Layers of Loss: A Scoping Review and Taxonomy of HD Caregivers’ Spiritual Suffering, Grief/Loss and Coping Strategies

Abstract

Context.

Huntington’s disease (HD), an incurable, multi-generational, autosomal dominant disorder, creating unique challenges and a myriad of spiritually-related stressors in those affected and their familial caregivers. Spiritual suffering, experiences of grief/loss, and coping strategies have not been systematically studied in HD caregivers.

Objectives.

To comprehensively define spiritual suffering, grief/loss, and coping strategies used by HD caregivers.

Methods.

A PRISMA-ScR scoping literature review was conducted. Data from included research articles were organized thematically using induction and open coding. A grounded, deductive approach was used to delineate a demarcated taxonomy of themes, which encompasses all three over-arching domains. Four reviewers, employing a modified Delphi approach, ascertained which themes were demonstrated by research participants in each study.

Results.

36 of 583 articles met the review criteria; none were published in the palliative care literature. Investigations primarily focused on intrapersonal (self-image) distress and existential angst; only rarely looked deeper into divine/transpersonal suffering, disrupted religious relationships, or meaning distress. HD caregivers experience profound grief/loss, expressed as disenfranchised grief that is associated with the ambiguous loss of their loved one, loss of family structure, social connectedness, and personal losses. Half of the studies reported maladaptive HD caregiver coping strategies—characterized by dysfunctional escape schemes; in contrast, transcendent/creative strategies were often unexplored.

Conclusion.

HD caregivers experience prolonged grief and other forms of spiritual suffering as they progressively lose their loved ones and disruption to their own lives. With an improved assessment tool, teams with spiritual and palliative care experts will better be able to support HD family caregivers.

Introduction

Huntington’s disease (HD) is an incurable, autosomal dominant neurodegenerative disorder; which slowly strips away a patient’s independence, demarcated by cognitive, psychiatric, and executive decline, behavioral and personality changes, affective problems as well as crippling motor impairments.^1–3 Moreover, HD presents with a painfully long decline, which eventually leads to a patient’s death over 20 years after diagnosis and 35 years after symptom onset.⁴ While many neurodegenerative disorders present in old age, HD typically presents in patients’ 30s and 40s when careers are developing and family concerns are paramount. Given the young age of onset, the hereditary risk to offspring of 50%,^1–3 and the prolonged disease course, HD presents a unique challenge to patients, families, and clinical care teams alike.^5–7 HD familial care partners often experience prolonged emotional distress and caregiver burden as the disease slowly robs them of their loved ones.^8–10 The very nature of the continuous caregiver experience of progressive loss in HD, where their loved one does not die for many years,¹¹ generates a context for chronic grief¹² or prolonged grief disorder.¹³ Studies show high rates of depression, anxiety, and other psychotic symptoms among care partners.^14,15 Some HD patients even begin manifesting the disease as children.^16,17 Not surprisingly, studies have demonstrated high rates of family dysfunction, adverse parenting, abuse, and stark impacts on all members of a family coping with HD.⁷ This continuous trauma experienced by HD care partners has detrimental effects on caregivers who often struggle to maintain their sense of self;^8,10 one seminal article infers that HD “partners have at least as much psychological distress as [patients], but partners have the tendency to draw back.”⁹ Furthermore, they observe that “the grief of [patients’] partners is often ‘disenfranchised’, or not socially recognized, as if they have no right to mourn.”⁹ Thus, in addition to all the physical and practical burdens of caregiving in HD, family members must personally deal with overwhelming psycho-socio-spiritual stressors.

Despite excellent primary palliative care provision by neurology teams^18–20 and the support of multiple national advocacy organizations,^21,22 we hypothesize that significant gaps remain—both in the knowledge of the breadth of HD caregiver suffering and in how other providers might help. Managing these gaps could potentially be addressed by palliative care (PC) experts; unfortunately, there is limited data on the role of PC in these caregivers. PC involvement rates with HD patients and their caregivers have been reported as low as 4%, even when they are at the end of their lives.²³ In addition, spirituality and spiritual concerns are ignored by the instruments usually used to measure caregiver quality of life (as well as by most non-palliative clinicians in family conferences),²⁴ and yet spirituality as a source of support and/or suffering is ubiquitously experienced by patients with devastating serious illnesses.^25,26 Public and medical awareness of HD, including understanding the experiences, burdens, and suffering of families is wanting. This lack of understanding extends to the PC community. We aim to evaluate the current state of HD caregivers’ emotional and spiritual suffering by asking: “what is known about the spiritual suffering, grief, and coping strategies for caregivers of HD patients?” We hope to provide a framework for palliative care and spiritual support experts to better address and support caregivers of HD patients over the unrelenting disease course of HD.

Methods

This scoping review was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses for Scoping Reviews (PRISMA-ScR) guidelines.²⁷

Eligibility Criteria

Only original research studies were eligible, all years were included. Quantitative, qualitative, and mixed-method studies were allowed. Exclusion criteria comprised review articles, studies for tool validation, single case reports (multiple patient case series are included), and articles not available in English (Table 1).

Table 1.

Study Eligibility Criteria

Research question: What is known about the spiritual suffering, grief, and coping strategies for caregivers of patients with Huntington’s disease? Literature Search: “Huntington’s Disease” AND “caregiver” AND “suffering” / “grief / “coping” and synonyms

Inclusion Criteria: Original research studies on caregivers of patients with Huntington’s disease All publication years up through July 2020 Study design can include: Quantitative, Qualitative, Mixed-Method, and Other relevant observational studies

Exclusion Criteria: Research articles not studying caregivers Studies developing or validating assessment tools Review articles Single case reports Commentaries and opinion articles Studies with goals or outcomes outside our study aim and question Articles not published in English

Search Strategy

The literature search strategy was developed with the input of a research librarian. The databases PubMed, CINAHL, EMBASE, and PsycINFO were searched using the following keywords and their synonyms: “Huntington’s Disease,” “caregiver” and “suffering” / “grief” / “coping” (Table 2).

Table 2. Literature Search Strategy.

We performed a literature search and consulted with a research librarian. The databases PubMed, CINAHL, EMBASE and PsycINFO were searched using the following keywords and their synonyms: “Huntington’s Disease” AND “caregiver” AND “suffering” / “grief” / “coping”. The following number of potential articles were identified with the corresponding search strategies:

PubMed: 268 articles	CINAHL: 105 articles EMBASE: 143 articles PsycINFO: 180 articles
Huntington Disease [MeSH] OR “Huntington Disease”[tiab] OR “Huntington’s Disease” [tiab] OR “Huntington Chorea” [tiab] OR “Chronic Progressive Hereditary Chorea” [tiab] OR “Huntington’s Chorea” [tiab] OR “Late-Onset Huntington Disease” [tiab] OR “Late Onset Huntington Disease” [tiab] OR “Juvenile Huntington Disease” [tiab] OR “Juvenile-Onset Huntington Disease” [tiab] OR “Juvenile Onset Huntington Disease” [tiab]	“Huntington Disease” OR “Huntington’s Disease” OR “Huntington Chorea” OR “Chronic Progressive Hereditary Chorea” OR “Huntington’s Chorea” OR “Late-Onset Huntington Disease”OR “Late Onset Huntington Disease”OR “Juvenile Huntington Disease”OR “Juvenile-Onset Huntington Disease” OR “Juvenile Onset Huntington Disease”
Caregivers [MeSH] OR Caregivers [tiab] OR Caregiver [tiab] OR Caregiving [tiab] OR Family [tiab] OR Spouse [tiab] OR Carer [tiab] OR partner [tiab] OR relative [tiab] OR offspring [tiab] OR dependent [tiab] OR wife [tiab] OR husband [tiab]	Caregivers OR Caregiver OR Caregiving OR Family OR Spouse OR Carer OR partner OR relative OR offspring OR dependent OR wife OR husband
“Existential suffering” [tiab] OR “existential distress” [tiab] OR “existential pain” [tiab] OR faith [tiab] OR “spiritual belief” [tiab] OR “religious belief” [tiab] “Stress, Psychological”[Mesh] OR Depression [mesh] OR Quality of Life [mesh] OR Anxiety [mesh] OR Emotions [mesh] OR shame [tiab] OR guilt [tiab] OR distress [tiab] OR anger [tiab] OR grief [tiab] OR Bereavement [tiab] OR Fear [mesh] OR Fear [tiab] OR Fears [tiab] OR Spirituality [tiab] OR religion [tiab] OR God [tiab] Adaptation, Psychological [mesh] OR “Psychological Adaptation” [tiab] OR “Psychological Adaptation” [tiab] OR “Coping Behavior” [tiab] OR “Coping Behaviors” [tiab] OR “Coping Skills” [tiab] OR “Coping Skill” [tiab] OR coping [tiab] OR “Adaptive Behavior” [tiab] OR “Adaptive Behaviors” OR well-being [tiab] OR distress [tiab] OR Suffering [tiab]	“Existential suffering” OR “existential distress” OR “existential pain” OR faith OR “spiritual belief” OR “religious belief” OR “Stress, Psychological” OR Depression OR Quality of Life OR Anxiety OR Emotions OR shame OR guilt OR distress OR anger OR grief OR Bereavement OR Fear OR Spirituality OR religion OR God OR Adaptation, Psychological OR “Psychological Adaptation” OR “Psychological Adaptation” OR “Coping Behavior” OR “Coping Behaviors” OR “Coping Skills” OR “Coping Skill” OR coping OR “Adaptive Behavior” OR “Adaptive Behaviors” OR well-being OR distress OR Suffering

Study Selection

The initial literature search identified 575 unique articles. Eight studies, which were not uncovered by the initial search, but thought to possibly meet the research objectives were hand-picked by the authors and added. The title and abstract of each initially identified article were screened for relevance by one reviewer (B.L.). 484 studies that met exclusion criteria or were deemed unrelated to our research objectives were removed. The remaining 99 research articles were then read in full by two reviewers (B.L. and B.M.) to assess eligibility and to ensure that the study design could demonstrate at least one of the initial themes in our review. 36 articles were deemed suitable for the final group qualitative analysis (Fig. 1).

Fig. 1.

PRISMA-ScR Flow Diagram

Thematic Induction and Taxonomy Synthesis

Thematic synthesis, the process of identifying both initial inductive descriptive and final distinct deductive analytical themes for the literature review, was conducted with a modification of Thomas and Harden’s three-step methodology.^28,29 Because we aimed to clearly delineate and define themes from a broad array of fields (including religion, spirituality, chaplaincy, psychology, mental health, grief, coping, and palliative medicine) and since these themes have been described variably by different disciplines, and furthermore, overlap in complex ways, we were concerned that initial open coding of the research studies might be overwhelming. Rather than begin with open coding, literature-based descriptive themes were initially induced to encompass all three over-arching caregiver domains: spiritual suffering, grief/loss, and coping. Similar modifications in the qualitative thematic analysis have been shown to provide structure and consistency, achieving evaluation goals without a loss of scientific rigor.³⁰ The domains we induced were spiritual suffering, grief/loss, and coping, each from literature subsets that may address or at least touch on other domains, but come from distinct perspectives. The coping domain was initially split between maladaptive and adaptive strategies, with the latter differentiating emotional management from problem-solving.³¹ Transcendent / creative coping was added during first-pass open coding when coping mechanisms that went beyond the first two were discovered; this addition was supported by the literature.^32–34 Initial induction of the 5 themes within the spiritual suffering domain was based on pertinent literature^35–41 and spiritual suffering assessment tools, as described below.^42–46 Because of the overlap between religion and spirituality, when religious elements were key factors in these social disruptions, they were included as a separate theme within spiritual suffering; when they were not, they were assigned to loss of social connectedness within the grief/loss domain.

Following descriptive thematic induction, using the grounding of those themes, more in-depth deductive coding theme development was begun by all four reviewers (B.L., F.W., D.F-D., and B.M.) with first-pass analysis of 15 of the 36 included research articles. Then, during a multiple-iteration deliberation process by the four reviewers, the similarities and differences within the themes were compared to generate distinct deductive thematic definitions within the taxonomy, ensuring that areas of overlap were minimized and that each final theme was well defined for the final analytical purposes. An additional review for data extraction was performed for articles that demonstrated analytical themes for which the definitions significantly changed.

Initially, descriptive themes were induced, based on medical, psychology, and spirituality literature. We subscribe to Christina Puchalski’s and collaborators’ national and international consensus definition of spirituality as “the dynamic dimension of human life that relates to the way persons experience, express and/or seek meaning, purpose and transcendence, and the way they connect to the moment, to self, to others, to nature, to the significant, and/or sacred.”⁴⁷ Spiritual suffering—also called spiritual distress or spiritual pain—is defined as significant separations from meaning, purpose, connectedness, and transcendence (e.g., hope).^48–50 Connectedness-based spiritual suffering encompasses significant struggles with self, the divine, and others, all of which are distinct.^{36,38,39,42,43,51} For example, patients with advanced cancer under PC in one study commonly experienced spiritual pain intrapersonally or in intra-psychic terms (e.g., suffering with despair, loss, regret), transpersonally or in relation to the divine (e.g., feeling abandoned by God, being without faith and/or a religious/spiritual community), and interpersonally (e.g., feeling unwanted by family members, feeling disconnected from others).³⁸ Existential issues deal with the examination of our existence, with ultimate concerns (or existential suffering sources) that include: finitude/death, isolation/disconnectedness, meaning in life, and freedom (e.g., moral choice).^35,52 Whether the term existential or spiritual is evoked is largely based on one’s theological orientation; with theists and/or religiously-oriented people preferring “spiritual” and atheists who focus on the secular and psychological aspects preferring the term “existential.”^{35,49,53–55} Experts on both sides of this semantic divide agree that to be human is to be spiritual (or existential), so we to use the terms interchangeably. The lines differentiating spiritual/existential suffering from psychological distress are also quite challenging.^56,57 We did not investigate psychological suffering, such as depression or anxiety, rather we ensured that our definitions met spiritual suffering criteria or described grief and loss.

A significant theme within spiritual suffering is meaning distress—as emphasized by Dame Cicely Saunders.⁴⁸ Meaninglessness/nihilism is usually delineated from hopelessness/existential fear.^58–61 Although there is certainly overlap between meaning distress and hopelessness/despair,⁶² we included the latter form of spiritual suffering with existential angst during the thematic synthesis process because they share future orientation. Further, the spiritual struggle inventory literature, in particular, largely demarcates spiritual suffering according to the level of one’s disconnectedness into three subsets: (1) divine or transpersonal disruptions; (2) disrupted religious relationships (interpersonal disconnects); and (3) intra-personal, self-image, or integrity distress.^{36,40,42,43,46,51,63,64} We ultimately expanded self-image spiritual suffering to include significant moral distress, deep regrets, and purposelessness during the synthesis process; while unshakable attacks by evil spirits were incorporated into divine/transpersonal suffering.^40,42,64 We also expanded the existential angst theme to include uncertainty,^65,66 which is a poignant element in family members who can be tested for and may carry the same HD gene as the affected loved one they care for.⁶⁷

Because none of the reviewed studies specifically measured or addressed prolonged grief disorder, we elected to analyze anticipatory grief⁶⁸ and prevalent grief symptoms together. Concentrating on caregivers of patients with neurodegeneration pressed us to define the ambiguous loss of the caregivers’ loved ones’ personhood/identity (leading to disenfranchised grief)^69,70 discretely from other losses, such as losses of family structure, or other social connectedness, and personal losses.

Professional grief supporters most often separate adaptive coping into two themes: healthy emotional management and problem-solving strategies.^71–74 Despite how important global meaning-focused, spiritual or faith-based coping is in neurodegenerative disease caregivers,^71,75 clinicians often ignore such transcendent coping strategies. Thus, we built the creative/transcendent coping theme from religious, spirituality, and palliative care literature. It includes many elements, which are difficult to define, such as peace, self-awareness, self-, and other-forgiveness / grace, acceptance with meaning reconstruction, and gratitude.^{40,41,59–61,71,76–79} Creatively engaging in the present experience or realizing “flow” and embracing aesthetics/art/music amidst spiritual suffering and loss, were also incorporated into this theme.^80–82 Other adaptive coping strategies that help transcend suffering,⁴⁵ many of which were promoted by founding leaders in death/dying and the hospice and PC movement (Elisabeth Kübler-Ross, Cicely Saunders, Balfour Mount), were included in the adaptive transcendent coping definition too, such as mindfulness meditation, reflection, prayer, and hope.^{48,50,83–85} We designated negative and passive spiritual coping strategies^39,40 as maladaptive dysfunctional escapes to differentiate those from the three adaptive coping mechanisms. Whereas anger toward God is associated with depression and bereavement adaptation problems,^86,87 we interpreted it as a collaborative, adaptive form of spiritual struggle,^86,87 since it is “normal” in some faith traditions and can also serve as a pivot point in positive spiritual coping.⁸⁸ We deemed oscillation between transcendent hope and periodic avoidance or “denial” of reality adaptive^79,89 and distinguished it from dysfunctional persistently-avoidant maladaptive escape strategies. Otherwise, the maladaptive coping definition induction was largely built on the antitheses of the three adaptive coping strategies, using tenacious evasion of realities/escape as the central defining element for this theme.⁹⁰

Data Extraction

Coding and deductive thematic data charting was completed by four independent reviewers. Their faith tradition self-identifications are Unitarian Universalist, Humanistic Jew, Catholic, and Mystical Christian / Taoist. Once deductive themes had been clearly defined, each reviewer individually read each article in full and when they believed that at least one clear, substantive demonstration of any individual theme was recorded by at least one participant in each study, they charted that along with page number references and germane comments. Thematic reviews were generated from diverse individual perspectives (a medical student; the Executive Director of HD Reach, a nonprofit organization working to improve the care and quality of life for those affected by HD; an HD neurology specialist; and a PC physician; from the above varied faith traditions), without hierarchy (each reviewer had an equal voice). Themes that were merely alluded to were not counted. We then employed a Group Delphi approach to deliberate on all charting judgment discrepancies (if all 4 reviewers independently believed a theme was demonstrated, no further discussion was undertaken).⁹¹ In order to move from any qualitative dissensus in a pragmatic way to consensus, audio-visual deliberation meetings with all 4 reviewers were held, in every case whenever two reviewers perceived that a theme was demonstrated and two did not. In addition, any solitary dissenter (whether claiming a theme was or was not demonstrated) could plead their case against the other three reviewers when that article was discussed.⁹² Four full group discussions were held, covering theme demonstration in about 9 articles each time. Whenever any discrepancies in theme demonstration occurred, group discussion resolved these to a final consensus.

Other data were also extracted from the research articles, including author(s), title, publication audience and year, country of origin, research design, number of study participants, and research objectives. Selected representative quotes from the research studies for each theme were extracted as well.

Results

Of the 583 unique study articles originally identified, 36 were included in the final thematic analysis. Journal focuses of the examined studies were nursing (8), sociology (7), genetics (6), neuroscience (6), psychology (4), medical (3), quality of life (1), and thanatology (1). None of the included studies were published in journals with a focus on palliative care (Table 3).

Table 3.

Included Study Characteristics

First Author Year Published	Journal Focus (Audience)	Participant Countries	Study Participants (Caregivers)	Number of Participants	Study Design
Anderson 2019165	Neuroscience	USA	Family Members	511	Survey
Aubeeluck 200610	Neuroscience	UK	Spouse / Partner	5	Other
Aubeeluck 201296	Quality of Life	UK	Family Members	47	Focus Groups
Brewer 200816	Psychology	UK	Parent	12	Interviews
Brouwer-DudokdeWit 2002140	Sociology	Netherlands	Unspecified	6	Case Studies
Cox 2012166	Nursing	USA	Unspecified	31	Survey
Dawson 200499	Nursing	Australia	Unspecified	19	Interviews
Decruyenaere 20059	Genetics	Belgium	Dyad	16	Survey
Domaradzki 2016101	Psychology	Poland	Family Members	55	Interviews
Etchegary 2011100	Medical	Canada	Family Members	10	Interviews
Halpin 201293	Thanatology	Canada and USA	Family Members	10	Interviews
Helder 2002131	Psychology	Netherlands	Spouse / Partner	90	Survey
Kavanaugh 2014117	Sociology	USA	Child	40	Survey
Kavanaugh 2017133	Sociology	Canada and USA	Family Members	43	Mixed-method
Keenan 2007118	Genetics	UK	Child	12	Interviews
Kessler 1993114	Genetics	USA	Spouse / Partner	5	Case Studies
Lewit-Mendes 2018119	Neuroscience	North America, Europe, Australasia, Asia	Child	84	Survey
Lowit 200590	Medical	UK	Spouse / Partner	10	Interviews
Mand 2015120	Neuroscience	Australia	Child	8	Interviews
Oliveira 202095	Genetics	Portugal	Family Members	9	Interviews
Oliver 1969143	Medical	UK	Family Members	40	Other
Oosterloo 202017	Neuroscience	Netherlands	Parent	10	Interviews
Roscoe 2009124	Sociology	USA	Family Members	17	Survey
Røthing 2015141	Sociology	Norway	Family Members	15	Interviews
Røthing 2014142	Nursing	Norway	Family Members	15	Interviews
Sherman 2020167	Neuroscience	USA	Family Members	17	Focus Groups
Sobel 200394	Sociology	Canada, USA	Unspecified	55	Interviews
Soltysiak 2007168	Nursing	UK	Unspecified	9	Focus Groups
Sparbel 2008121	Genetics	Canada, USA	Child	32	Focus Groups
Tyler 19835	Sociology	South Wales (UK)	Family Members	76	Other
Vamos 20077	Psychology	Australia	Child	40	Survey
Williams 2000169	Genetics	USA	Unspecified	18	Mixed-method
Williams 2009a122	Nursing	Canada, USA	Child	24	Focus Groups
Williams 2013170	Nursing	USA	Child	44	Survey
Williams 2012171	Nursing	USA, UK	Family Members	227	Survey
Williams 2009b14	Nursing	Canada, USA	Family Members	42	Focus Groups

Study Characteristics

The characteristics of the 36 included studies are summarized in Table 3. The earliest from 1969, and the latest, in 2020. Twenty-four studies were conducted in a single country (8 USA; 8 UK; 2 each from Australia, Netherlands, Norway; 1 each from Portugal, Canada); 7 were conducted in 2 countries (6 Canada and USA, 1 UK and USA); 1 was multinational (North America, Europe, Australia, Asia). Of the 36 included studies, 13 employed interviews, 10 were quantitative survey studies, 6 reported on focus groups, 2 were case studies, 2 used a mixed-method research methodology, and 3 represented other types of studies. A total of 1,704 participants were reported, ranging from 5 to 511 participants per individual study. The average number of participants was 47; the median was 19. In many instances, study participant (caregiver) relationships to the individual suffering from HD were not specified, or only designated as “family member”; when it was stated, caregivers included children (8), spouses/partners (4), and parents (2); one study specifically studied the patient-caregiver dyad.

Comprehensive Taxonomy of Spiritual Suffering, Grief/Loss, and Coping Strategy Themes

The taxonomy is presented in Table 4. The average number of themes demonstrated in each study was 4.6; the median was 5. Two of the 36 studies failed to demonstrate any of the 14 themes; in one article, 13 of the 14 were demonstrated. 21 of the 34 studies that demonstrated one or more themes did not demonstrate a single theme within the spiritual suffering domain, whereas only 4 failed to demonstrate a grief/loss theme (Fig. 2).

Table 4.

Comprehensive Taxonomy of Spiritual Suffering, Grief/Loss, and Coping Strategy Themes

Meaning Distress	Struggling with meaninglessness in life or suffering, nihilism; questioning meaning in life: “Why me?” “What’s the point?”
Divine / Transpersonal Suffering	Divine detachment / alienation. Feeling God has abandoned, is angry at, punishing/judging the patient/caregiver; unshakable attacks by evil spirits. Shattered God Image / world-view; unresolved anger or bitterness toward God. Questioning cosmic justice / fairness, and/or faith / trust relationship with God / the world. Fear of going to Hell.
Existential Angst in Uncertainty	Struggling with uncertainty by experiencing significant angst/dread, hopelessness/despair, and/or intense fear regarding the future. [Hope is a meaning-based feasible-if transcendent-goal, with a pathway and agency. It is not outcome- or event-based]. Grave anxiety associated with genetic testing for an inherited disorder.
Disrupted Religious Relationships (Interpersonal)	Spiritual (meaning-based and purpose-related) and religious (beliefs and practices) tensions and conflicts with family, friends, and faith leaders and communities. Hurt or offended by failures in one’s faith community (e.g., by condemnation for anger at God, exclusion from, gossip about, or failure to openly support one’s struggles without bias).
Self-Image Distress (Intrapersonal)	Struggling with or loss of personal identity / sense of self, personhood, dignity; unstable values and/or feeling of purpose in life, beliefs and faith practices. Guilt/shame, self-blame, deep regrets; moral distress in caregiving vs. other roles; helplessly witnessing undue suffering in their loved one. Biopsychosociospiritual trauma / violence / abuse wounds.
Grief Symptoms	Explicit: (1) anticipatory grief; and/or (2) symptoms, including overshadowing sadness and/or anger/irritability, numbness, decreased concentration, preoccupation, helplessness; sleep, appetite and functional disturbances.
Ambiguous Loss of Loved One	The ambiguous loss of the patient’s / loved one’s personhood / identity (typically physical presence with cognitive, affective, and/or behavioral decline) leading to disenfranchised grief (wherein the loss cannot be openly acknowledged, socially sanctioned or publicly mourned). Along with other symptoms, spousal caregivers may feel trapped and say, “This is not the person I married” and/or ruminate about their loved one before…
Loss of Family Structure	Loss of family structure / cohesion, fractured previously-intimate family relationships / bonds. Displays of familial emotional / relational cutoff, estrangements, conflicts, with unfulfilled longings or no desires for forgiveness / reconciliation.
Loss of Social Connectedness	Isolation / loneliness. Loss of important relationships / social connectedness outside the family. Caregivers may feel detached, like no one cares or understands, seek isolation from embarrassment, and/or not have the time to socialize.
Personal Losses	Practical personal life losses: Arrested personal and professional / educational development. Personal societal connection losses, e.g., job, school, childhood, financial and living resources.
Healthy Emotional Management	Processing and expressing lament and anger (including at God), ambivalence, fear/anxiety, guilt, and sadness; practicing self-forgiveness; having a positive affect and attitude.
Active Problem-Solving	Accurate appraisal, active problem-solving; seeking psychological, social, and/or spiritual/religious support; new boundary setting, arranging respite; good self-care (exercise, diet, sleep, etc.); exercising agency, acting on plans.
Creative / Transcendent Coping	Seeking peace, self-awareness, forgiveness, grace, love. Accepting reality with meaning and purpose reconstruction and hope reframing; experiencing flow [positive life engagement in the now] and joy. Embracing aesthetics/art/music, gratitude, humor, faith, mystery/unknowing. Practicing mindfulness meditation, reflection, contemplative prayer, collaborative (with one’s Image of God) spiritual coping; self-compassion.
Dysfunctional “Coping” Escapes	Persistent emotional or relational disengagement / escape [not oscillation between hope and fearful “avoidance,” which is normal]. Dysfunctional emotional management, e.g., remaining stuck in self-blame, depression, paralyzing anxiety/fear and/or anger. Promoting family dysfunction with emotional cutoff, triangulation, gossip, secrets, projection, passive aggression, blame-shifting; intentional social isolation. Passive religious “coping,” e.g., petitionary prayer, clinging to unrealistic wishes. Not acting on plans; lack of self-care / boundaries; substance use (e.g., ETOH, benzodiazepines).

Fig. 2.

Spiritual Suffering, Grief/Loss, and Coping Strategy Theme Demonstration

Spiritual Suffering Themes

The domains of spiritual suffering were demonstrated variably across the studies examined, with certain themes confirmed frequently and others declared only sparingly. Many studies (10/36) demonstrated the theme of existential angst in uncertainty. A participant in one study shows this by saying:

“I’ve had three very close family members die of cancer, and you go through it and you don’t necessarily get over it, but you do get on with your life … and there is support for the survivor. You know, with Huntington’s, the time period is so long and it’s just this very slow walk down a very long road. You know each day is just slightly worse than the day before. And there is no end to the tunnel, and you don’t know what you’re going to face.”¹⁴

Self-image (intrapersonal) distress was also present across many (9/36) of the analyzed studies. One caregiver poignantly said, “I’m very concerned, I have these meltdowns … it scares me because I’m trying to be strong and I’m trying to be a superwoman and be great at my job, be a great wife, be a great mom.”¹⁴ As an example of an understanding and positive interpretation by a caregiver who was also a genetic carrier, one 47-year-old—who was depressed following his own diagnosis of HD—recounted his father’s suicide, saying:

“We had a farm, and one day he [father] just kind of brought in the veterinarian and he put all the animals to sleep on the farm. I guess he felt maybe we couldn’t take care of them. Another day he took me aside just to make sure I knew how to run the farm, and stuff like that. And, of course, what happened was he killed himself. … I can certainly understand why he made that decision and I think he really kind of did it for our family’s benefit too.”⁹³

However, only a single study demonstrated the themes of either meaning distress or divine/transpersonal suffering (that article showed a clear demonstration of both).⁹⁴ The theme of disrupted religious relationships (interpersonal) was similarly rarely addressed and was confirmed by only 2 of the studies.^93,94 Although one article exhibited all five spiritual suffering themes,⁹⁴ 58% of the articles (21/36) failed to demonstrate even one.

Grief/Loss Themes

The themes of grief and loss were well-represented across the evaluated studies. 86% (31/36) of the articles demonstrated at least one grief/loss theme; three demonstrated all five. Loss of family structure (22/36), loss of social connectedness (21/36), and loss on a personal level (21/36) were quite commonly demonstrated. Loss of the caregiver’s affected loved one’s identity/personhood, which is associated with disenfranchised grief, was also a common theme, demonstrated in 16 studies. Compared to other topics surrounding loss, the theme of general grief symptoms and anticipatory grief was demonstrated in fewer studies overall (5/36).

Coping Themes

75% (27/36) of the reviewed articles demonstrated at least one coping theme; one study demonstrated all four.⁹⁵ Adaptive coping mechanisms were demonstrated across multiple studies. Active problem-solving was the most demonstrated theme and was present in 19 of the 36 studies. Healthy emotional management was demonstrated in 12 articles, and creative/transcendent coping mechanisms were present in 10 of the studies. Maladaptive coping mechanisms were demonstrated in half (18/36) of the analyzed studies.

Representative Thematic Quotes

Many of the research studies included quotes from participant caregivers. Representative quotes demonstrating each of the 14 themes from various studies were extracted and reproduced in Table 5.

Table 5.

Representative Study Participant Quotes Demonstrating Each Theme

Theme	Author (Year)	Quotes (page number)
Meaning Distress	Sobel (2003)	“You hear all these percentages and I’ve always thought, ‘big deal for the one who gets it—with anything—heart disease, whatever.’ You’re the loser, and that’s the one thing we have to prepare ourselves for. We can be the losers in the game.” (51)
Divine / Transpersonal Suffering	Sobel (2003)	A 16-year-old brother of a sister who tested positive told their mother: “God doesn’t have a plan. He just sets up a guideline and away we all go.” Their mother replied: “Yes. Your sister lost the lottery.” (53)
Existential Angst in Uncertainty	Cox (2012)	“I may also develop the disease myself one day. No one wants to settle down with someone who may develop HD.” (292)
	Keenan (2007)	“I love my mum to bits, I always want to help her as much as I can, but it just gets so much as times … And every time when I go in and open her door, I’m always dreading in case I see her lying there with a cracked skull.” (124) A 26-year-old, who supported her 12- and 16-year-old cousins and their mother (with HD): “… when my gran was away on holiday I was about tearing my hair out … anytime there’s an argument, her mum storms out saying ‘Oh I’m going to take pills, I’m going to kill myself,’ stuff like this. And I’m like at my work thinking what the hell can I do? You see she hasn’t got her husband anymore; he left…” (123)
	Mand (2015)	“I think I’d feel a lot of guilt if I was gene-negative, because even though I’d dodged a bullet, my brother and sister were still in the firing line, and I wouldn’t breathe easy until I knew they didn’t have it.” (213)
Disrupted Religious Relationships	Sobel (2003)	“People at church brushed it off with, ‘God will provide a miracle,’ and they weren’t allowing me to face the reality.” (52)
Self-Image Distress (Intrapersonal)	Sobel (2003)	“He [the father] was extremely upset because he felt he had done this to his daughter. He started to hate himself. I think he loathes himself and wants an excuse not to live anymore.” (52)
	Williams (2009b)	“I’m very concerned, I have these meltdowns … it scares me, because I’m trying to be strong and I’m trying to be a superwoman and be great at my job, be a great wife, be a great mom.” (793)
Grief Symptoms	Williams (2000)	Anticipatory grief after their loved one’s positive genetic test: “The main thing that bothers me is that I know how she’s going to be and I’d like to spend more time with her and my job just doesn’t allow it. I feel like I’m missing the best part of her.” (357)
Ambiguous Loss of Loved One	Aubeeluck (2012)	“I have always enjoyed my wife’s company, but … I get these alternating feelings of sadness at the gradual passing of a warm and loving relationship with my wife, then anger at the behaviour. I think the worst thing is this roller-coaster nature of the mood swings so I never quite know who I’m going home to.” (1431)
	Brewer (2008)	“Adam … doesn’t appear to be anything like what you’ve ever seen … in HD. Adam is just really badly behaved; doesn’t listen, doesn’t do as he’s told, hyperactive, like he’s been charged up, doesn’t listen … totally different, like nothing I’ve ever seen.” (8)
	Dawson (2004)	“I guess in a way the grieving of [loss of a husband] is over. I realize that I’ve now got a dependent whose personality is quite different to the man I married. Quite totally different actually so I now look at him as a 12, 13-year-old male child.” (126) “I miss the companionship. Having a dependent who’s no longer a husband that you can no longer talk to anymore because you can’t have conversations anymore unless he’s starting the conversation.” (127) A parent, regarding an adult son: “He was getting very aggressive like we were walking on eggshells towards the end. He was starting to get aggressive and hitting … into the children [grandchildren], … and we couldn’t cope with that.” (127)
	Røthing (2014)	“What hurts me most is that you lose the one you loved. A complete different person is sitting in the dining room today, another person than the one who was my husband years ago. That is sad for me. I am more like a caring person now, not his spouse and loved one as I was.” (702) “Yes, there is a lot of frustration because me and my sister were best friends, super friends, sharing everything, clothes, boyfriends, and excitements, and now she is not here…” (702)
Loss of Family Structure	Etchegary (2011)	“People don’t know that kids need counseling too. They are living in a verbally abusive environment.” (231)
	Mand (2015)	“It’s a pretty negative situation in my dad’s family … when we go to grandma’s we can’t mention it, it’s like it’s something to hide because that’s how they all view it, like it’s shameful … my aunties and uncle are like ‘it’s dad’s disease now.’” (212)
	Williams (2011)	“I wanted to stand by her forever, but now I realise I am not a saint who can go on giving and giving without getting any love or peace. I don’t expect we will manage to remain a family much longer.” (142)
Loss of Social Connectedness	Brewer (2008)	“I don’t go shopping with him … I wouldn’t go … into the town centre, because he just wanders off … he pokes everybody, … and you’re on a bus and lots of people look. … I’ve always said I’d rather … cut out a few of the things in the day, … because that’s making him quite socially unacceptable. People find that hard to tolerate … Especially where you’re in a situation where other people may look.” (11)
	Cox (2012)	“Social circle is very small because of HD.” (292)
	Oosterloo (2020)	“Maybe she wouldn’t have been so alone and isolated from other children. She was so alone, that was incredibly sad. Of course, I don’t know how she experienced it.” (9)
Personal Losses	Aubeeluck (2006)	“The suffocation of my space and time, I miss out on so many things and instead I am on the never-ending relentless journey towards her death.” (101)
	Aubeeluck (2012)	“…the other part that goes with it is the costings. We won’t have anything to do with it as the carers we, we make sure that - there is a real implication between what the government are defining as healthcare and social care and when you back to the finances cos they’re all interlinked there are a number of hoops that you’ve already got with a neurological terminal condition, it’s ridiculous, there should be a much simpler way, um and I think a a a way of relief to come …” (1431)
	Cox (2012)	“I am stuck at home caring for my mom. I love her and want to care for her, but I am stuck, which is killing my independence and my ability to find happiness in relationships.” (292)
	Keenan (2007)	“Before school we had to get my mum bathed, changed, get her breakfast, plus get us showered and changed. Plus you’d have to do all the tidying up before you went … and then coming home tea would have to get made. I missed most of my third year at school because of it. I didn’t like leaving mum here on her own during the day while me and my sister were at school and my dad was out working so some days I would skive off just to make sure she was all right.” (122)
	Mand (2015)	“I don’t go to school, I quit in April. I just help dad around the house, he needs it because he works full time and my brother is at school, so I stay home and look after the house … Most of my friends are still at school so I don’t get to see them often.” (212)
	Sparbel (2008)	A teenager: “My dad [with HD]… he doesn’t eat, you have to feed him. If he’s not cooperating, then she [my unaffected mother] has to take care of everything else … so I try to watch over her [my mom] too … I’ll run her errands, I’ll clean the house, cook some food, so she takes care of my dad. There’s always something that needs to be done.” (332)
	Williams (2009b)	“I may get, if I’m lucky, some nights maybe an hour or two hours of sleep … I’ve had 5 surgeries myself and … my husband would call me to help him in the bathroom and I could barely take care of myself.” (793)
Adaptive Coping: Healthy Emotional Management	Kavanaugh (2017)	An 18-year-old, in response to a youth support camp: “The camp has affected me in such a positive way. HD does not frighten me anymore. I am not scared of my future. It has … been life changing.” (330) A 17-year-old, in response to a youth support camp: “I am much more positive and not so embarrassed. I am better in dealing with stressful situations in positive ways. HD doesn’t scare me anymore.” (330)
	Williams (2009a)	A teenager explains sadness and anxiety management: “… trying to, you know, enjoy the last proofs of my mom before something really bad happens.” (282)
Adaptive Coping: Active Problem-Solving	Aubeeluck (2012)	“When I was helping to care for my father, I remember how difficult it was. I started going to one [a support group]. It’s small and I travel 150 miles round trip, but it is so worth it. That would also give you a day to … just you, take a little extra time and treat yourself to dinner or something. Take care of yourself first. You are no good to anyone else if you’re falling apart.” (1430)
	Kavanaugh (2017)	“I met lots of friends who have connections to HD along with skills to cope with the disease. I learned a lot to help me deal with everyday life.” (330)
	Keenan (2007)	“We’re starting to change the structure of the house so that it’s accessible for my mum, and the bathroom is not big enough. So these are all things that we’re gradually changing and gradually looking at. It’s all about managing your parents – the tables have turned!” (125)
	Oliveira (2020)	“I have never hidden her disease from anyone, … we would go out for a walk or to the hairdresser … or even to the same restaurant.” (5)
	Røthing (2015)	“I have chosen to work full-time, actually now also with the possibility of working at home, to reduce overtime work. … But, I prefer to go to work because it is better. Somehow, my function at work is better than my function at home; my work keeps me going, with good colleagues. It means a lot to me, it is the only place I can socialize.” (573) “I try to stay healthy. Sleep as much as I can and go for walks alone. I live a regulated life. Sometimes, it happens, I find time for a little trip, alone or with my children. It is rare. I need something to look forward to and something nice to think of later. I have to, if not, I know I will be depressed.” (573)
Adaptive Coping: Creative / Transcendent Coping	Aubeeluck (2012)	“When I was helping to care for my father, I remember how difficult it was (sigh) especially looking and feeling like I was somehow seeing my own future played out before me. I’m glad the Lord God is your strength, I can relate. He is mine also. As difficult as it is sometime, remember that is a tremendous amount of strength.” (1430) “… as a family we can get through whatever life’s challenges are. HD has brought us closer.” (1432)
	Halpin (2012)	“…my attitude is like life is like a gift every day. Every day is like a free day to me. And not every day is a good day and not every day is equal but in general it’s pretty good. … That’s sort of how I see life, and I’ve had all these nice mental thinking days of my life.” (327)
	Keenan (2007)	“I see everybody else as different and my mum’s normal because I’ve lived with it … whereas everybody else would see my mum as different but I don’t. … I’ll walk down the street with mum and not care what anybody else thinks.” (125)
	Lowitt (2005)	“You can’t really plan for it – I just take one day at a time. It’s so slow you just adapt.” (5)
	Oliveira (2020)	“Shame? What shame? I am not ashamed! I have a sick son, I’m not ashamed.” (5)
	Williams (2009a)	“When this is over, and if you don’t get it, you’ll be a better person in the long haul. You’ll have, uh, spent your time in hell, so … if you don’t get this … then, your life’s going to be great because you went through hell already.” (284)
	Williams (2009b)	“You look for little things. I got a great family, I got great friends. But our faith and my church has gotten me through more.” (793)
Maladaptive Coping: Dysfunctional “Coping” Escapes	Aubeeluck (2012)	“…we don’t want anyone to tell us, we don’t want anybody in the house, we’ll cope with this on our own and its all the burden on all the carers then. Cos you have that burden that they don’t want anybody in the house and they deny that they are ill.” (1432) “We only found out that HD was in the family recently and it was such a shock. We are still having troubles getting information from any of the family, … now my brother-in-law is acting the same, in the space of one conversation he told my husband that he had the test and … then told him that if my husband’s test comes out negative, then he will get tested himself. … I don’t understand why he would lie like that.” (1432)
	Keenan (2007)	“I dreaded going home because I got beaten up [by my dad] … So I turned into a bit of a rebel at 15 – alcohol, drugs, coming home late.” (126)
	Lowit (2005)	“Well you know, he wouldn’t talk about it at all. It was difficult to find anyone to talk to within his family. I didn’t know about it (HD) and they weren’t going to tell me anything about it.” (4)
	Oliveira (2020)	“They don’t tell much, because my father’s family was very afraid of what others could think or say ⋯ this [HD] was a taboo, one would not speak nor admit it because they’d be ashamed.” (4) “My older sister never did the test. She doesn’t deal well with the disease, she drinks, she’s not working. She believes she has the disease and that she will die and so she has to enjoy life now.” (5)
	Røthing (2014)	Speaking of caring for her mother and younger siblings: “I could not tell about it to my father. I isolated myself from others, and in dark times, after I had put smaller siblings to bed, their schoolbags were packed, food for the next day made ready and the house cleaned up, I had ten minutes for myself.” (702) “Our son moved out early, but our daughter who stayed at home was like a chopping block for her HD affected mother. When something went wrong she was always the one to blame. She must have suffered a lot.” (703)
	Sobel (2003)	“There were some wicked fights because all of our emotions were too close to the surface. It wasn’t very pretty. It was pretty harsh. Nobody knew what to do with what they were feeling.” (52)

Discussion

This study confirms the hypothesis that HD patient caregivers’ burdens are high and that they have significant unmet needs. As one participant said, “Caregivers have enough responsibilities on their hands to spend hours researching for help.”⁹⁶ Variables such as income, economic pressure, and social support predict life quality among caregivers of people with progressive neurologic diseases,⁹⁷ and yet these factors only begin to scratch the surface of the multifaceted forms of suffering that these caregivers experience. Caregiver quality of life is a different concept than caregiver burden.⁶ The suffering associated with caring for a patient with HD outstrips the burden in relation to the realms of physical, emotional, time, financial, and other social drains.

A Quality Care Gap Well-Suited to Palliative Care

There is a pressing need for increased involvement of PC experts to collaborate with neurology teams to help support patients with all neurodegenerative diseases,⁹⁸ and this specifically includes the needs of their caregivers, including long-term psychological and emotional support^99,100 and empathic communication skills.¹⁰¹ In recent years, the advantages of PC involvement in patients with ALS and their caregivers have been increasingly demonstrated.¹⁰² Several recent reviews have documented a high burden of symptoms in late-stage HD patients potentially amenable to palliative care interventions.^23,103,104 In one study, 2/3 of such patients lacked advanced directives.¹⁰⁵ Furthermore, HD patients most in need of palliative care are often too disabled to access the specialty clinics where they have established therapeutic relationships.

Religious faith and spirituality have been shown to provide a powerful avenue for meaning-making, well-being, and coping in ALS patients and their caregivers.^75,106–108 Spirituality has also been shown to improve the quality of life and reduce the risk of disease and death for caregivers of geriatric oncology patients.¹⁰⁹ Meaning distress in bereaved caregivers, as they cope with the loss of a loved one has also been demonstrated.⁵⁹ Spirituality has not been specifically investigated as a means of coping for caregivers of HD patients,²³ however patients with serious illnesses frequently experience their disease through a spiritual hermeneutic, both as a source of support for coping and transformation and/or as a basis of concern/suffering.²⁵ The Huntington’s Disease Peer Workgroup concluded that we should “improve support for families in caregiving -- and in grief. And we can educate, counsel, and support HD families across generations.”¹¹⁰ They also recommended the following call to action: “Screen for and respond to spiritual distress expressed by patients with HD and their families, extending spiritual care to them and supporting their spiritual experience. The potentially changing spiritual experience and needs of people with HD must be met throughout the disease.”¹¹⁰

A recent report on challenges in delivering complicated palliative neurology care to patients with motor neuron disease highlighted: (1) prolonged timelines of disease progression, (2) threats to personhood, (3) prognostic uncertainty, and (4) existential distress specific to neurological disease, including emotional, psychological and spiritual distress resulting from loss of function, autonomy and death.¹¹¹ A recent review promoted integrated spiritual care for people with neurodegenerative conditions and their caregivers, specifically suggesting developing and delivering belief- and value-based care models, in order to prevent health-related suffering.¹¹² Ideally, caregivers of patients with such devastating chronic illnesses as HD should be introduced to generalist palliative care and “referral for specialist palliative care support should be made at any time when physical, social, psychological, or spiritual unmet needs are not able to be satisfactorily resolved by the primary caring team.”¹¹³ Lacking formal training in palliative and spiritual care, HD specialists who focus on the clinical needs of patients are often limited in their ability to manage the spiritual suffering, grief and coping needs of caregivers.

Thematic Demarcation between Grief/Loss, Spiritual Suffering, and Coping

By identifying and inducing prevalent themes from various literature and then deliberating on the similarities and differences within themes, we have generated the first comprehensive taxonomy of distinct thematic definitions for 10 types of spiritual suffering, grief, and loss, and 4 additional themes relating to coping. The subjects of grief/loss and spiritual/existential suffering, in particular, are intermingled in complex ways. As an example of how complicated the interrelationships are between various types of suffering, the following participant quote from a focus group study touches on at least four distinct themes in our taxonomy:

“I know that there must be others who have HD and also are the sole caregivers to a parent, but it feels like there is no place to go where I can express the pain involved in this and the guilt because there are times I feel as though I can’t take it anymore. It is often a painful place mixed with cries of despair and then times when all goes as well as can be expected but it seems lately I am running out of the heart to go on being the one responsible for mum’s needs while feeling the disease myself but there is no-one else to help, it is my job.”⁹⁶

Suffering complexity generates areas where various thematic definitions “touch” others. This is well illustrated by a unique study that captured the experiences of caregivers through a ‘photovoice’ method, wherein spousal caregivers of HD patients took photographs and then artistically described them.¹⁰ One such participant’s photo showed a children’s swing set and slide with a bicycle, soccer ball, and scooter piled in front of the swing, with the caption: “Toys in the garden. With a genetic disease it means that we choose not to have children – our future is taken away from us.”¹⁰

Grief and Loss in HD Caregivers

Each person’s grief experience is unique, and yet similar aspects can be characterized. Within the domain of grief/loss, many HD caregivers experience disenfranchised grief, which is related to the gradual ambiguous loss of their attachment to their loved one’s personhood and identity before they die. Loss in disenfranchised grief may be socially negated, socially unspeakable, or both. Such socially-unsanctioned grief leaves many caregivers mourning in solitude without support as if they feel they have no right to mourn.^9,69 Some spousal caregivers do not want their children exposed to the experience of watching their affected parent “fall apart” or deteriorate before their eyes.¹¹⁴ Other times, caregivers’ grief processes are thwarted by the absence of finding meaning in the situation they find themselves in.⁹⁴ One study stressed that finding meaning was crucial to combat feelings of helplessness and despair; and that without finding meaning, caregiver grief remains unresolved and disenfranchised.⁹⁴

Not only do caregivers lose their loved ones as they knew them, but they also experience a loss of their former family structure. Patients with HD’s mood and behavioral problems can drastically alter their family’s relationships.¹¹ HD families commonly experience a loss of family structure as evidenced by fractured previously-intimate relationships and/or conflicts that may have escalated to emotional cutoffs and estrangements.^115,116 These broken family bonds may leave caregivers further isolated. Withdrawal from social networks and isolation can be a dynamic and two-way process, since both the shame felt over people’s reactions to loved ones with HD (societal pressures) and the intense time-constraint burdens of caregiving play important roles in fostering intentional seclusion.^16,95 One study suggested that parental caregivers often find it challenging to ask for help and support, increasing their isolation.¹⁶ Some children caregivers—many of whom have had their adolescence interrupted by role reversal and the ambiguous loss of their parent’s identity—also find it difficult to discuss HD or their situation with their peers. The majority of caregivers in one study had quit attending support meetings, claiming that although they valued and praised them, that meeting other caregivers made things worse because they were presented with an even more dismal vision of their future.⁹⁰

In addition to the loss of time and other living resources, such as financial strains, personal losses include arrested personal and professional/educational development, as tragically demonstrated when children care for their parent with HD. As a parent with HD begins deteriorating, many children experience instrumental and emotional parentification, which is frequently overwhelming. For example, children—sometimes as young as grammar-school-aged—may carry out household tasks, such as washing, shopping, cooking, cleaning;^117–122 and may feed, bathe, toilet, provide company for and emotionally console their parent with HD;^{117,118,120,122} sometimes relaying school problem experiences or skipping school to do so.^{117,119,120,122} In this way, the child’s parentification and the parent’s dependency warps the traditional family structure, generating profound personal losses such as loss of innocence, and loss of time with friends, along with educational, developmental, and individuation delays associated with interrupted adolescence. One research study found that the frequency of childhood caregiving directly correlated with higher conflict with the ill parent and more problems with school;¹¹⁷ others concluded that young adult and teenage caregivers act as important supportive linchpins in the family system.^118,122

Spiritual Suffering in HD Caregivers

Spiritual suffering among HD caregivers may be devastating. Spirituality has been defined in the PC literature as encompassing four major themes: meaning-making, purpose, connectedness, and transcendence, with or without a relationship with what most of us call “God.”^47,49 HD family caregivers’ spiritual suffering is likely persistent/chronic and may manifest as recurrent struggles in meaning-making, loss of their own identity/personhood/dignity, as well as that of their affected loved one, relationship/connectedness strain (with others, themselves, and for theists, God), isolation, shattered God images—including anger at and/or feelings of abandonment by God—as well as psycho-spiritual suffering, such as hopelessness, despair, and feelings of unfairness.^37,123 Spiritual suffering screening and assessment tools,^{42–44,46,51} which have only recently begun to be described and validated, provide an opportunity for quantifying this experience.

The themes within the domain of spiritual suffering were not demonstrated nearly as frequently in this review as those in the grief/loss domain, however, this may be due to a relative de-emphasis on spiritual suffering in the studies we reviewed. This is supported by our finding that one study showed a clear demonstration of all 5 spiritual suffering themes.⁹⁴ Also, of the 10 studies that employed surveys, only one used an inventory that queried spirituality as a resource for coping;¹²⁴ neither it nor any of the others probed spiritual suffering. After anyone in a family receives an HD diagnosis, caregivers’ whole worlds change. Their plans for the future and their family get turned upside down overnight. This existential dread can manifest as hopelessness/despair,¹²⁵ and/or intense fear regarding the future.

Grave anxiety over pre-symptomatic genetic testing in HD further elongates the timeline of uncertainty because it cannot determine the date of symptom onset.

Self-image distress includes significant struggling with or loss of personal identity or loss of the caregiver’s sense of self, personhood, or dignity; as well as instability of values and/or their feeling of purpose in life, beliefs, and/or faith practices. Guilt, shame, self-blame, deep regrets, and moral distress in how much time and energy to expend in caregiving vs. other life roles are other manifestations of self-image (intrapersonal) distress. Huntington’s disease patients and their possibly-unaffected siblings¹²⁶ and children,¹²⁷ frequently consider attempting, and sometimes complete suicide.^128,129 As a testament to the depth of existential/spiritual suffering in HD families, the prevalence of suicidal ideation in HD is alarming and significantly higher than in other neurodegenerative disorders. Caregiver self-image distress can be either exacerbated or confirmed by their loved ones’ suicidality.

Meaning distress, divine or transpersonal spiritual suffering, and disruptions of very meaningful religious relationships were uncommonly demonstrated in this review. They were uncovered, however. A few articles mentioned these, once as a mixture of disrupted religious relationships and divine/transpersonal suffering, demonstrated by how one caregiver rejected their religious upbringing and became an atheist after his loved one attempted suicide.⁹³ We suspect that divine or transpersonal suffering and disrupted religious relationships are under-reported in our review, because of the spirituality and spiritual suffering knowledge gap on the part of many of the researchers. The actual incidence of spiritual suffering themes can only be determined by research methods that balance the investigation of this domain with querying other forms of pain and loss.

Coping in HD Caregivers

Caregiving coping research has been traditionally guided by Lazarus and Folkman’s 1984 model, which asserts that coping begins when a loved one’s state is appraised as threatening, harmful, or challenging, and goes on to address the management of that distress.¹³⁰ Following this, Folkman began stressing one’s affective appraisal of the threats (positive, negative, or mixed),³¹ which furthered the distinction between problem-solving and healthy emotional management. Other coping psychology experts defined coping as a self-regulatory model of behavior, which describes the relationship between illness perceptions, coping mechanisms, and peoples’ quality of life, implicating coping as a significant mediator for well-being.¹³¹ More recently, Folkman and Park have described a third distinct type of coping: meaning-focused coping, which draws on values, goals, and beliefs.^32,33 Meaning-making coping has been hypothesized to be especially important in stressful situations that are prolonged and chronic,³² such as the context that HD family caregivers face. It incorporates faith-based religious and spiritual coping³⁴ and goes beyond the typical psychological processes of problem-solving and emotion-focused strategies, so we chose to label it creative/transcendent coping. In the studies we reviewed, the most commonly demonstrated HD caregiver coping strategies were adaptive coping through active problem-solving (19) and dysfunctional or maladaptive escapes (18). Twelve studies revealed that HD caregivers used adaptive healthy emotional management strategies and 10 demonstrated adaptive transcendent/creative coping mechanisms.

One area in which we struggled during our taxonomy development was in determining how best to characterize caregiver avoidance, such as in social situations. Are these behaviors adaptive or maladaptive?³² HD patient caregivers are often, but not always socially avoidant. For example, although participants in one study avoided support groups, out of fear of a dismal portrayal of their future;⁹⁰ the assessment of camps for children growing up in a family riddled with the HD gene are uniformly positive.^132–134 Another study of families struggling with juvenile HD found that long-term support from a social worker was highly valued.¹⁷ While some forms of such avoidance may be maladaptive, such as persistent emotional or relational disengagement, two psycho-spiritual models suggest that intermittent avoidance may be adaptive, allowing much-needed respite from caregiving distress. The oscillation model of existential angst (fluctuation between denial and acceptance across the dynamic “space” of “middle knowledge”), as originally described by Avery Weisman;⁸⁹ and re-illustrated by Jacobsen, et al,⁷⁹ demonstrates how periodic avoidance is normal—adaptive—human behavior. Weisman describes “middle knowledge” as a paradoxical “area of uncertain certainty, … somewhere between open acknowledgment of death and its utter repudiation.”⁸⁹

In bereavement, a similar model that normalizes oscillation has been promoted by Margaret Stroebe and associates. She claims that the dynamic process of oscillating between confronting and avoiding both the stressors of loss- and restoration-oriented coping, which describes the temporary “denial” of one’s losses and/or restorative tasks, is both normal and beneficial (Fig. 3).¹³⁵ We deemed these forms of oscillation as adaptive, transcendent coping, because of the intra-personal, meaning-making, spiritual formation nature of the process.^60,136 Persistent emotional, meaning-making, and/or relational disengagement, on the other hand, is maladaptive. Although grief work can occur with the help of others, it is essentially intrapersonal.^12,135 Worden’s tasks of mourning include (1) accepting the reality of the loss, (2) processing the pain, (3) adjusting to a world without the loved one, and (4) finding a way to remember them while embarking on the rest of one’s life journey.¹² His mourning process tasks can be applied to prolonged caregiver grief during long-term neurodegenerative decline before a loved one’s death. Importantly, his third task embraces intrapersonal spiritual adjustments to how grieving individuals view the world without the person they were so intimately attached to;^12,135 these are chiefly meaning-making endeavors.^{33,48,60,77,135}

Fig. 3. Transcendent Adaptive Oscillations in Coping with Grief and Loss.

As grief-stricken people embark on the necessary tasks of coping; grapple with existential finitude, decline or any significant loss; they oscillate between confrontation of concrete realities (below) and what may appear to be denial (above), but what is actually healthy, adaptive periodic avoidance. The intra-personal journey through this messy process, from left to right and across Weisman’s dark “middle knowledge” space of “uncertain certainty”⁸⁹ is normal, adaptive transcendent coping. The meaning-reconstruction that occurs in this dark space ultimately leads to acceptance (to the right), which empowers the grief-stricken individual to adjust to a new world.

Transcendence means moving beyond concrete notions of oneself, the physical world, and connecting outside oneself, whether that connection is to God or something sacred, typically to provide a grounding for meaning (re-)construction. Transcendent coping includes dynamic—perhaps by oscillation—acceptance of (concrete) realities as well as developing equanimity in the face of struggling with the unknown, again, accompanied by meaning reconstruction. This type of coping is frequently expressed by caregivers of HD patients as “taking one day at a time;”⁹⁴ which we interpreted as positively surrendering to life “in the now”, similar to Mihaly Csikszentmihalyi’s creative invention or experiencing “flow” as a momentary transcendent engagement with everyday life.^81,137 Transcendent coping includes embracing activities and attitudes that go beyond emotional, cognitive, and physical processes, manifested by employing humor, faith, the arts, or experiencing joy and practicing self-compassion.

We sometimes found differentiating transcendent coping from active problem-solving or healthy emotional management challenging. Similarly, teasing transcendence out of following religious traditions can be tricky. Sometimes, meaning-making spiritual formation includes a caregiver’s rejection of earlier images of God or religious constructs that they have found counterproductive to their life journey. For example, one study participant—who became an atheist—followed up “… my attitude is like life is like a gift every day. Every day is like a free day to me.” with “And I regard my religious days as not fully living. I was living in fear of funny things. Superstitious things.”⁹³ On the other hand, Roscoe, et al found that high levels of spiritual involvement and beliefs were indicative of successfully finding meaning in times of hardship, allowing caregivers of HD patients to accept things as they are.¹²⁴ Helder, et al administered the 14-item COPE inventory^138,139 to 90 HD spousal caregivers and found that they ranked “acceptance” first and “reinterpretation and growth” fourth; whereas “turning to religion” was ranked ninth.¹³¹

Maladaptive “coping” is highlighted by persistent deliberate emotional and relational avoidance or escape mechanisms, manifesting as family secrets,^{90,94–96,114,140–142} closed family systems,^94–96,120 or obstinate intentional social isolation.^{9,95,96,122,142} Maladaptive strategies also include blame-shifting, emotional cutoff, alcoholism and substance use, and in the most horrific cases, physical and sexual abuse and even incest.^5,143

Current HD Caregiver Well-Being and Suffering Assessment Tools

The 34-item measure of HD caregiver quality of life (HD-QoL-C) that is most often employed primarily assesses caregivers feelings and satisfaction, only superficially addressing two aspects of spiritual suffering; four aspects of grief/loss with none that query the ambiguous loss of their loved one’s identity, and only lightly addressing coping without any specific inventory of active problem solving or maladaptive strategies.¹⁴⁴ Furthermore, this tool has been shown to have limited psychometric value, hampering its usefulness and suitability in measuring HD caregivers emotional and psychological distress.^145,146

The three research publications that yielded the most robust results in this review, demonstrating 9, 10, and 13 of the 14 themes, were all interview studies.^94,96,120 This highlights how surveys tend to be focused on only one or at most two of the domains, and often overlook spiritual suffering and transcendent coping. Thus, we conclude that a better screening tool is needed, importantly combined with personal interviews of HD caregivers to further explore nuances—such as distinguishing between healthy oscillation (Fig. 3) and persistent denial/escape—as well as investigating meaning distress and transpersonal suffering or transcendent coping, which have been uncovered by such screening. Ideally, this screening and exploration should be undertaken by experts who excel in empathic communication and understand all three domains as well as how various themes touch upon other themes. While this is outside the scope of specialist neurology care, it could be accomplished by the integration of concordant palliative and spiritual care experts.

Limitations

The prevalence of any form of spiritual suffering, grief/loss, and adaptive or maladaptive coping among caregivers of patients with HD cannot be ascertained by a literature review, as the data are influenced by each research team’s focus. This review included a variety of research study methods, many of which were descriptive, and only some of which were subjected to rigorous qualitative analysis. The research quality of the included studies was not ascertained. The articles we reviewed were conducted on a fairly homogeneous group of participants; a more diverse population may yield different results. Despite these limitations, it has been possible to formulate compelling conclusions.

Next Steps

Our findings generate health policy, clinical and research implications, not just for caregivers of patients who are suffering from HD, but for all patients and their caregivers who have serious, debilitating, life-threatening illnesses. Unfortunately, medicine often neglects spirituality.^147–149 It has been suggested that this separation between religion/spirituality and medicine is promulgated by the following beliefs: (1) hospitals provide technologies and cures, rather than humanistic care; (2) physicians are scientists and health managers rather than whole-person healers; (3) humans are divisible into the material and immaterial, with no connection between body and soul/spirit, so health and well-being are not related to spiritual notions; and (4) the engagement of existential fear can only be dealt with by religious communities and spiritual leaders, not clinicians.^148,149 Healthcare policies to overcome these barriers and system-wide cultural biases include: (1) requiring education in basic spirituality and suffering screening^150,151 and training in primary spiritual care skills for all clinicians;^{26,147,152–155} (2) requiring that medical institutions partner with local religious communities and incorporate spiritual care experts, such as chaplains,^{150,154,156,157} in order to protect the personal and human aspects of compassion and care; (3) routinely incorporating spiritual care into the medical care of seriously ill patients by generalists,^{26,147,149,150,152,157} and (4) requiring honest determinations of what is necessary to provide whole patient-centered care with professionalism, including sensitive inquiry and engagement of each individual’s values, particularly as they affect their medical decision-making.^{152,158–160}

From clinical and research standpoints, existing HD caregiver quality of life instruments do not address spiritual suffering, grief/loss, and coping comprehensively. Spiritual suffering is probably underreported because it is under-investigated. Seminal PC articles illuminate the need for spiritual suffering screening and assessment tools that are rigorously developed, clinically relevant, and adapted to a diversity of clinical settings.^161,162 Spiritual suffering assessment tools are now available, many of which we used in our initial thematic induction. Three are highlighted here: the PC-7, developed for patients with advanced illnesses where end of life issues are pertinent;⁴³ the Religious and Spiritual Struggles Scale (RSS);⁴² and the Spiritual Distress Assessment Tool (SDAT), which was developed for geriatric rehabilitation.⁴⁴ Neither the SDAT nor the RSS assesses grief or loss; the PC-7 does, but without addressing the ambiguous loss of a loved one’s personhood; none of the three assesses coping. In addition, all were developed and validated in patients as opposed to caregivers. A broader comprehensive screening tool—which focuses on caregivers and assesses grief/loss and coping too—is needed. For effective research and comprehensive clinical screening, our taxonomy can be used as a springboard to develop one, not only for those caring for HD loved ones but also for those caring for patients with other disabling illnesses. Perhaps a modification of one of these tools—using the taxonomy that we developed (Table 4) as a guide—incorporating non-redundant elements of validated caregiving coping assessments (e.g., selected questions from the 14-item brief RCOPE⁶⁴ to fill the adaptive transcendent coping query gap) is the answer. Ultimately, we hope to engage spiritual care experts to develop such a comprehensive, practical (shorter) assessment tool for screening and engage the HD community to pilot, administer and validate it, proving its feasibility and reliability. Then palliative and spiritual care experts can be better prepared to join with HD care teams to aid in screening for and exploring spiritual suffering, grief/loss, and coping in more depth; further supporting caregivers with active, engaged empathetic listening, which will by its very nature promote healing and provide compassionate holistic care.^{47,50,58,83,163}

Conclusion

The burdens of caring for a patient with HD encompass every aspect of humanity, including spiritual suffering and grief. We can safely assume, based on this review, that spiritual suffering and grief are ubiquitously experienced by caregivers of patients with HD. These sources of prolonged pain and loss are rarely seen by the public or healthcare professionals.¹⁶⁴ Attendance to spiritual suffering, grief and loss, and supporting adaptive coping are areas where PC experts excel, and yet addressing these important aspects of whole-person care in caregivers of HD patients is greatly missing in the palliative care literature. We propose developing a comprehensive screening tool—based on our taxonomy—to address both currently-identified and poorly-identified palliative care needs to better support HD caregivers in their multifaceted suffering and coping and ultimately facilitate the integration of specialist palliative and spiritual care with primary neurology team-based care for HD patients and their distressed family members.

Key Message.

HD caregivers experience prolonged grief as they lose their loved ones, their former family roles and experience genetically based existential uncertainty. With improved assessment tools, focusing on spiritual suffering, grief, and coping, teams with palliative and spiritual care experts will be better able to support HD caregivers and their families.