function. The Persian translation of the BMFSI questionnaire was previously validated on Iranian patients (Cronbach’s alpha = 0.85).
Female sexual function index (FSFI): This 19-item questionnaire is used to evaluate female sexual function in 6 domains. The domains include desire, arousal, lubrication, orgasm, satisfaction, and pain. Each item is scored based on a 6-point Likert scale ranging from 0 indicating no sexual activity in the past four weeks to 5 indicating high satisfaction. The sum of the score for each domain and the total score was calculated for the patients. Therefore, the total score would range between 6 and 36. The higher FSFI scores indicate better sexual functioning. The cut-off for the total FSFI score is 28, while the cut-offs for FSFI domains include 3.3 for desire, 3.4 for each of the arousal, lubrication, and orgasm domains, and 3.8 for each of the satisfaction and pain domains. The Persian translation of the FSFI questionnaire was previously validated on the Iranian population (Cronbach’s alpha = 0.70).
The symptom checklist-90-revised (SCL-90-R): This 90 items self-report questionnaire is used for rapid evaluation of the type and severity of psychological symptoms. The SCL-90-R items are scored based on a five-point Likert scale ranging from 0 indicating none to 4 indicating severe. Patients should have a minimum of 6-grade education to be able to respond to the questionnaire items. SCL-90-R evaluates psychological symptoms in 9 dimensions, including somatization, obsessive-compulsive, interpersonal sensitivity, depression, anxiety, hostility, phobic anxiety, paranoid ideation, and psychoticism. This questionnaire includes three indices, global severity index (GSI), positive symptom distress index (PSDI), and positive symptom total (PST). These indices are used for the scoring and interpretation of the SCL-90-R questionnaire. The mean and standard deviation (SD) for the SCL-90-R score are 50 and 10. Higher scores in each domain indicate the higher severity of psychological symptoms in that domain. The Persian translation of the SCL-90-R questionnaire was previously validated on the Iranian population (Cronbach’s alpha = 0.98, Cronbach’s alpha for domains ranged between 0.75 and 0.92).
Demographic data including age, gender, time of HTLV-1 diagnosis, underlying diseases (hypertension and diabetes), atherosclerosis risk factors, including low-density lipoprotein (LDL), high-density lipoprotein (HDL), triglyceride (TG), metabolic syndrome, waist circumference, and socio-economic status (education level, marital status, and income level). The cut-off for categorizing income level was a monthly income of 20 Million Rials (equivalent to 80 US$). All patients filled out the SCL-90-R and EDSS questionnaires in the clinic. Male patients filled out the BMFSI, while female patients filled out the FSFI questionnaire.
Data were analyzed using the statistical package for social sciences (SPSS) software version 16. The Shapiro-Wilk test was used to evaluate the normality distribution of continuous variables. Mean and standard deviation (SD); and median and interquartile range (IQR) were used to present continuous variables with normal and non-normal distribution, respectively. Frequency and percentage were used to describe continuous and categorical variables, respectively. Since the number of male patients with low sexual function was small, a statistical comparison was not possible; therefore, the low and moderate sexual function groups were merged. Continuous variables were compared between groups using the independent t-test or the Mann-Whitney test based on normality. Comparison of the distribution pattern of the categorical variables was performed using the Chi-square or Fisher exact tests. All tests were two-tailed and a P < 0.05 was considered statistically significant.
Of the 127 identified patients, 117 (92.1%) patients had documented diagnoses of HTLV-1 based on ELISA and Western blot or PCR and were included in the study. Among these 117 patients, 56 (47.9%) were female and 61 (52.1%) were male. The mean age of the patients was 35.3 ± 6.3 years. All patients were married. The mean duration of HTLV-1 infection diagnosis was 3.7 ± 3.0 years. More than half (68, 58.1%) of the patients had a high income. Most of the patients (54, 46.9%) had university degrees, while high school graduates, middle school, and primary school comprised 32 (27.4%), 25 (21.4%), and 6 (5.1%) of the population, respectively.
The mean score for SCL-90-R, BMFSI, and FSFI and their domains are presented in Table 1. Among the 61 male patients, 6 patients did not report sexual intercourse in the past 4 weeks and were excluded from the analysis. Among the 55 remaining male patients, 7 (12.7%) had a low sexual function, 20 (36.4%) had a moderate sexual function and 28 (50.9%) had a high sexual function. The sexual function status of the 56 female patients in this study is presented in Figure 1. Based on the total FSFI score 34 (60.7%) female patients had a poor sexual function and 22 (39.3%) had a good sexual function.
A comparison of the demographic variables between categories of sexual function is presented in Table 2. There was a significant difference in the mean age between sexual function status groups in both the male (P = 0.004) and female patients (P = 0.047). There was a significant difference in the mean number of children between sexual function status groups in both the male (P = 0.006) and female patients (P = 0.007). However, there was a significant difference in the distribution pattern of economic status between sexual function status groups only in male patients (P < 0.001).
A comparison of SCL-90 total and domain scores between sexual function categories among female patients is presented in Table 3. Among female patients, there was a significant difference in depression (P = 0.001), interpersonal sensitivity (P = 0.017), anxiety (P = 0.006), psychoticism (P = 0.002), and GSI (P = 0.002) scores between patients with good and poor sexual function. This finding indicates that the score in these SCL-90 domains was significantly higher in female patients with poor sexual function compared to those with good sexual function. A comparison of the SCL-90-R total and domain categories between sexual function categories among male patients is presented in Figure 2. There was no significant difference in any of the SCL-90 domains between sexual function categories.
A comparison of FSFI domain scores between sexual function categories among female patients is presented in Figure 3. The prevalence of depression was significantly higher in patients with poor sexual function compared to those with good sexual function based on desire, arousal, lubrication, orgasm, satisfaction, and pain (P < 0.05). The prevalence of hostility was significantly higher in patients with poor sexual function compared to those with good sexual function based on desire and arousal (P < 0.05). The prevalence of interpersonal sensitivity was significantly higher in patients with poor sexual function compared to those with good sexual function based on lubrication, orgasm, and satisfaction (P < 0.05). The prevalence of paranoid ideation was significantly higher in patients with poor sexual function compared to those with good sexual function based on arousal (P = 0.048). The prevalence of psychological abnormality was significantly higher in patients with poor sexual function compared to those with good sexual function based on desire, arousal, lubrication, orgasm, and satisfaction (P < 0.05) [Figure 2].
Chronic disease can have a significant effect on sexual function in both the patient and the partner. All domains of sexual function can be affected by chronic diseases. The effect of chronic disease on sexual function is multifactorial and can be due to both the physiological and psychological effects of chronic diseases. Physiologically, chronic disease can cause erectile dysfunction, ejaculation delay, and anorgasmia in men and reduced lubrication, delayed orgasm or anorgasmia, and reduced orgasm intensity in women. However, the psychological effects of chronic disease including chronic stress, anxiety, reduced self-esteem, and disease-related changes in the relationship between couples can also alter sexual function. Being a chronic disease with neurological involvement makes HTLV-1 a risk factor for sexual dysfunction in patients. This study aimed to evaluate sexual function in both men and women with asymptomatic HTLV-1 and to evaluate the relationship between sexual dysfunction and psychiatric disorder.
The findings of this study showed that the prevalence of sexual dysfunction was low among men (12.7%) and moderate among women (36.4%). Mean age and number of children were significantly higher in male patients with low sexual function compared to those with high sexual function, while the prevalence of poor economic status was significantly higher in the moderate sexual function category compared to other categories. Among female patients, depression was significantly more prevalent in patients with bad sexual function compared to those with good sexual function based on desire, arousal, lubrication, orgasm, satisfaction, and pain. The frequency of hostility, interpersonal sensitivity, paranoid ideation, and psychological abnormalities was significantly higher in female HTLV-1 patients with bad sexual function compared to those with good sexual function based on at least one of the FSFI domains. Furthermore, the mean age and number of children were significantly higher in female patients with bad sexual function compared to those with good sexual function.
Similar to the findings of the current study in terms of male sexual function in asymptomatic HTLV-1 patients, two previous studies on male patients with HTLV-1 infection who had an EDSS score of 0, showed that increased age was significantly related to erectile dysfunction in patients with HTLV-1 infection.[22,35] In contrast to the findings of the current study, a study on male asymptomatic HTLV-1 patients showed that erectile dysfunction was related to psychological abnormalities. However, the current study found a significant difference in GSI between male patients with bad sexual function compared to those with good sexual function. The reason for this difference might be the different sample sizes of the studies as well as the different outcome measurement tools used in the studies. While our study used the BMFSI questionnaire, which evaluates different domains of sexual function, the mentioned study used the international index of erectile function. To the best of our knowledge, few studies have evaluated sexual function in patients with HTLV-1 infection.
In contrast to the findings of the current study in terms of the prevalence of sexual dysfunction among asymptomatic female patients with HTLV-1, the prevalence of sexual dysfunction was reported to be 54.4% in a study on 72 female HTLV-1 patients, which was higher than the prevalence of female sexual dysfunction in our study. The reason for the difference might be related to the geographical differences as the prevalence of sexual dysfunction among healthy women in the mentioned study was higher than the prevalence of female sexual dysfunction in the patient population in our study (44.9% and 36.4%, respectively).
Similar to the findings of the current study in terms of the relationship between female sexual dysfunction and demographic characteristics in asymptomatic HTLV-1 carriers, a study on 72 female patients with HTLV-1 infection reported that the mean number of children was significantly higher in patients with sexual dysfunction. It was previously shown that sexual satisfaction was significantly higher among nulliparous healthy women. Therefore, it can be hypothesized that although sexual function among asymptomatic female HTLV-1 patients was more prevalent compared to healthy individuals, these patients are similarly affected by parity. However, a previously mentioned study showed that the prevalence of poor economic status and low education level was significantly higher in female patients with sexual dysfunction, which was in contrast to the findings of our study. The reason for this difference might be the unequal distribution of patients in different sexual function categories in the current study, which prevented us from achieving a significant difference. A systematic review of 135 studies from 41 countries on healthy women showed that poor physical and mental health, stress, genitourinary problems, and dissatisfaction in relationship with the spouse were among the risk factors for poor female sexual function in healthy women, while the effect of age, education, and employment on female sexual function was unclear. The study hypothesized that an increased education level might result in increased awareness of sexual needs and rights and thus may cause more sexual dissatisfaction when facing life sexual experiences in couples. The study also found a relationship between low economic status and problems in desire. Therefore, the findings of the current study in terms of no relation between economic education level and female sexual function in asymptomatic HTLV-1 patients might be justifiable. However, considering the lack of relationship between sexual function and economic and educational status, it can be hypothesized that the observed poor sexual function among asymptomatic female HTLV-1 patients might be attributed to other physical and mental factors that have not been evaluated in the current study.
One of the limitations of our study was a patient refusal to participate in the study due to cultural taboos. Another limitation of our study was the unequal distribution of patients in each sexual function category. This shortcoming may be addressed by using a stratified sampling method in further studies. The strength of our study was the inclusion of patients of both sexes in one study. This study design provides a real-time measure of the condition among both sexes who live in almost similar geographical regions and times.
The present study provides new information regarding the psycho-sexual consequences of the virus. As far as we know, many of the findings are the first in our research. The results of the study emphasize that it is important to pay attention to the psychological problems of virus carriers and their impact on sexual function, especially in women.
Financial support and sponsorship
The funding source had no role in the preparation of this manuscript.
Conflicts of interest
The authors have no conflict of interest to declare.
This study was performed as the thesis for the medical doctorate degree of the second author (P9505). The author should appreciate the support of Vice-chancellor for research at Mashhad University of Medical Sciences (971875).
1. Kaplan JE, Osame M, Kubota H, Igata A, Nishitani H, Maeda Y, et al. The risk of development of HTLV-I-associated myelopathy/tropical spastic paraparesis among persons infected with HTLV-I. J Acquir Immune Defic Syndr (|y1988) 1990;3:1096-101
2. Miller M, Achiron A, Shaklai M, Stark P, Maayan S, Hannig H, et al. Ethnic cluster of HTLV-I infection in Israel among the Mashhadi Jewish population. J Med Virol 1998;56:269-74
3. Osame M, Usuku K, Izumo S, Ijichi N, Amitani H, Igata A, et al. HTLV-1 associated myelopathy. A new clinical entity. Lancet 1986;327:1031-2
4. Gessain A, Barin F, Vernant JC, Gout O, Maurs L, Calender A, et al. Antibodies to human T-lymphotropic virus type-I in patients with tropical spastic paraparesis. Lancet 1985;2:407-10
5. Rafatpanah H, Hedayati-Moghaddam MR, Fathimoghadam F, Bidkhori HR, Shamsian SK, Ahmadi S, et al. High prevalence of HTLV-I infection in Mashhad, Northeast Iran: A population-based seroepidemiology survey. J Clin Virol 2011;52:172-6
6. Zihlmann KF, de Alvarenga AT, Casseb J. Living Invisible: HTLV-1-Infected Persons and the lack of care in public health. PLoS Negl Trop Dis 2012;6:e1705
7. Fullerton C, Florenzano R, Acuna J. Comorbidity of chronic diseases and psychiatric disorders among patients attending public primary care. Rev Med Chil 2000;128:729-34
8. Bellini M, Bruschi C, Franchini L, Giacanelli F, Gritti FM, Ferrari G, et al. Diagnosi psichiatrica di depressione maggiore in soggetti con infezione HIV. Minerva psichiatrica 1994;35:129-38
9. Joaquim de Carvalho AG, Galvão-Phileto AV, Lima NS, Santos de Jesus R, Galvão-Castro B, Lima MG. Frequency of mental disturbances in HTLV-1 patients in the state of Bahia, Brazil. Braz J Infect Dis 2009;13:5-8
10. Stumpf BP, Carneiro-Proietti AB, Proietti FA, Rocha FL Interdisciplinary HTLV Research Group. Higher rate of major depression among blood donor candidates infected with human t-cell lymphotropic virus type 1. Int J Psychiatry Med 2008;38:345-55
11. Castro N, Oliveira P, Freitas D, Rodrigues W, Muniz A, Carvalho E. Erectile dysfunction and HTLV-I infection: A silent problem. Int J Impot Res 2005;17:364-9
12. Souza LS, Lins-Silva DH, Dorea-Bandeira I, Barouh JL, Tolentino A, Bandeira ID, et al. Prevalence and factors associated with depression and anxiety in people living with HTLV-1: A systematic review with meta-analysis and meta-regression. Gen Hosp Psychiatry 2021;73:54-63
13. Guiltinan AM, Kaidarova Z, Behan D, Marosi C, Hutching S, Kaiser M, et al. Major depression and generalized anxiety disorder among human T-lymphotropic virus Types I–and II–infected former blood donors. Transfusion 2013;53:60-8
14. Gascón MRP, Capitão CG, Casseb J, Nogueira-Martins MCF, Smid J, de Oliveira ACP. Prevalence of anxiety, depression and quality of life in HTLV-1 infected patients. Braz J Infect Dis 2011;15:578-82
15. Chang SR, Yang CF, Chen KH. Relationships between body image, sexual dysfunction
, and health-related quality of life among middle-aged women: A cross-sectional study. Maturitas 2019;126:45-50
16. Tepavcevic DK, Kostic J, Basuroski ID, Stojsavljevic N, Pekmezovic T, Drulovic J. The impact of sexual dysfunction
on the quality of life measured by MSQoL-54 in patients with multiple sclerosis. Mult Scler 2008;14:1131-6
17. Lou WJ, Chen B, Zhu L, Han SM, Xu T, Lang JH, et al. Prevalence and factors associated with female sexual dysfunction
in Beijing, China. Chin Med J (Engl) 2017;130:1389-94
18. Owiredu WKBA, Owusu AO, Amidu N, Quaye L, Gyasi-Sarpong CK, Dapare PPM, et al. Sexual dysfunction
and sexual quality of life among the physically challenged in the kumasi metropolis, ghana. Health and Quality of Life Outcomes 2015;13:3
19. Courtois F, Gérard M, Charvier K, Vodušek DB, Amarenco G. Assessment of sexual function in women with neurological disorders: A review. Ann Phys Rehabil Med 2018;61:235-44
20. Di Stasi V, Verde N, Maseroli E, Scavello I, Cipriani S, Todisco T, et al. Female sexual dysfunction
as a warning sign of chronic disease development. Current Sexual Health Reports 2019;11:307-19
21. Silva MTT, Mattos P, Alfano A, Araújo AQ-C. Neuropsychological assessment in HTLV-1 infection: A comparative study among TSP/HAM, asymptomatic carriers, and healthy controls. J Neurol Neurosurg Psychiatry 2003;74:1085-9
22. Oliveira P, Castro NM, Muniz AL, Tanajura D, Brandão JC, Porto AF, et al. Prevalence of erectile dysfunction in HTLV-1–infected patients and its association with overactive bladder. Urology 2010;75:1100-3
23. Martins ALL, Grassi MFR, de Aquino Firmino A, Araujo JPL, Paixao TS, Galvão-Castro B, et al. Human T-lymphotropic virus-1–associated myelopathy/tropical spastic paraparesis is associated with sexual dysfunction
in infected women of reproductive age. Sex Med 2018;6:324-31
24. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS). Neurology 1983;33:1444-52
25. Rosen RC, Riley A, Wagner G, Osterloh IH, Kirkpatrick J, Mishra A. The international index of erectile function (IIEF): A multidimensional scale for assessment of erectile dysfunction. Urology 1997;49:822-30
26. Aliakbari Dehkurdi M, Alipour A, Zare H, Shahidi G, Barghi Irani Z. The effectiveness of cognitive-behavioral therapy with old people (CBTO) on quality of life in patients who suffered from Parkinson Disease (PD). Research in Psychological Health 2014;7:23-33
27. Rosen R, Brown C, Heiman J, Leiblum S, Meston C, Shabsigh R, et al. The Female Sexual Function Index (FSFI): A multidimensional self-report instrument for the assessment of female sexual function. J Sex Marital Ther 2000;26:191-208
28. Mohammadi kh, Heydari M, Faghihzadeh S. The female sexual function index (fsfi): Validation of the iranian version. Payesh 2008;7:269-78
29. Groth-Marnat G. Handbook of psychological assessment. John Wiley & Sons. 2009
30. Anisi J, Babaei S, Barani M, Mohammadlo H, Ebrahimi F. Determine the psychometric properties by Symptom Checklist-90-Revised (SCL-90-R) among military forces. EBNESINA 2016;17:13-8 Available from: http://ebnesina.ajaums.ac.ir/article-1-316-en.html
. [Last accessed on 2023 Apr 25]
31. Parish KL. Sexuality and haemophilia: Connections across the life-span. Haemophilia 2002;8:353-9
32. Verschuren JEA, Enzlin P, Dijkstra PU, Geertzen JHB, Dekker R. Chronic disease and sexuality: A generic conceptual framework. J Sex Res 2010;47:153-70
33. Carrillo González GM, Sánchez Herrera B, Chaparro Díaz L. Chronic disease and sexuality. Investigación y Educación en Enfermería 2013;31:295-304
34. Fisher B, Graham K, Duffecy J, McAnulty R, Burnette M. Chronic disease, disability, and sexuality. Sexual Function and Dysfunction. Westport, CT: Praeger. 2006;2:233-60
35. de Oliveira CJV, Neto JAC, Andrade RCP, Orge MdLG, de Matos SNFL, Rocha PN, et al. Hormonal and psychogenic risk factors for erectile dysfunction in men with HTLV-1. J Sex Med 2019;16:1763-8
36. McCool-Myers M, Theurich M, Zuelke A, Knuettel H, Apfelbacher C. Predictors of female sexual dysfunction
: A systematic review and qualitative analysis through gender inequality paradigms. BMC Womens Health 2018;18:108