Neck Disability and Insomnia in Head and Neck Cancer Survivors

doi:10.21203/rs.3.rs-1517752/v1

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Neck Disability and Insomnia in Head and Neck Cancer Survivors

https://doi.org/10.21203/rs.3.rs-1517752/v1

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Purpose: Head and neck cancer (HNC) treatments often have a substantial long-term impact on physical appearance, psychological well-being, and physiologic functions. Our study examines the relationship between symptoms of neck disability and insomnia among post-treatment HNC survivors.

Methods: Cross-sectional analysis of adult survivors of squamous cell cancer of the oral cavity, oropharynx, and larynx/hypopharynx treated at a single-center, university-affiliated HNC survivorship clinic between August 2018 and March 2021. The primary outcome is Insomnia Severity Index (ISI) score. Multivariable ordinal regression was used to analyze the association between neck disability index (NDI) scores and insomnia.

Results: A total of 411 predominantly male(77.9%) survivors with an average age of 63.07±11.53 years, were included in the analysis. Primary cancer sites were oropharynx(48.7%), oral cavity(28.0%), and larynx/hypopharynx(23.3%). Mean ISI and NDI scores were 7.09±6.66(range=0-28) and 8.83±8.06(range=0-38), respectively. After controlling for age, race, treatment modality, tumor site, tumor staging, and time since treatment, the odds of a survivor reporting insomnia was 8.65 times higher in those with mild neck disability(95% OR (4.31, 17.37), p<0.001) and 48.12 times higher in those with moderate to complete neck disability(95% OR (22.35, 103.58), p<0.001) when compared to those with no neck disability

Conclusions: The acute symptom burden of neck disability is shown to be highly associated with insomnia severity. HNC providers should address an array of symptoms for early diagnosis and intervention. Our results support the need for a multidisciplinary care model for post-treatment HNC survivors to facilitate screening, access and early intervention for survivor well-being.

Head and Neck Cancer

Insomnia

Neck Disability

Head and Neck Surgery

Quality of Life

Head and neck cancer (HNC) treatments often have a substantial long-term impact on physical appearance, psychological well-being, and physiologic functions. Dramatic shifts in demographics due to the prevalence of human papillomavirus (HPV)-related carcinoma and intensification of treatment have contributed to an increasing cohort of survivors with long post-treatment courses with increasing late- and long-term treatment-related toxicities [1–6]. These toxicities contribute to decreased quality of life (QOL), necessitating novel, multidisciplinary therapy to address their unique psychosocial and physical needs [7–10]. As a result, meaningful measures of QOL in the form of patient-reported outcome measures (PROM) have become essential in HNC survivor care, predicting prognosis and areas in which targeted therapy may provide the most benefit [11–13].

Neck disability is one of the leading impairments in post-treatment HNC survivors, affecting up to two-thirds of patients treated for the disease [14–16]. The effect of treatment on the pain and physical impairment of the neck improves after treatment, only to progress later in the patient’s survivorship course [17–20]. Neck disability has been associated with numerous effects on psychosocial and QOL outcomes, impacting areas where neck motion and strength are required and the well-being and social function of the survivor [15, 17, 21–24]. The severity of neck disability can be mitigated not only by treatment radiotherapy de-escalation and focus on modified or limited neck dissection where appropriate, but also the early intervention of therapy focused on maintenance of muscle mass and flexibility [25–30]. This focus on early intervention and facilitation of access to care is a key benefit to the multidisciplinary survivorship care model, which reduces delays in therapy and the impact of post-treatment toxicity [8, 31–34].

In addition to physical impairments, survivors are often affected by various psychological side effects of treatments [35–38]. Up to half of those treated for cancer are affected by insomnia, contributing to poor QOL and prognosis [11, 39, 40]. Insomnia often begins with treatment in cancer patients with side effects, pain, fatigue, and distress contributing to aggravated insomnia during and after treatment with accumulation post-treatment [41–44]. While the effect of HNC treatment on insomnia has been well-reported, there is a paucity of information on the relationship between neck disability and insomnia in the survivor population. In this study, we examine the relationship between reported neck disability and insomnia, further exploring the intersection between the physical and psychological impacts of HNC therapy.

We conducted a retrospective, cross-sectional analysis of 411 HNC survivors who completed PROM questionnaires on neck disability and insomnia during their visit to the UPMC Head and Neck Cancer Survivorship Clinic between August 2018-March 2021. All adults (≥ 18 years) who completed treatment for squamous cell carcinoma of the oral cavity, oropharynx, and larynx/hypopharynx at their initial visit were included in the analysis. Survivors with a history of recurrence, second primary carcinomas, or distant metastasis were excluded. The University of Pittsburgh’s Human Research Protection Office approved this study.

Demographics and clinical characteristics were abstracted from the medical record, including variables of age, sex, race (White, Other [e.g., African American/Asian]), marital status, tumor site (i.e., oropharynx, oral cavity, larynx/hypopharynx), American Joint Committee on Cancer (AJCC) staging (7th and 8th edition), treatment modality (i.e., surgery alone, non-surgical, and surgery plus adjuvant), and time since treatment completion. Analysis was completed for survivors both immediately and over six months since treatment completion.

Neck Disability Index

The Neck Disability Index is a 10-question measure of the impact of disability on functional activities, pain, personal care, sleep, and movement, with higher scores indicating more severe disability [45]. Each item is scored from 0–5, increasing with severity, with scale scores ranging from 0–50. The minimal clinically important difference (MCID) is reported in prior studies as approximately 10 points [46–49]. The NDI has been used to measure neck dysfunction reliably and consistently in HNC patients [22, 45, 50–53]. In our study, NDI was used as a continuous scale to evaluate the relationship with insomnia, with higher scores indicating increasingly severe neck impairment, and categorized into three groups: no disability (≤ 4), mild disability (5–14) or moderate-complete disability (> 15). Each NDI subsection was analyzed for its relationship with the insomnia category. For the univariable and multivariable analysis, the question related to sleep was removed to prevent confounding the relationship.

Insomnia Severity Index

Insomnia was measured using the insomnia severity index (ISI), a seven-item questionnaire with questions on sleep quality, maintenance, and interference with daily functioning [54]. It is a reliable and valid questionnaire in the HNC and cancer survivor population with questions referring to symptoms within the prior two weeks [55–57]. MCID for the ISI is reported in other studies as 6 points [58]. Total score ranges from 0–28, and measurements were used on a continuous and categorical scale, with higher scores indicating more clinically severe insomnia. For ordinal regression models, patients were stratified into three groups: no insomnia (score 0–7), subthreshold insomnia (score 8–14), and clinical insomnia (score > 14).

Statistical Analysis

All statistical analysis was performed using RStudio (1.1.456; RStudio, Inc, Boston, Massachusetts) and SAS v9.4 (SAS Institute, Cary, North Carolina). We calculated frequency (percentage) for categorical variables and mean ± standard deviation (SD) for continuous variables for the descriptive analysis. Univariable linear regression was performed to analyze the association between independent variables, including age, time since treatment, sex, race (White, Other [e.g., African American/Asian]), marital status, AJCC 7th edition staging [i.e., early (stage I/II) or advanced (stage III/IV)], tumor site (i.e., oral cavity, oropharynx and larynx/hypopharynx), HPV status (i.e., positive, negative, unknown, or not applicable), and NDI, and insomnia category. Considering both statistical and clinical significance, the multivariable linear regression models included age, race, time since treatment, cancer site, staging, and NDI category. Variables with a p-value less than 0.05 were considered significant.

A total of 2575 HNC survivor visits were identified for eligibility in the analysis, with 1800 excluded due to non-squamous cell carcinoma, site other than oropharynx, oral cavity, or larynx/hypopharynx, incomplete treatment, recurrence, metastasis, second primary, or repeated visit. The preliminary analysis consisted of 775 individual post-treatment HNC survivors, with an additional 364 visits excluded from the final analysis due to incomplete or missing PROMs data. The final analysis consisted of 411 HNC survivors, and the identification of participants is shown in the consort diagram (Fig. 1).

The cohort was predominantly male (n = 320, 77.9%), white (n = 383, 93.2%) with a mean ± SD age of 63.07 ± 11.53 years and an average time since treatment of 34.8 ± 63.22 months. The most common tumor site was oropharynx (n = 200, 48.7%), followed by oral cavity (n = 115, 28.0%), and larynx/hypopharynx (n = 96, 23.3%). The majority of patients presented with an advanced stage at diagnosis (n = 256, 63.2%). Non-surgical intervention (n = 166, 34.0%) and surgery with adjuvant treatment (n = 197, 54.3%) were more common than surgery alone (n = 48, 11.7%). Demographic and clinical characteristics of the included patient population are summarized in Table 1.

Table 1

Demographic and clinical characteristics (n = 411)
Variables	M ± SD	n(%)
Age, y	63.07 ± 11.53
Gender
Female		91 (22.1)
Male		320 (77.9)
Race
White		383 (93.2)
Other		28 (6.8)
Tumor Site
Oral Cavity		115 (28.0)
Oropharynx		200 (48.7)
Larynx/Hypopharynx		96 (23.3)
Tumor Stage
Early		149 (36.8)
Advanced		256 (63.2)
Treatment Modality
Surgery Alone		48 (11.7)
Surgery + Adjuvant		197 (54.3)
Non-Surgical		166 (34.0)
HPV Status
Positive		173 (42.1)
Negative		36 (8.8)
NA		22 (5.3)
Unknown		180 (43.8)
NDI Category
None		141 (34.3)
Mild		170 (41.4)
Moderate to complete		100 (24.3)
Time Since Treatment, m	34.8 ± 63.22

Table 2 shows the insomnia distribution divided into three categories, no insomnia (≤ 7 points), subthreshold insomnia (8–14 points), and clinical insomnia (≥ 15 points). Mean ISI score was 7.09 ± 6.66 (range =0–28). The majority had no reported insomnia (n =253, 61.6%) followed by subthreshold insomnia (n = 95, 23.1%) and clinical insomnia (n = 63, 15.3%). For the analysis, questions about the impact of sleep in the NDI were removed. Mean NDI score was 8.83 ± 8.06 (range = 0–38). Neck disability distribution (mean ± SD) is reported in Table 1. Perceived neck disability was associated with an increase in insomnia severity (p < 0.001) from those with no reported insomnia (NDI score 5.86 ± 6.01), subthreshold insomnia (NDI score 13.34 ± 8.03), and clinical insomnia (NDI score 20.00 ± 9.23) seen in Fig. 2. The association between all NDI sections and the insomnia categories were also evaluated. An increase in severity across all sections was associated with higher reported insomnia symptoms (p < 0.001) as seen in Table 3.

Table 2

Insomnia Severity Distribution
	Insomnia Severity Category
	None (n = 253)	Subthreshold (n = 95)	Clinical (n = 63)	p-value
Age, y	63.93 ± 11.98	61.88 ± 11.29	61.4 ± 9.73	0.059
Gender				0.414
Female	202 (63.13)	67 (20.94)	51 (15.94)
Male	51 (56.04)	28 (30.77)	12 (13.19)
Race				0.128
White	238 (62.14)	91 (23.76)	54 (14.1)
Other	15 (53.57)	4 (14.29)	9 (32.14)
Tumor Site				0.380
Oral Cavity	74 (64.35)	28 (24.35)	13 (11.3)
Oropharynx	120 (60)	50 (25)	30 (15)
Larynx/Hypopharynx	59 (61.46)	17 (17.71)	20 (20.83)
Tumor Stage				0.470
Early	88 (59.06)	37 (24.83)	24 (16.11)
Advanced	161 (62.89)	57 (22.27)	38 (14.84)
Treatment Modality				0.592
Surgery Alone	31 (64.58)	13 (27.08)	4 (8.33)
Surgery + Adjuvant	124 (62.94)	42 (21.32)	31 (15.74)
Non-Surgical	98 (59.04)	40 (24.1)	28 (16.87)
HPV Status				0.462
Positive	102 (58.96)	42 (24.28)	29 (16.76)
Negative	25 (69.44)	7 (19.44)	4 (11.11)
NA	15 (68.18)	6 (27.27)	1 (4.55)
Unknown	111 (61.67)	40 (22.22)	29 (16.11)
NDI Category				< 0.0001
None	130 (92.2)	10 (7.09)	1 (0.71)
Mild	101 (59.41)	49 (28.82)	20 (11.76)
Moderate to complete	22 (22)	36 (36)	42 (42)
Time Since Treatment, m	38.94 ± 66.6	31.68 ± 58.19	22.86 ± 55.17	0.069

Table 3

Insomnia severity across individual neck disability index sections
		Insomnia Severity Category
		None	Subthreshold Insomnia	Clinical Insomnia	p-value
Neck Disability Index Sections	SECTION 1 - PAIN INTENSITY	0.61 ± 0.88	1.41 ± 1.16	1.84 ± 1.25	< 0.001
	SECTION 2 - PERSONAL CARE	0.28 ± 0.86	0.66 ± 1.14	1.33 ± 1.32	< 0.001
	SECTION 3 - LIFTING	1.23 ± 1.66	1.84 ± 1.65	2.6 ± 1.75	< 0.001
	SECTION 4 - WORK	1.19 ± 1.46	2.14 ± 1.48	3.03 ± 1.46	< 0.001
	SECTION 5 - HEADACHES	0.36 ± 0.73	1.03 ± 1.07	1.46 ± 1.42	< 0.001
	SECTION 6 - CONCENTRATION	0.36 ± 0.72	0.97 ± 0.96	1.48 ± 1.37	< 0.001
	SECTION 7 - SLEEPING	0.55 ± 0.81	2.36 ± 1.18	3.44 ± 1.35	< 0.001
	SECTION 8 - DRIVING	0.43 ± 1.06	0.98 ± 1.37	1.93 ± 2.02	< 0.001
	SECTION 9 - READING	0.29 ± 0.74	0.75 ± 1.14	1.13 ± 1.43	< 0.001
	SECTION 10 - RECREATION	0.58 ± 1.04	1.22 ± 1.42	1.81 ± 1.64	< 0.001

Ordinal regression analysis demonstrated that neck disability severity is directly associated with insomnia severity after controlling for age, race, treatment modality, tumor site and stage, and time since treatment. The odds of a survivor reporting insomnia was 8.65 times higher in those with mild neck disability (95% OR (4.31, 17.37), p < 0.001) and 48.12 times higher in those with moderate to complete neck disability (95% OR (22.35, 103.58), p < 0.001) than those who report no disability. No association was seen between age (p = 0.669), treatment modality between surgical intervention and surgical with adjuvant (p = 0.450) or non-surgical intervention (p = 0.213), tumor site between oral cavity and oropharynx (p = 0.578), or larynx/hypopharynx (p = 0.616), stage (p = 0.176), or time since treatment (p = 0.966). The results of the multivariable analysis are summarized in Table 4. When examining those over 6 months post-treatment (n = 180), odds of a survivor reporting insomnia was 3.03 times higher in those with moderate neck disability (95% OR (1.18, 8.07), p = 0.022) than those who report no disability, though for those with mild disability no significant relationship was found, as seen in Table 5.

Table 4

Multivariable ordinal regression model on the associations between demographic and clinical characteristics and insomnia
Variables		Odds Ratio (95% CI)	p-value
Age, y		1.00 (0.98, 1.02)	0.669
Treatment Type	Surgery Alone	(Base)
	Surgery + Adjuvant	1.35 (0.63, 2.90)	0.450
	Non-Surgical	1.71 (0.75, 3.91)	0.213
Tumor Site	Oral Cavity	(Base)
	Oropharynx	1.20 (0.62, 2.31)	0.578
	Larynx/Hypopharynx	1.17 (0.58, 2.37)	0.616
Tumor Stage	Early	(Base)
Tumor Stage	Advanced	0.68 (0.40, 1.18)	0.176
Neck Disability	None	(Base)
	Mild	8.65 (4.31, 17.37)	< 0.0001
	Moderate to Complete	48.12 (22.35, 103.58)	< 0.0001
Time Since Treatment, m		1.00 (1.00, 1.00)	0.966

Table 5

Multivariable ordinal regression model on the associations between demographic and clinical characteristics and insomnia for survivors > 6 months post-treatment(n = 180).
Variables		Odds Ratio (95% CI)	p-value
Age, y		0.99 (0.96, 1.02)	0.592
Treatment Type	Surgery Alone	(Base)
	Surgery + Adjuvant	0.57 (0.21, 1.60)	0.290
	Non-Surgical	0.59 (0.19, 1.77)	0.345
Tumor Site	Oral Cavity	(Base)
	Oropharynx	0.62 (0.24, 1.56)	0.307
	Larynx/Hypopharynx	0.64 (0.22, 1.84)	0.411
Tumor Stage	Early	(Base)
Tumor Stage	Advanced	1.64 (0.77, 3.52)	0.201
Neck Disability	None	(Base)
	Mild	1.69 (0.68, 4.21)	0.260
	Moderate to Complete	3.03 (1.18, 8.07)	0.022
Time Since Treatment, m		1.00 (0.99, 1.01)	0.227

Neck disability and insomnia contribute to a large number of physical, social, and psychological outcomes for individuals. Our study contributes to a growing body of literature regarding the relationships between post-treatment outcomes and the relationship between physical and psychological health in HNC survivors. We found a strong association between symptoms of neck disability and insomnia severity within the HNC survivor population.

While sleep disturbance has been demonstrated in HNC populations before and during treatment, the underlying cause is not well established. There are numerous ways in which sleep is affected among survivors, including hypersomnolence, sleep-related breathing disorders, xerostomia contributing to increased water intake and nocturnal diuresis, and insomnia. Kim et al. established that those who experience high-intensity neck pain and comorbid musculoskeletal pain were strongly associated with clinical insomnia for patients [59]. Our results support not only the association between neck pain and insomnia, but an association between all items in the neck disability index, including impairments in work, concentration, personal care, and recreational activity with increasingly severe insomnia symptoms.

This association extends from the acute post-treatment phase across all reported neck disability severities to late and long-term outcomes in those with moderate or severe neck disability. This may be due in part to physical impairment limiting exercise, activities of daily living, and social interaction contributing to a cluster of psychological outcomes such as depression and anxiety, which are highly correlated with insomnia in other settings [60–63]. Those who experience psychological symptoms such as insomnia also report more severe pain and physical impairment [61, 64, 65]. Likely, the outcomes closely interact, and the facilitation of care can lead to drastic improvements in the survivor’s QOL. Our results suggest that the association between reported neck and insomnia symptoms decreases long-term for many survivors with mild symptoms. Those with severe neck symptoms may continue to have related insomnia, though our study is limited to a single point in time. These results may partly be due to the impact of the acute symptoms of treatment contributing to insomnia and neck disability or those survivors' recovery or adaptation to their symptoms. Those survivors who report moderate or higher neck disability after six months are still significantly more likely to report more severe insomnia symptoms suggesting target areas for improving patient outcomes and well-being in survivorship initiatives. Ridner et al. have previously shown that fibrosis in HNC survivors may increase over time after 12 months post-treatment, which may explain part of this dissociation with neck disability increasing in severity over time where insomnia symptoms may remain stable or improve in mild to moderate cases [66].

Understanding the relationship between post-treatment symptoms helps guide therapy to improve survivor well-being. Physical therapy and activity are shown to improve neck disability symptoms [67, 68]. Additionally, increased activity leads to dramatic QOL improvements in individuals with insomnia, suggesting that a dual therapy focused on neck range of motion and maintenance of muscle mass with exercise may improve the survivors’ lives across a spectrum of outcomes [69–71]. The high reports of pain and increased physical symptoms in those with insomnia additionally support the use of a multidisciplinary approach to symptom management and the involvement of specialists for cognitive behavior therapy and early psychiatric intervention to mitigate the onset of physical symptoms and reduce the pain burden of survivors [59, 72–74]. Our results show the interaction between these two post-treatment outcomes can contribute to a poor QOL for survivors, evidence of the need for early screening for insomnia and neck pain in the survivorship population allowing for timely referral and therapeutic intervention. Given the potential bidirectional relationship between neck disability and insomnia, future studies should examine the impact of insomnia treatment among HNC survivors on these outcomes.

Our study explores the relationship between patient-reported physical symptoms following HNC treatment and insomnia in the survivorship population. While a causal relationship cannot be established due to lack of longitudinal follow-up, the inclusion of survivors across a broad range of age, tumor site and stage, varying treatment modality, and time since treatment contribute to results generalizable to a broad HNC survivor population. While patient-reported insomnia was recorded, the prevalence of sleep disorders such as hypersomnolence or sleep apnea was not investigated.

More significant neck pain and related physical limitations is associated with increasing severity of insomnia in the HNC survivorship population. Though the interaction between neck disability and insomnia is yet to be fully elucidated, this relationship between physical impairment and reduced psychosocial well-being is supported by other studies and identifies areas that can be targeted for intervention to improve the QOL of cancer survivors. To improve long-term prognosis, HNC providers should consistently identify those survivors experiencing a higher symptom burden. This supports the need for a multidisciplinary care model for post-treatment HNC survivors to facilitate screening, access to care, and early intervention for the well-being of survivors. Additional research to characterize trajectory, therapeutic intervention, and time since treatment may help to further understand the relationship between neck disability and insomnia.

Funding: N/A

Conflicts of interest/Competing interests: N/A

Ethics approval: This study was approved by the University of Pittsburgh’s Human Research Protection Office (IRB no: STUDY20050058). The procedures used in this study adhere to the tenets of the Declaration of Helsinki.

Consent to participate: N/A

Consent for publication: N/A

Availability of data and material: The data that support the findings of this study are available from the corresponding author, MLN, upon reasonable request.

Code availability: N/A

Authors' contributions: All authors, Harris, Li, Atchison, Soose, Piva, Imes, Johnson, and Nilsen contributed to the study conception and design. Material preparation, data collection and analysis were performed by Alexandria Harris, Jinhong Li, Karley Atchison, and Marci Nilsen.The first draft of the manuscript was written by Alexandria Harris and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Acknowledgement: N/A

Conflicts of Interest: The authors have no relevant financial or non-financial interests to disclose.

Funding: The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

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Neck Disability and Insomnia in Head and Neck Cancer Survivors

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Neck Disability Index

Insomnia Severity Index

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