Perspectives on menopause and women with HIV

Figures & data

Figure 1 The stages of the menopausal transition in women.

Notes: **Approximate expected level based on assays using current international pituitary standard. From Harlow SD, Gass M, Hall JE, et al. Executive summary of the stages of reproductive aging workshop +10: addressing the unfinished agenda of staging reproductive aging. Menopause. 2012;19(4):387–395.²¹ With permission from Wolters Kluwer Health, Inc. Copyright ©2012.
Abbreviations: FSH, follicle-stimulating hormone; FMP, final menstrual period; AMH, anti-Mullerian hormone.

Table 1 Classification of menopausal states^14,15,22

Term	Definition
Natural menopause	Permanent cessation of menstruation resulting from a loss of ovarian follicular activity; diagnosis is made retrospectively after 12 months of amenorrhea in the absence of any other pathological or physiological cause
Perimenopause	The period immediately prior to menopause, when the endocrinological, biological, and clinical features of approaching menopause commence, and the first year after menopause
Premature menopause (or premature ovarian failure)	Menopause that occurs at an age less than two standard deviations below the mean established for the reference population; generally, refers to menopause prior to the age of 40 years
Induced menopause	Cessation of menstruation that follows either surgical removal of both ovaries (with or without hysterectomy) or iatrogenic ablation of ovarian function (including chemotherapy or radiation therapy)

Table 2 Summary of studies assessing age of menopause in women with HIV

Authors	Study design	Location	Population	Menopause definition	Findings
Clark et al^Citation84	Cross-sectional	USA	52 HIV-positive women ≥40 years with adequate menopausal information; 50% postmenopausal	• FSH >35 mU/mL or	Mean age of menopause was 47 years (range 32–57 years)
				• Self-report of amenorrhea >6 months with age ≥55 years or
				• Investigator’s diagnosis
Schoenbaum et al^Citation81	Cross-sectional	USA	571 women 52.9% HIV-positive; 17.8% postmenopausal	Self-report of amenorrhea >12 months	HIV independently associated with risk of menopause (OR 1.73)
					Among those with HIV, having a CD4 count >500 (OR 0.191) or CD4 200–500 (OR 0.346) associated with decreased risk of menopause
					In HIV-positive women:
					• median age of menopause was 46 years (IQR 39–49 years)
					• 26% had early menopause
					In HIV-negative women:
					• median age of menopause was 47 years (IQR 44.5–48 years)
					• 10% had early menopause
Boonyanurak et al^Citation82	Cross-sectional	Thailand	268 HIV-positive women ≥40 years of age; 20.5% women postmenopausal	Self-report of amenorrhea >12 months	Mean age of menopause was 47.3 years (SD 5.1 years); this was 2.2 years earlier than the mean age of menopause in general population in Thailand of 49.5 years (SD 3.1 years)
Calvet et al^Citation19	Prospective cohortstudy Study followed premenopausal women enrolled between 1996 and 2010	Brazil	667 HIV-positive women ≥30 years of age who were followed for a median of 5 years	Self-report of amenorrhea >12 months	Natural menopause occurred in 132/667 women during follow-up:
					• median age of menopause was 48 years (IQR 45–50 years)
					• 27% had early menopause (<45 years)
					• 2.3% had premature menopause (<40 years)
					Early natural menopause associated with:
					• early menarche (HR 2.70)
					• smoking (HR 3.00)
					• HCV coinfection (HR 6.26)
					• CD4 count <50 (HR 6.64)
Fantry et al^Citation13	Cross-sectional	USA	120 HIV-positive women ≥40 years of age; 25% postmenopausal	Self-report of amenorrhea >12 months	Median age of menopause was 50 years (95% CI 49–53 years)
					• 20% had early menopause (40–45 years)
					• 35% had premature menopause (<40 years)
Cejtin et al^Citation85	Cross-sectional evaluation of data collected from the prospective Women’s Interagency Health Study (WIHS)	USA	1,431 women ≤55 years of age • 1,139 HIV-positive • 292 HIV-negative	Self-report of no menstrual period on 2 sequential visits with elevated FSH (>25 mIU/mL)	Median age of menopause was 47 years (range 35–55 years) (no difference between HIV-positive and HIV-negative women)
					In HIV-positive women, no association of menopause with CD4 count, virologic suppression, AIDS-defining illness or ART
Ferreira et al^Citation80	Cross-sectional	Brazil	96 HIV-positive and 155 HIV-negative women ≥40 years of age	Self-report of amenorrhea >12 months	Median age of menopause in HIV-positive women was 47.5 years
de Pommerol et al^Citation74	Prospective cohort study	France	404 HIV-positive women, followed for a median of 8.8 years; 24.3% postmenopausal	Self-report of amenorrhea >12 months	24.3% were postmenopausal with median age of menopause of 49 years (IQR 40–50 years)
					• 22% had early menopause (40–45 years)
					• 12% had premature menopause (<40 years)
					Earlier onset of menopause associated with:
					• African–American ethnicity (HR 8.16)
					• injection drug use (HR 2.46)
					No association with smoking, ART, nadir CD4, or AIDS-defining illness

Abbreviations: HR, hazard ratio; OR, odds ratio; HCV, hepatitis C virus; ART, antiretroviral therapy; FSH, follicle-stimulating hormone; SD, standard deviation; CI, confidence interval; IQR, interquartile range.

Table 3 Summary of studies assessing menopausal symptoms in women with HIV

Authors	Study design	Location	Population	Findings
Clark et al^Citation84	Cross-sectional	USA	52 HIV-positive women ≥40 years with adequate menopausal information; 50% postmenopausal	In HIV-positive menopausal women, higher CD4 count associated with increased prevalence of hot flashes:  23% in those with CD4 <200 vs 54% in those with CD4 >500
Fantry et al^Citation13	Cross-sectional	USA	120 HIV-positive women ≥40 years of age; 25% postmenopausal	Postmenopausal HIV-positive woman had higher rates of:  Hot flashes (86.7%)  Vaginal dryness (53.3%) Menopausal status was associated with development of hot flashes (OR 4.2)
Miller et al^Citation94	Cross-sectional	USA	289 HIV-positive and 247 HIV-negative women	96% of all women had at least 1 menopausal symptom  88.6% had psychological symptoms  61% had vasomotor symptoms HIV infection independently associated with increased symptoms (OR 1.24)
Ferreira et al^Citation80	Cross-sectional	Brazil	96 HIV-positive and 155 HIV-negative women ≥40 years of age	HIV infection independently associated with menopausal symptoms (OR 1.65) HIV-positive had high prevalence of psychological (97.9%) and vasomotor symptoms (78.1%) No association between menopausal symptoms and CD4 count
Boonyanurak et al^Citation82	Cross-sectional	Thailand	268 HIV-positive women ≥40 years of age; 20.5% women postmenopausal	In HIV-positive women, menopausal status was associated with:    Night sweats (P=0.03)  Change in sexual desire (P=0.01) versus general Thai population, HIV-positive more likely to have:  Hot flashes (47% vs 37%)  Night sweats (48% vs 21%)
Looby et al^Citation97	Cross-sectional	USA	33 HIV-positive women and 33 HIV-negative women between ages of 45–52 years	HIV-positive women had greater severity of hot flashes compared to HIV-negative women (P=0.03) and greater severity of menopausal symptoms (P=0.008) HIV-positive women also had more:  Sleep difficulties (P=0.04)  Depression (P<0.05)  Irritability (P<0.05) Anxiety (P<0.05) In HIV-positive women, severity of hot flashes did not correlate with CD4 count or duration of HIV infection
Johnson et al^Citation98	Cross-sectional	USA	150 HIV-positive women and 128 HIV-negative women	No difference in prevalence of hot flashes or vaginal dryness based on HIV status HIV-positive women were less likely to know the etiology of their hot flashes or vaginal dryness
Lui-Filho et al^Citation27	Cross-sectional	Brazil	273 HIV-positive and 264 HIV-negative women aged 40–60 years of age	HIV sero-status not associated with menopausal symptoms (either vasomotor or psychological symptoms) Hot flashes and vaginal dryness more likely to occur in women who were perimenopausal or postmenopausal
Maki et al^Citation102	Cross-sectional evaluation of data collected from the prospective Women’s Interagency Health Study (WIHS)	USA	835 HIV-positive and 335 HIV-negative women aged 30–65 years	Prevalence of depressive symptoms did not differ between HIV-positive and HIV-negative women Depressive symptoms did vary with stage of menopause (33% in premenopausal, 47% in early perimenopausal, 42% in late perimenopausal, and 43% in postmenopausal)  Early perimenopausal status had higher risk of depression (OR 1.92 in HIV-positive women) Among HIV-positive women:  Increased depression if CD4 <200 (OR 2.14)  Less depression when adherent to ART (OR 0.67)
Rubin et al^Citation99	Cross-sectional	USA	708 HIV-positive and 278 HIV-negative women aged 30–65 years	No difference in menopausal symptoms between HIV-positive and HIV-negative women (trend to HIV-positive having more sleep disturbances than HIV-negative [P=0.07]) Early perimenopausal women more likely to report depressive symptoms than premenopausal (OR 1.84); postmenopausal women more likely to report sleep disturbances than premenpausal (OR 1.83) HIV-positive women had worse outcomes on tests of cognitive function, but this was not associated with menopausal status; those with depression and/or anxiety also had poorer cognitive function
Sorlini et al^Citation107	Cross-sectional	Italy	20 HIV-positive and 21 HIV-negative women ≥65 years	No difference in depression between HIV-positive and HIV-negative women Among HIV-positive women, depression was associated with having a CD4 count <500 (P=0.02) A greater proportion of HIV-positive women than HIV-negative women had pathological scores on neuropsychological testing

Abbreviations: OR, odds ratio; ART, antiretroviral therapy.

Table 4 Summary of studies assessing bone mineral density (BMD) and osteoporosis in women with HIV and menopause

Authors	Study design	Location	Population	Findings
Yin et al^Citation144	Cross-sectional	USA	31 HIV-positive postmenopausal women compared to 186 historical-matched (age, ethnicity) HIV-negative controls	Mean BMD lower in HIV-positive group vs controls
				Prevalence of osteoporosis 42% (vs 23%) at lumbar spine (P=0.003)
				Prevalence of osteoporosis 10% (vs 1%) at total hip (P=0.003)
				Correlates of low BMD were:
				Years since menopause (P=0.02)
				Lowest weight (P=0.001)
				No association with duration of HIV infection, ART, CD4 count
Arnsten et al^Citation133	Cross-sectional	USA	263 HIV-positive and 232 HIV-negative women ≥40 years of age	HIV-positive women had lower BMD at femoral neck (P=0.001) and lumbar spine (P=0.04) vs HIV-negative women
				HIV was an independent predictor of low BMD (especially in non-Black women)
				CD4 count, ART and use of PIs not associated with low BMD
Anastos et al^Citation155	Cross-sectional	USA	274 HIV-positive and 152 HIV-negative women	Prevalence of low BMD was higher in ART-naïve HIV-positive women compared to HIV-negative women (OR 4.36), indicating an independent association with HIV infection
				Prevalence of low BMD higher in women receiving PI-therapy (OR 3.72) compared to HIV-negative women
				PI-based ART associated with lower BMD than non-PI-ART (P=0.014)
				Longer lopinavir use correlated with lower BMD (P=0.006) and longer efavirenz use associated with higher BMD (P=0.004)
Yin et al^Citation132	Cross-sectional analysis of data from a prospective cohort study	USA	92 HIV-positive and 95 HIV-negative women ≥40 years of age who were postmenopausal and not on hormone therapy	HIV-positive women were more likely to have low BMD at lumbar spine, femoral neck and total hip
				BMD was 5.9% lower in HIV-positive vs HIV-negative women at the total hip
				HIV was an independent predictor of BMD at the lumbar spine and total hip
				No difference between HIV-positive and HIV-negative for fragility fractures
				No difference by ART status
Yin et al^Citation140	Cross-sectional analysis of data from a prospective cohort study	USA	92 HIV-positive and 95 HIV-negative women ≥40 years of age who were postmenopausal and not on hormone therapy	HIV-positive women had increased bone turnover markers compared to HIV-negative women
				No difference between:
				ART vs no ART
				Ritonavir vs no ritonavir in ART regimen
				Greater induction of peripheral blood mononuclear cells into osteoclast-like cells when exposed to autologous HIV-positive serum (vs HIV-negative) and serum containing ritonavir (vs non-ritonavir-based ART)
Pinto Neto et al^Citation141	Cross-sectional	Brazil	300 HIV-positive patients with median age 46 years (57.7% male and 42.3% female)	Low BMD in 54.7% of patients (95% CI 49.1%–60.3%)
				Independent predictors of low BMD were:
				BMI <25 kg/m^2 (OR 2.9)
				Menopause (OR 13.4)
				Undetectable viral load (OR 7.9)
				Zidovudine use (OR 0.2) and nevirapine use (OR 0.1) were protective against low BMD
Sharma et al^Citation145	Longitudinal	USA	245 HIV-positive and 219 HIV-negative women	HIV-positive women had lower baseline BMD at femoral neck (P=0.02) and total hip (P<0.01) than HIV-negative women, but there was no difference in prevalence of osteoporosis between HIV-positive and HIV-negative women
				No difference between HIV-positive and HIV-negative women in rate of BMD decline over time
				Also no difference in BMD decline between:
				Tenofovir vs no tenofovir use
				PI vs no-PI use
				In multivariate analysis, menopause and chronic HCV infection associated with greater decline in BMD
Gomes et al^Citation120	Cross-sectional	Brazil	273 HIV-positive women aged 40–60 years; 206/273 answered questions related to study	33.5% had low BMD at lumbar spine and 33.1% at femoral neck
				Low BMD at lumbar spine and femoral neck associated with:
				Age >50 years (P<0.01 at LS and FN)
				Menopause (P<0.01 at LS and FN)
				Increased FSH >40 mIU/mL (P<0.001 at LS and P<0.01 at FN)
				Menopause associated with 23-fold increased risk of low BMD at lumbar spine (P<0.01) and 57-fold increased risk of low BMD at femoral neck (P<0.01)
				No association between low BMD and smoking, alcohol, nadir CD4 count, viral load, tenofovir use, protease inhibitors, or duration of HIV infection
Dravid et al^Citation147	Cross-sectional	India	536 HIV-positive patients (66% men and 34% women) with median age 42 years	In ART-naïve patients:
				67% had low BMD and 29.6% had osteoporosis
				In ART-experienced patients:
				80.4% had low BMD and 36.6% had osteoporosis
				Low BMD associated with:
				Increased age (P<0.001)
				Reduced BMI (P<0.001)
				Smoking (P=0.05)
				Menopause (P=0.03)
Prior et al^Citation146	Case-control	Canada	138 HIV-positive women and 402 HIV-negative controls matched for age and geographic region	HIV-positive women more likely to have other osteoporosis risk factors such as smoking, menstrual irregularity, weight loss, glucocorticoid use
				No difference in BMD between HIV-positive and HIV-negative women
				HIV-positive cases had higher rates of lifetime fragility fractures compared to HIV-negative controls (26.1% vs 17.7%, OR 1.7); however, HIV status itself not associated with fracture in multivariable analysis when other osteoporosis risk factors taken into account
Yin et al^Citation149	Prospective cohort study – Women’s Interagency Health Study (WIHS)	USA	1,728 HIV-positive and 663 HIV-negative women followed for median 5.4 years	One-third of new fractures were fragility fractures
				No difference between HIV-positive and HIV-negative women in history of self-reported fracture
				In multivariate analysis, new fracture was associated with older age, white race, HCV infection, and increased creatinine, but not HIV status
				In HIV-positive patients, older age, white race, smoking, and history of ADI were associated with new fracture, while NNRTIs were slightly protective (OR 0.92); there was no association with ART, CD4 count or cumulative tenofovir exposure

Abbreviations: ART, antiretroviral therapy; BMI, body mass index; PI, protease inhibitor; HCV, hepatitis C virus; IDU, injection drug use; FSH, follicle-stimulating hormone; OR, odds ratio; BMD, bone mineral density; CI, confidence interval; LS, lumbar spine; FN, femoral neck; ADI, AIDS-defining illness; NNRTI, non-nucleoside reverse transcriptase inhibitor.

Table 5 Guidelines for assessment of BMD in patients with HIV

Source and location	Year of publication	Recommendations for screening
Brown et al. Recommendations for evaluation and management of bone disease in HIV. Clin Infect Dis.^Citation131 [USA]^a	2015	It is appropriate to assess all HIV-positive patients for risk of low BMD and fragility fracture
		All patients >50 years of age should have height assessment every 1–2 years
		BMD assessment with DEXA-scan is recommended for:
		All patients who have a major risk factor for osteoporosis
		Postmenopausal women
		Men ≥50 years of age
		Previous fragility fracture
		Glucocorticoid use at dose ≥ equivalent of prednisone 5 mg/day for >3 months
		High falls risk
		All other patients should be assessed for osteoporosis risk based on age-specific recommendations:
		Assessment with comprehensive clinical tool (such as the FRAX^b) is suggested for:
		Premenopausal women >40 years of age
		Men 40–49 years of age
		Some experts suggest those with HIV should be considered to have a secondary cause of osteoporosis when utilizing the FRAX tool
		Those who have an intermediate to high risk of fracture on FRAX should go on to have DEXA scan
		No screening required for those <40 years of age unless other risk factors (as mentioned earlier) are present
Aberg et al. Infectious Diseases Society of America. Primary care guidelines for the management of persons infected with HIV: 2013 update by the HIV Medicine Association of the Infectious Diseases Society of America. Clin Infect Dis.^Citation121 [USA]	2013	Baseline bone densitometry (DEXA) screening is recommended for:
		Postmenopausal women
		Men ≥50 years of age
Asboe et al. British HIV Association guidelines for the routine investigation and monitoring of adult HIV-1-infected individuals, 2011. HIV Med.^Citation180 [UK]	2011	Assess patients for risk factors for reduced BMD (eg, with FRAX) at:
		Initial HIV diagnosis
		Prior to initiation of ART
		Reassess these risk factors every 3 years when on ART and for those ≥50 years of age
		BMD assessment (usually with DEXA) should be performed for:
		Men ≥70 years of age
		Women ≥65 years of age
		Consider DEXA in men and women ≥50 years of age if intermediate to high risk FRAX or other risk factorsc
European AIDS Clinical Society. EACS Guidelines Version 7.1. EACS; 2014.^Citation181 [Europe]	2014	Consider all patients for classic risk factorsd for osteoporosis
		Measure 25(OH) vitamin D in all persons at presentation
		Consider DEXA for patients with ≥1 of the following (preferably before ART initiation):
		Postmenopausal women
		Men ≥50 years of age
		History of low-impact fracture
		High falls riske
		Clinical hypogonadism
		Oral glucocorticoid use at dose ≥ equivalent of prednisone 5 mg/day for >3 months
		Assess effect of risk factors by including DEXA results into FRAX
		Do not use for those <40 years of age
		Consider using HIV as a cause of secondary osteoporosis

Notes:

a Reproduced from Brown TT, Hoy J, Borderi M, et al. Recommendations for evaluation and management of bone disease in HIV. Clin Infect Dis. 2015;60(8):1242–1251,¹³¹ by permission of Oxford University Press. Copyright ©2015.

b FRAX: World Health Organization Fracture Risk Assessment Tool: https://www.shef.ac.uk/FRAX/tool.jsp; Use country-specific FRAX algorithm; consider checking off box for “secondary osteoporosis” in patients with HIV (expert opinion).¹³¹

c Additional risk factors include HIV or related risk factors, such as increased duration of HIV infection, low nadir CD4 count and hepatitis virus co-infection.

d Classic risk factors include older age, female sex, hypogonadism, family history of hip fracture, low BMI (<19 kg/m²), vitamin D deficiency, smoking, physical inactivity, history of low-impact fracture, alcohol excess, steroid exposure (equivalent to ≥5 mg prednisone per day for >3 months).

e Using Falls Risk Assessment Tool: www.health.vic.gov.au/agedcare/maintaining/falls/downloads/ph_frat.pdf.

Abbreviations: ART, antiretroviral therapy; DEXA, dual-energy X-ray absorptiometry; FRAX, Fracture Risk Assessment Tool; BMD, bone mineral density; BMI, body mass index.

Table 6 Interpretation of fracture risk assessment and DEXA scores in assessment of bone disease

Source	Result	Interpretation
Risk of Fracturea	≤10% risk of major osteoporotic fracture in 10 years	Low risk
	10%–20% risk of major osteoporotic fracture in 10 years	Moderate risk
	≥20% risk of major osteoporotic fracture in 10 years and/or ≥3% risk of hip fracture	High risk
DEXA scanb	T-score. −1.0	Within normal limits
	T-score ≤−1.0 but. −2.5	Osteopenia
	T-score ≤−2.5	Osteoporosis

Notes:

a Based on a validated clinical tool such as the FRAX¹⁸² or the Canadian Association of Radiologists and Osteoporosis Canada (CAROC) tool.¹²³

b Use T-scores for postmenopausal women and men aged ≥50 years; use z scores for patients aged <50 years; based on the femoral neck score.¹²⁴ Reproduced from Brown TT, Hoy J, Borderi M, et al. Recommendations for evaluation and management of bone disease in HIV. Clin Infect Dis. 2015;60(8):1242–1251,¹³¹ by permission of Oxford University Press. Copyright ©2015.

Abbreviations: FRAX, Fracture Risk Assessment Tool; DEXA, dual-energy X-ray absorptiometry.

Table 7 2015 Guidelines for management of bone disease in patients with HIV

Source	Year of publication	Patient population	Recommendation for repeat screening	Recommendations for management
Brown et al. Recommendations for evaluation and management of bone disease in HIV. Clin Infect Dis.^Citation131	2015	Patients younger than 40 years	No routine screening suggested; assess when develop major risk factor or become >40 years of age	All patients:  Adequate calcium intake  Adequate vitamin levels and supplementation if requiredb  Lifestyle modifications   Smoking and alcohol cessation   Falls prevention   Exercise
		Patients aged 40–50 years with a low 10-year fracture risk based on FRAX (no DEXA required)	Monitor FRAX every 2–3 years
		Patients with moderate 10-year fracture risk:  FRAX ≥10% but <20%  Lowest T-score >−2.5  No history of hip or vertebral fracture	Repeat DEXA in 1–2 years if advanced osteopenia (T-score between −2.00 and −2.49) Repeat DEXA in 5 years if mild osteopenia (T-score between −1.00 and −1.99)
		Patients with clinical osteoporosis:  Patients with high 10-year fracture riska  T-score <2.5 at FN, TH or LS on DEXA scan  Previous hip or vertebral fracture	Repeat DEXA in 2 years	Exclude secondary causes of osteoporosisc Treat osteoporosis as per general population:  Bisphosphonates first-line therapy (alendronate or zoledronic acid preferred)  Review therapy at 3–5 years Consider avoiding TDF or boosted PIs if low BMD or osteoporosis (but benefits of ART outweigh risks)

Notes:

a ≥20% risk of major osteoporotic fracture in 10 years and/or ≥3% risk of hip fracture (with or without incorporation of BMD result); based on validated clinical tool such as the FRAX.

b Check vitamin D levels in those with low BMD or previous fracture or risk factors for vitamin D deficiency (dark skin, sun avoidance, malabsorption, obesity, chronic kidney disease, or on treatment with efavirenz); supplemental vitamin D if deficient and target level >30 μg/L.

c Secondary causes of osteoporosis include: type 1 diabetes mellitus, osteogenesis imperfecta in adults, untreated long-standing hyperthyroidism, hypogonadism, or premature menopause (<45 years), chronic malnutrition, malabsorption, and chronic liver disease. Reproduced from Brown TT, Hoy J, Borderi M, et al. Recommendations for evaluation and management of bone disease in HIV. Clin Infect Dis. 2015;60(8):1242–1251,¹³¹ by permission of Oxford University Press. Copyright ©2015.

Abbreviations: BMD, bone mineral density; ART, antiretroviral therapy; PIs, protease inhibitors; TDF, tenofovir disoproxil fumarate (Viread^®); FN, femoral neck; TH, total hip; LS, lumbar spine; FRAX, Fracture Risk Assessment Tool; DEXA, dual-energy X-ray absorptiometry.

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