Introduction

Religion and spirituality are important to HIV-infected patients. In a study that evaluated 2266 patients from the HIV Cost and Utilization Study (HCSUS), 85% responded that spirituality was “somewhat” or “very important” to their lives [1]. Sixty-five percent of HIV infected individuals rated the importance of religion similarly. Notably, 72% responded that they “often” or “sometimes” used religion and spirituality when making decisions; and 65% responded that they use religion and spirituality when they confront problems [1]. Religious and spiritual involvement has also been tightly correlated with improved mood, less depressive symptoms, greater well-being, and less self-blame among HIV-infected individuals [2–4].

There is some debate about the operational definitions of spirituality and religion [5, 6]. In the literature, spirituality is defined as an internal, personal, emotional expression of the sacred, and is measured by exploring spiritual well-being, peace, and comfort derived from faith and spiritual connectedness. Religion is defined as an outward formal, institutional expression of the sacred, associated often with a prescribed set of beliefs or dogma. Religiosity is often measured by asking about the importance of religion, belief in God, and frequency of attendance at religious services or other group activities. Religion and spirituality are often tightly correlated, but not always [5, 6].

While religious and spiritual involvement may correlate with improved emotional wellness, an important question remains: Does religious involvement make a difference in HIV clinical outcomes? Several studies have shown that religious involvement is associated with reduced mortality among the general population [7, 8], and those with cardiovascular disease [9]. These studies use attendance at religious services as the measure of religious involvement [7–9]. Religion and spirituality as a construct is more complex than the single variable of religious participation [5, 6]. After adjusting for important potential confounders such as access to antiretroviral treatment, adherence, race, ethnicity and substance use, the association between religion and spirituality with t-cell counts, viral load, mortality, and other clinical outcomes, is unknown. This systemic review of the literature seeks to address this important question.

Methods

Six databases were searched for relevant studies published from 1980 to June 2016 from related fields: medicine (MEDLINE), psychology (PSYCHinfo), nursing (Cumulative Index of Nursing and Allied Health Literature), religion (American Theological Library Association Religion Database), and sociology (Sociological Abstracts), and the Cochrane Central Register of Controlled Clinical Trials. Standard protocol was followed for Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) [10]. Search terms were HIV, religion, spirituality, t-cell, CD4 cell, viral load, disease progression, morbidity, and mortality. Two researchers independently employed these search criteria. The title and abstract of each article were screened for relevancy. Eligible studies included HIV-infected patients. We excluded studies that did not provide information on the association between religion or spirituality and an HIV clinical outcome, such as mortality or CD4 cell counts. We excluded those papers which focused exclusively on complementary and alternative medicine (CAM) as well as mindfulness. We considered CAM outside the scope of this current review. Endnote software was used to manage the files [11].

Results

The electronic search identified 671 studies (Fig. 1). 57 studies were duplicates, leaving 614 studies for consideration. 421 studies were excluded based on screening the abstracts. 128 studies did not address the care of patients with HIV infection. 112 addressed the care of patients with HIV but did not address religiosity or spirituality. 101 were about religion or spirituality and did not address HIV related outcomes. 52 addressed medical complications of HIV. 19 were reviews or opinion pieces. 9 addressed pediatric patients and did not include HIV related outcomes.

Fig. 1
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PRISMA search strategy

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The full text of the remaining 193 papers were reviewed. 178 were excluded. Of these, 101 addressed mental health related issues. 77 addressed complementary medicine and mindfulness practices. The remaining 15 papers were reviewed for inclusion in the study.

Description of Studies

Among the 15 papers (see Table 1), there were six longitudinal studies (40%) [12–17]. Three studies (20%) were case–control [18–20]. The remaining six studies (40%) were cohort studies or convenience samples [21–26]. One study (7%) was conducted outside the United States [20]. Two studies (13%) were conducted prior to the Highly Active Antiretroviral Therapy (HAART) era [25, 26]. The median number of subjects enrolled in each study was 147 with a range of 33–1138. Ten studies (67%) reported a positive association with religion/spirituality and measurable clinical outcomes [12, 13, 15, 16, 18–21, 23, 26]. Two studies were neutral [22, 25]. Two studies (13%) reported a negative correlation between religion/spirituality and biological markers [17, 24]. One study (7%) identified features of religiosity and spirituality that had both negative and positive associations with HIV clinical outcomes [14].

Table 1 Studies evaluating the association between religion/spirituality and HIV-related outcomes
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Most studies used several validated questionnaires, such as the Ironson-Woods Spirituality/Religiousness Index, the Spiritual Well-Being Scale, and the Duke University Religion Index (DUREL) [13, 14, 17–23, 25, 26]. Fitzpatrick et al. [12] used a more general questionnaire about the use and importance of spirituality and prayer. Ironson et al. [15] and Kremer et al. [16] used qualitative interviews and essays to assess religiosity and spirituality. Van Wagoner et al. [24] relied upon demographic information assessing church attendance.

Positive Association Between Religious Involvement, Spirituality, and HIV Clinical Outcomes

Eight studies explicitly evaluated religious involvement and spirituality with HIV viral load and CD4 cell count. Woods et al. evaluated 106 mildly symptomatic HIV+ men who have sex with men (MSM). Religious behavior (e.g. Regular service attendance, prayer, spiritual discussion, religious reading) was associated with higher CD4 cell count. Interestingly, religious coping (e.g. Place trust in God, seeking comfort in religion) was not correlated with biomarkers but was correlated with less depressive symptoms [26]. Ironson et al. enrolled 100 people in a longitudinal study that evaluated the changes in spirituality and religiousness after a diagnosis of HIV over a period of 4 years. Her team found that 45% of patients had an increase in religiousness and spirituality after HIV diagnosis. This increase predicted greater preservation of CD4 cells and better control of viral load. Of note, this association remained significant after controlling for demographic variables, initial disease status, psychiatric comorbidity, church attendance, and health behaviors such as drug use [14]. In a cross-sectional study, Dalmida et al. evaluated 129 predominantly African-American HIV-infected women and found that greater religious well-being, spiritual well-being, and existential well-being were associated with higher CD4 cell count, beyond what was explained by demographic variables and medication adherence [21]. The largest cohort evaluated 1138 HIV positive patients with psychiatric illness and substance abuse diagnoses [23]. Higher spirituality was associated with improved adherence to HAART, which in turn correlated with an undetectable viral load [23].

A four year longitudinal study by Ironson et al. evaluated the perception of God among patients with HIV infection. This study uniquely evaluated the quality or character of belief in addition to the intensity of belief or quantity of religious practice. Patients completed the View of God inventory which explores whether patients perceive God as being benevolent and forgiving or harsh, judgmental, and punishing [15]. They found that patients who view God as benevolent had higher CD4 cell count and improved viral load response. These results remained significant after controlling for church attendance, mood, coping strategies, and health behaviors [15].

Marconi et al. evaluated several variables among 158 HIV+ patients in an urban South African clinic. In a multivariate model, not having an active religious faith was independently associated with detectable viral load (>1000 copies) and lower CD4 cell count [20]. Similarly, Trevino et al. [17] evaluated 429 patients and found that spiritual struggle was associated with detectable viral load and more HIV related symptoms. In a longitudinal study, Kremer et al. [16] followed 177 patients over 4 years. The researchers employed directed interviews and patient-written essays to determine patients’ spiritual coping. Qualitative analysis was used to derive common anchoring principles. Positive spiritual coping was defined as using spirituality and religion as a supportive resource. Patient who used spirituality to avoid punishment from God were considered to have negative spiritual coping. Sixty-five percent of patients reported being engaged in positive spiritual coping which was associated with sustained undetectable viral load and higher CD4 cell count [16].

Religious Involvement and Survival

Four studies examined the association between religious involvement and survival. Ironson et al. [18] evaluated “spiritual transformation” among patients with HIV, which they define as when patients regard the sacred as central in their life which involves, “a radical reorganization of one’s identity, meaning, and purpose in life.” Among the 147 patients, 80 experienced spiritual transformation. Those patients who experienced spiritual transformation were 5.35 times more likely to achieve 5 year survival. Additionally, these patients were more likely to achieve an undetectable viral load and also had a higher CD4 cell count [18]. Another study by Ironson et al. [13] compared 79 long-term survivors with 200 age-matched controls using the Ironson-Woods Spirituality/Religiousness Index. Faith in God, religious behavior, increased compassion towards others, increased prayer, and overall sense of peace was associated with long-term survival. In this study, while demographic confounders were controlled for, viral load, CD4 count, and HIV medications were not. 30% of long-term survivors and 50% of the comparison group were not prescribed protease inhibitors. Interestingly, greater spirituality and religiousness was also correlated with lower cortisol levels [13].

In a follow-up longitudinal study of 177 patients with initial CD4 cell counts of 150–500, patients who experienced spiritual reframing, gratitude, empowerment, and overcame spiritual guilt were 2–4 times more likely to survive over a 17 year period [15].

Fitzpatrick et al. evaluated spiritual activities among 901 HIV positive patients at baseline and 1 year follow up. Patients who participated in spiritual activities were at reduced risk of death after adjusting for income, AIDS diagnosis, CD4 count, smoking, alcohol use, and substance abuse. Even those not receiving antiretroviral therapy were at reduced risk of death (Hazard Ratio 0.4, 95% CI 0.2–0.9) compared to those who did not practice spirituality [12].

Neutral Association Between Religion and HIV Clinical Outcomes

Two studies showed a neutral or equivocal outcome. Ramer et al. studied spirituality and self-transcendence using Reed’s Self-Transcendence Scale and the Spirituality subscale of the Ferrans and Powers Quality of Life Index among a convenience sample of 420 HIV/AIDS patients [20, 27, 28]. They found that self-transcendence was associated with improved energy (p < .05) and acculturation (p < .05). Spirituality was also associated with improved energy (p < .001) and less pain (p < .02). However, neither spirituality nor self-transcendence was associated with disease progression or severity [18]. A small study by Woods et al. evaluated a convenience sample of 33 African-American women patients and found no association between religious coping and CD4 cell count [24].

Religious and Spiritual Involvement Associated with Worse HIV Clinical Outcomes

Two studies demonstrated an overall negative association between religious involvement and biological outcomes; and one showed both a positive and negative association [14, 17, 24]. A study by Van Wagoner et al. evaluated patients who presented for initial care as a university associated HIV clinic. They found that men who have sex with men (MSM) who also attend church regularly present with a lower t-cell count than those MSM who do not attend church regularly [24]. In a longitudinal study over 12–18 months among 429 patients, Trevino et al. [17] showed that spiritual struggle was associated with a detectable viral load as well as more HIV related symptoms. Similarly, in a 4 year longitudinal study, Ironson et al. [14] showed that a negative view of God (viewing God as harsh or punishing) predicted a faster disease progression.

Discussion

We conducted a systematic review of the English language literature to identify studies evaluating the association between religion, spirituality and HIV clinical outcomes. Of the 15 studies included, 11 demonstrated a positive association between religion, spirituality and HIV clinical outcomes, two were neutral, and two were negative, and one showed both positive and negative associations (Table 1). These studies showed that religious involvement and spirituality were associated with an increased CD4 cell count, decreased viral loads, and decreased mortality (Table 1).

While several studies suggest that religious involvement and heightened spirituality have a positive correlation with HIV biological outcomes, there are several provocative questions that arise. For instance, Dalmida et al. have proposed that the positive correlation between HIV outcomes and spirituality may be particularly important among ethnic minorities and the poor where there may be few other coping resources [15]. However, several studies demonstrate a positive association between religious and spiritual involvement and HIV biomarkers even after controlling for socio-demographic variables (Table 1).

Further, religion may be a particularly complex variable among the MSM community where the studies did not reveal a clear pattern. Van Wagoner et al. [22] demonstrate that church-going MSM present later in their disease with a lower CD4 cell count. However, Woods et al. [25] found that church attendance among gay men was associated with a higher CD4 cell count. These disparate findings may be due to the differences in the demographics of the study population, the type of churches patients attended, the regional differences in religious culture. Church culture and support for MSM activity likely varies widely across denominations and specific congregations and may impact the experience of organized religion by MSM. For instance, Woods et al. speculate that many religious organizations regard homosexual activity as against social norms. This may influence the willingness of HIV-infected individuals to seek screening or further care. Denial of HIV risk among churchgoing MSM may also play a role. The authors also acknowledge that reverse causality may play a role: sick patients may begin attending religious services more frequently. However, in the cohort reported on by Woods et al. [25], patients had a relatively recent diagnosis and had well-established religious practices.

What these studies do suggest is that a constellation of variables hang together: poor social support, spiritual struggle, low-self esteem, poor quality of life, more HIV related symptoms, and worse virologic control. This suggests the need for adjustment for these variables, using state of the art techniques such as propensity score matching, in studies evaluating the association between religion, spirituality and HIV outcomes. They also suggest that interventions will need to take a coordinated approach to the patient’s well-being in which each of these issues are addressed. Viral control—a biological marker—cannot be separated from the patient’s spiritual well-being, psychological symptoms, and social support.

And yet, addressing religion and spirituality in HIV-infected patients can be particularly challenging. Some patients may feel shame or guilt in their HIV status [24]. Some religious traditions are overtly hostile or judgmental to people with HIV [24].

Limitations to the literature and this systematic review are to be considered. First, most of the studies were small, enrolling between 100 and 200 people and focused on the populations of specific clinics in resourced settings. This may affect the generalizability of our findings. Further, only six studies were longitudinal. The constructs of spirituality and religious involvement can evolve over time and therefore have a variable influence upon health. Second, there is the potential of publication bias: studies with a positive association are more likely to be published. Third, the study of the association of HIV and spirituality has primarily been conducted by a relatively small group of researchers. These studies are robust and of high quality—including the most recent 17-year longitudinal study of 177 patients [17]. And yet, different perspectives may lead to new understanding of this important association.

An important consideration in evaluating questions of religion and spiritual belief is the question of causality. The cross-sectional nature of most of this research prevents the evaluation of potential cause and effect relationships. Does HIV infection, like any serious illness, lead to spiritual questioning or doubt? Or rather, does it spur individuals to seek spiritual solace and strength? The question is, of course, which comes first? Does the spiritual struggle of a significant disease cause the depression or vice versa? Does a patient’s poor social support lead to the depression and low-self esteem? Another consideration is the use of validated instruments for religion and spirituality. Spiritual struggle and depression may, in fact, be measuring the same emotional construct and simply applying two different labels, a spiritual label and a psychological one [5, 6].

Conclusion

Providers who care for patients with HIV infection should be aware of a patient’s spirituality and religious involvement and may want to encourage it as a source of solace and meaning. However, as Ironson’s paper suggests: the quality of one’s belief can impact CD4 count and viral load [15]. Depending upon the patient’s specific beliefs, spirituality and religious involvement may have positive or negative effects for patients living with HIV. Regarding God as harsh and punishing can have harmful effects such as faster disease progression compared with those who viewed God as benevolent and forgiving. Blanket encouragement or discouragement of religious beliefs may be ill advised. Instead, providers should seek to understand the role spirituality and religion plays in their patient’s life and respond in a more nuanced manner. Additional research should investigate the longitudinal relationships between religion, spirituality and HIV outcomes with better adjustment for confounding factors. These data may offer additional support for a possible intervention study designed to increase the engagement in religious and spiritual endeavors among HIV-infected patients.