Postural stability using different neck positions in normal subjects and patients with neck trauma

Subjects with neck problems, such as whiplash injuries, often complain of disturbed equilibrium and, in some instances, provocation of the neck position can elicit such problems. The importance of neck proprioceptors for maintaining balance is gaining increased interest, moreover the function or malfunction of the otoliths may disturb equilibrium in certain head positions. The aim of the study was to create a reference material for postural control and its dependence on head position in healthy subjects and to compare this with a set of patients with known neck problems and associated vertiginous problems. A total of 32 healthy subjects (16 men, 16 women, age range 21-58 years) as well as 10 patients age range 27-62 years (mean 44 years) with neck problems and associated balance problems since a whiplash injury were tested for postural control using the EquiTest dynamic posturographic model. The normal subjects were initially split into four age groups in order to estimate the effects of age on performance. The postural stability was evaluated for dependence of support surface conditions (stable or sway-referenced), visual input (eyes open or closed) and head position (neutral, left rotated, right rotated, extended backwards or flexed forward) using analysis of variance (ANOVA) with Tukey's post hoc test in case of a significant factor effect. As expected, visual cues as well as stable support surface improve postural stability (p < 0.001). Postural stability is statistically different in the head extended backwards condition compared with the other four head positions (p < 0.001 in all cases) in both patients and controls. Eliminating this test condition from the analysis, only a slight (p < 0.05) difference between head forwards and head turned left remained. This pattern of results remained if the normal subjects were only split into two age groups instead of four. Finally, the patient group exhibited significantly lower postural performance than all the groups of normal subjects (p <0.01), but none of the normal groups differed significantly from each other. It is concluded that the postural control system is significantly challenged in the head extended backwards condition in both normal subjects and patients with previous whiplash injury and persistent neck problems. The patient group differed statistically from all groups of normal subjects. This suggests that neck problems impair postural control, and that the head extended position is a more challenging task for the postural system to adapt to. Whether this is due to utricular malpositioning, central integrative functions or cervical proprioceptive afferents is not within the scope of this study to answer.     

Influence of Neck Proprioception on Vibration-induced Postural Sway

Objective --Several reports have shown that the direction of the postural responses induced by vestibular stimulation is affected by the positions of the neck and torso. The aim of this study was to investigate whether the postural responses to vibratory proprioceptive stimulation of the calf muscles are affected by the position of the head and thus by proprioceptive and vestibular information from the neck and head. Material and Methods --Ten normal subjects were exposed to vibratory proprioceptive stimulation of the calf muscles when the head was maintained in five different positions: in a neutral position facing forwards, with the head turned to the right or left sides or with the head tilted backwards or forwards. Body movements were evaluated by analyzing the anteroposterior and lateral torques induced towards the supporting surface. Results --The analysis showed that only the anteroposterior body sway was significantly affected by the position of the head. The anteroposterior postural responses were primarily increased during the tests with the head tilted backwards or forwards, whereas the postural responses were unaffected by head torsion towards the sides. The lateral responses were primarily affected by vision and not by the position of the head. Conclusion --The findings suggest that the responses evoked by vibratory proprioceptive stimulation of the calf muscles may be affected by different mechanisms, either by purely proprioceptive information or by an interaction between proprioceptive and vestibular information. Moreover, the increasing difference between the test conditions over time suggests that fatigue of the neck muscles may be one of the factors affecting the responses induced by the perturbations.     

Direction of Galvanically-induced Vestibulo-postural Responses during Active and Passive Neck Torsion

The direction of a postural response induced by galvanic vestibular stimulation depends on the head and trunk position. The relative importance of afferent information (proprioception) and efferent motor command/corollary discharge is unknown. We studied the direction of body sway evoked by galvanic vestibular stimulation in 9 healthy subjects during active and passive head positioning at 0° frontal position, 35° to the left, and 75° to the right, using a custom-built collar. At 0° and 75° there were no significant differences in sway direction between active and passive head positioning. The galvanic stimulation invoked sway toward the anode, mainly in the inter-aural direction. The sway direction differed significantly between active and passive positioning at 35° to the side (p&lt;0.05). When the head was actively kept in this position, the body sway was mainly in an inter-aural direction. The sway shifted to a naso-occipital direction when the head was passively positioned at 35°. Our results indicate that the afferent proprioceptive information has the largest influence on the direction of the galvanically-induced postural response, although some dependence on efferent motor commands and non-linear cervical proprioception cannot be ruled out entirely.     

Influence of neck proprioception on vibration-induced postural sway

OBJECTIVE: Several reports have shown that the direction of the postural responses induced by vestibular stimulation is affected by the positions of the neck and torso. The aim of this study was to investigate whether the postural responses to vibratory proprioceptive stimulation of the calf muscles are affected by the position of the head and thus by proprioceptive and vestibular information from the neck and head. MATERIAL AND METHODS: Ten normal subjects were exposed to vibratory proprioceptive stimulation of the calf muscles when the head was maintained in five different positions: in a neutral position facing forwards, with the head turned to the right or left sides or with the head tilted backwards or forwards. Body movements were evaluated by analyzing the anteroposterior and lateral torques induced towards the supporting surface. RESULTS: The analysis showed that only the anteroposterior body sway was significantly affected by the position of the head. The anteroposterior postural responses were primarily increased during the tests with the head tilted backwards or forwards, whereas the postural responses were unaffected by head torsion towards the sides. The lateral responses were primarily affected by vision and not by the position of the head. CONCLUSIONS: The findings suggest that the responses evoked by vibratory proprioceptive stimulation of the calf muscles may be affected by different mechanisms, either by purely proprioceptive information or by an interaction between proprioceptive and vestibular information. Moreover, the increasing difference between the test conditions over time suggests that fatigue of the neck muscles may be one of the factors affecting the responses induced by the perturbations.     

Neck Muscle Vibration Alters Visually Perceived Roll in Normals

The objective of this study was to determine whether vibration of dorsal neck muscles or of the mastoid bone or of both modified the perception of visual orientation in the head roll-tilt plane in normal subjects. Measurements of the subjective visual vertical (SVV) were obtained from 26 normal human subjects. Subjects reported the SVV in the upright and in the left and right 30° static head roll-tilt positions. Subjects then reported the SVV while vibration was applied to the left or right dorsal neck or left or right mastoid. Both head position and vibration independently modified settings of the SVV. In head-tilted positions, vibration of the upper dorsal neck muscles (on the side of the head opposite to the head tilt) caused a significantly greater shift of the SVV in the opposite direction of head roll-tilt compared to vibration of the lower dorsal neck muscles or of the mastoid. These results support a role for cervical somatosensory information in perception of visual orientation in the roll plane. Our findings may help explain the differences observed in visual orientation perception in normal subjects between head alone and whole-body roll-tilt. Finally, vibration of neck muscles in the head roll-tilted plane may be a useful method to test cervical somatosensory function possibly by increasing their response to external stimulation. The views expressed in this article are those of the author and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, nor the U. S. Government.     

Observation of Vestibular Asymmetry in a Majority of Patients over 50 Years With Fall-Related Wrist Fractures

Previously, we have observed vestibular asymmetry in about one-third of healthy senior citizens and in about two-thirds of subjects with previous hip fractures and no other significant ailments. Wrist fractures are considered a harbinger of hip fractures. If vestibular asymmetry is correlated with falls and fractures among the elderly then it should also be reflected among subjects with wrist fractures. Sixty-six consecutive patients (mean age 67.8 years) who had sustained a fall-related wrist fracture during a 10-month period were included in the study. The frequency of head shake nystagmus among the patients was compared to that found among 49 healthy senior citizens (mean age 74.9 years). Nystagmus after head shaking, indicating asymmetric vestibular function, was found in 50 participants (76%) (p &lt;0.001). Thirty-eight of these were graded with distinct or prominent nystagmus responses. Sixty percent of the subjects with horizontal nystagmus had a wrist fracture coinciding with the slow phase of nystagmus. Twenty-three subjects reported 30 previous fall-related fractures during the previous 10 years. Subjects with nystagmus after head shaking sustained 26 of these fractures. The frequency of signs of vestibular asymmetry was significantly higher (p &lt;0.001) among the subjects than among healthy senior citizens. These findings suggest that an asymmetric vestibular function could be an epidemiologically important contributory factor to falls and wrist fractures among the elderly population.     

Neck dissection for non-squamous malignancy

Of 1030 patients who underwent neck dissection (radical, modified or selective) in a 27-year period 103 had malignant neck nodes from a primary site in the head and neck with a histological diagnosis other than squamous carcinoma. There were 71 men and 32 women in this group with a mean age of 55 years. 28 patients had neck dissection as part of their initial treatment and 75 for later nodal recurrence. Five-year survival was 52% (40-63%). Survival was site dependent, best for thyroid tumours and worst for tumours of the major salivary glands (χ2/1 = 6.52, P < 0.05). Histology significantly affected survival, best for papillary tumours and worst for melanoma and undifferentiated tumours (χ2/1 = 3.85, P < 0.05). Survival was worse with advanced N stage but varied little with node level. The number of nodes invaded had a highly significant effect on survival (χ2/1= 23.94, P < 0.001), but extracapsular rupture had no effect. Advanced T stage at the time of surgery had a significant adverse effect on survival using univariate analysis, but this effect disappeared using multivariate analysis. In the 75 patients who had neck dissections for nodal recurrence the presence of a simultaneous recurrence at the primary site had no significant effect on survival. These patients had a better 5-year survival than patients having neck dissection for squamous disease, but the usual predictors of survival in squamous carcinoma do not always apply to non-squamous malignancy. Keywords head and neck cancer non-squamous neck dissection survival     

Osteosarcoma of the Head and Neck: Meta-analysis of Nonrandomized Studies

To assess the role of adjuvant therapy in the treatment of osteogenic sarcoma of the head and neck, treatment and survival information from 173 patients with osteosarcoma of the head and neck was entered into a database. A meta-analysis of the data was attempted with primary emphasis on the effect of adjuvant therapy on disease outcome. The overall 5-year survival was 37%. Patients with mandibular and maxillary tumors had similar survival rates; both groups fared significantly better than patients with extragnathic tumors (P<0.001). Treatment with surgery alone was associated with significantly longer survival rates (P<0.03) than surgery with adjuvant therapy. In the majority of patients reported, information about surgical margins was not available. For this reason, the differences may not adequately represent the effect of adjuvant therapy. While there have been encouraging results with adjuvant treatment protocols for long bone osteosarcoma, the ultimate role of radiation and chemotherapy in the management of osteosarcoma of the head and neck remains unproven. Nevertheless, we recommend that adjuvant therapy be considered due to the poor prognosis in osteosarcoma of the head and neck.     

Validation of the Charlson Comorbidity Index in Patients With Head and Neck Cancer: A Multi-institutional Study

Comorbid conditions are medical illnesses that accompany cancer. The impact of these conditions on the outcome of patients with head and neck cancer is well established. However, all of the comorbidity studies in patients with head and neck cancer reported in the literature have been performed using the Kaplan-Feinstein index (KFI), which may be too complicated for routine use. This study was performed to introduce and validate the use of the Charlson comorbidity index (CI) in patients with head and neck cancer and to compare it with the Kaplan-Feinstein comorbidity index for accuracy and ease of use. Study design was a retrospective cohort study. The study population was drawn for three academic tertiary care centers and included 88 patients 45 years of age and under who underwent curative treatment for head and neck cancer. All patients were staged by the KFI and the CI for comorbidity and divided into two groups based on the comorbidity severity staging. Group 1 included patients with advanced comorbidity (stages 2 or 3), and group 2 included those with low-level comorbidity (stages 0 or 1). Outcomes were compared based on these divisions. The KFI was successfully applied to 80% of this study population, and the CI was successfully applied in all cases ( P < 0.0001). In addition, the KFI was found to be more difficult to use than the CI ( P < 0.0001). However, both indices independently predicted the tumor-specific survival ( P = 0.007), even after adjusting for the confounding effects of TNM stage by multivariate analysis. Overall, the CI was found to be a valid prognostic indicator in patients with head and neck cancer. In addition, because comorbidity staging by the CI independently predicted survival, was easier to use, and more readily applied, it may be better suited for use for retrospective comorbidity studies.     

站立于海绵垫及坚硬平板时头部后仰对正常人姿势稳定性的影响

目的探讨对正常青年进行姿势描记时,不同站立条件下头部后仰对其姿势稳定性的影响。方法对34名健康青年人进行四种站立条件下的姿势描记仪检查,分别为:①站立于坚硬平板、头部直立;②坚硬平板、头部后仰50￣55°;③海绵垫、头部直立;④海绵垫、头部后仰50￣55°。每种条件下分别测试睁眼和闭眼时的姿势稳定性,采用身体重心晃动速度(swayvelocity,SV)为研究参数。结果(1)头部直立时,站立于海绵垫与站立于坚硬平板上身体重心SV比较,睁眼时(t=15.484,P<0.001)和闭眼时(t=19.302,P<0.001)均有显著增加。(2)睁眼时,在两种站立平面上,头部直立和后仰时SV间比较,差异无显著性意义(坚硬平板和海绵垫平面上的P值分别是0.083和0.616);而闭眼时,无论站立平面条件如何,头部后仰时SV均显著高于头部处于直立位时(P值均小于0.001);(3)闭眼时头部后仰引起的SV增加程度,站于海绵时高于站于坚硬平板时(t=5.757,P<0.001)。结论人体本体觉受到干扰时,其静态平衡姿势稳定性降低;正常青年人闭眼同时头部后仰可使姿势稳定性降低,且头部后仰可能使机体对本体觉的依赖增加。     

Resource Utilization and Patient Morbidity in Head and Neck Reconstruction

Many papers have addressed the technical aspects of free tissue transfer in head and neck cancer patients. However, there has not been a critical assessment of the impact of free tissue transfer on resource utilization and patient morbidity compared with pedicle flap reconstructions. Two cohorts of patients derived from 245 consecutive reconstructions were tightly matched by age, site, stage, and histology, yielding 44 patient pairs differing in method of reconstruction. Patients undergoing free flap reconstruction spent more time in the operating room than those reconstructed with pedicled flaps (993 min vs. 777 min, P < 0.0001). The group with free flap reconstruction spent fewer days in the surgical intensive care unit and hospital (2 days vs. 2.5 days; 18.5 days vs. 22.6 days). This difference is attributed to the paucity of postoperative complications in the group with free flap reconstruction (fistula formation 4.5% vs. 21%, P < 0.04). These data indicate that the continued use of sophisticated reconstructive techniques in head and neck cancer patients is economically sound as assessed by patient morbidity and resource utilization.     

Vestibular and stabilometric findings in whiplash injury and minor head trauma

Vertigo and postural instability following whiplash and/or minor head injuries is very frequent. According to some authors, post-whiplash vertigo cannot be caused by real injury to vestibular structures; other authors maintain that vestibular damage is possible even in the case of isolated whiplash, with vascular or post-traumatic involvement. Furthermore, many of the balance disorders reported after trauma can be justified by post-traumatic modification to the cervical proprioceptive input, with consequent damage to the vestibular spinal reflex. The aim of this study was to evaluate the vestibular condition and postural status in a group of patients (Group A, n = 90) affected with balance disorders following whiplash, and in a second group (Group B, n = 20) with balance disorders after minor head injury associated with whiplash. Both groups were submitted to videonystagmography (VNG) and stabilometric investigation (open eyes - O E, closed eyes - CE, closed eyes with head retroflexed - CER) within 15 days of their injuries and repeated within 10 days after conclusion of cervical physiotherapy treatment. The VNG tests revealed vestibulopathy in 19% of cases in Group A (11% peripheral, 5% central, 3% in an undefined site) and in 60% of subjects in Group B (50% peripheral, 10% central). At the follow-up examination, all cases of non-compensated labyrinth deficit showed signs of compensation, while there were two cases (2%) in Group A and one case (5%) in Group B of PPV. As far as the altered posturographic recordings are concerned, while there was no specific pattern in the two groups, they were clearly pathologic, especially during CER. Both in OE and in CE there was an increase in the surface values and in those pertaining to shifting of the gravity centre on the sagittal plane, which was even more evident during CER. In Group A, the pre-post-physiotherapy comparison of CER results showed that there was a statistically significant improvement in the majority of the parameters after treatment. Moreover, in Group B there was frequent lateral shifting of the centre of gravity that was probably linked with the high percentage of labyrinth deficits. The comparison between the first and second stabilometric examinations was statistically significant only in those parameters referring to gravity centre shifting on the frontal plane, which was probably due to the progressive improvement in the associated vestibulopathy rather than to the physiotherapy treatment performed for the cervical damage. Hence, our study confirms that only in a minority of cases can whiplash cause central or peripheral vestibulopathy, and that this is more probable after minor head injury associated with whiplash. In addition, our data confirm that static stabilometry is fundamental for assessing postural deficits following a cervical proprioceptive disorder. In these cases, in fact, analysis of the different parameters and the indices referring to cervical interference not only permits evaluation of altered postural performance, but also detects and quantifies destabilisation activity within the cervical proprioceptive component.     

The influence of the cervical proprioception on the postural reflexes--experimental and clinical study

The aim of the study was to estimate the effect of the neck proprioception on the postural reflexes in the cases of the cervical pathology in the whiplash injury and degenerative disease of the cervical vertebral column. The investigation using ENG and stabilometry was performed in 81 patients. Experimental observations were done among 10 pigeons with limitation of the neck proprioceptors action by special neck tutor. Their postural reflexes were analysed during balance test on the seesaw. Our conclusion is, that disorders of the proprioceptors impulastion can damage the postural reflexes even in patients with normal labyrinth function.     

Neck Dissections: Predicting Postoperative Drainage

Objectives Most head and neck dissections performed in conjunction with carcinomas of the upper aerodigestive tract require drain insertion. The time that the drains remain in place largely determines the duration of postoperative hospitalization. This study sought to retrospectively compare different neck dissections in terms of postoperative drainage and duration of hospitalization. We also sought to identify any correlation between total intraoperative blood loss and postoperative drainage. Materials and Methods Radical, modified radical, and selective neck dissections performed in conjunction with resection of a carcinoma of the upper aerodigestive tract over a 3‐year period were evaluated. Total intraoperative blood loss at surgery, and amount and duration of postoperative drainage for each neck dissection were recorded. Results Seventy‐nine neck dissections were performed on 52 patients, 27 (52%) of whom had bilateral neck dissections. Median drainage was 116.5 mL, 172 mL, and 319 mL for selective, modified radical, and radical neck dissections, respectively. Drainage differed significantly by type of neck dissection (P <.001). Drains remained in place a median of 4 days with no significant difference between different types of neck dissections. Drainage was clearly correlated with total intraoperative blood loss (Spearman correlation = 0.44, P <.001). Conclusion The postoperative drainage per day was higher in radical neck dissections than modified radical neck dissections and lowest in selective neck dissections. This difference was not reflected in the duration that the drains would remain in place. Total intraoperative blood loss is a strong predictor of the amount and duration of postoperative drainage.     

Influence of Vibration to the Neck,Trunk and Lower Extremity Muscles on Equilibrium in Normal Subjects and Patients with Unilateral Labyrinthine Dysfunction

To investigate the role of proprioceptors of different skeletal muscles in postural control, in normal subjects and patients with unilateral labyrinthine dysfunction (ULD), the effect of vibration on these muscles was studied by postulography. The subjects comprised 59 normal subjects and 12 patients with ULD due to resection of acoustic tumours. Sagittal body sway was observed during vibration to the triceps surae, tibialis anterior and upper dorsal neck muscles. No significant change in sway was observed in the frontal plane in normal subjects. Significant differences between normal subjects and patients were found on stimulation of the muscle groups of triceps surae and biceps femoris during vibration. In patients with ULD, vibration to the dorsal neck muscles caused a deviation towards the diseased side. It can be speculated that the upper dorsal neck muscle plays an important role in maintaining the body balance in the frontal plane in patients with ULD. On the other hand, the lower extremity muscles, especially the muscles on the dorsal side of the body, play a significant role in adjusting the standing posture in the sagittal plane.     

Polymorphism of Methylenetetrahydrofolate Reductase (MTHFR) gene and risk of Head and Neck Squamous Cell Carcinoma

Methylenetetrahydrofolate reductase gene (MTHFR) C677T polymorphism may be a risk factor for head and neck squamous cell carcinoma due to changes in folate levels that can induce disorders in the methylation pathway, which results in carcinogenesis.AimTo evaluate MTHFR C677T polymorphism in patients with head and neck squamous cell carcinoma and in individuals with no history of cancer, and to assess the association of this disease with clinical histopathological parameters.Series and MethodsA retrospective study that assessed gender, age, tobacco, alcohol consumption and clinical histopathological parameters in 200 patients (100 with disease and 100 with no history of cancer). PCR-RFLP molecular analysis was carried out and the chi-square test and multiple logistic regression were applied for the statistical analysis.ResultsThere was no association between MTHFR C677T polymorphism and head and neck cancer (p = 0.50). Significant differences between the study and control groups were observed at age over 50 years, tobacco use, and male gender (p <0.001). There was no association of disease with clinical-histopathological parameters.ConclusionNo association between the MTHFR C677T polymorphism and head and neck squamous cell carcinoma was possible in this study.     

Motion sickness susceptibility associated with visually induced postural instability and cardiac autonomic responses in healthy subjects

Conclusions This study supports the hypothesis that postural sway and autonomic responses to moving visual stimuli may be associated with motion sickness susceptibility. Characteristics of the cardiac sympathovagal balance during exposure to provocative stimulation may be a marker of individual susceptibility to motion sickness.

Objective To assess the relationship between postural and autonomic responses to a simulated visual motion environment and reported susceptibility to motion sickness.

Material and methods Fifteen healthy subjects were exposed to sinusoidally oscillating visual motion in roll at frequencies of 0.1–0.4 Hz. Recordings were made of postural sway and respiratory frequency and electrocardiograms were obtained from which heart rate variability (HRV) was computed in order to probe cardiac sympathetic and parasympathetic activity.

Results In subjects with a low susceptibility to motion sickness as rated using a standardized questionnaire, there was no significant effect of visual stimulus on postural sway or HRV at any frequency of motion. Subjects with a high susceptibility to motion sickness showed significant postural instability induced by visual stimuli (p<0.01). Visual stimuli presented at a frequency of 0.1 Hz significantly increased the low-frequency power (LF) of HRV, decreased the high-frequency power (HF) of HRV and increased the LF:HF ratio in these subjects (p<0.05).     

Effect of head position on vestibular evoked myogenic potentials with toneburst stimuli

Conclusion. The present study demonstrated the robustness of VEMP testing with toneburst stimuli, since it is hardly affected by head position, i.e. base or tonic excitation levels of the saccule and inferior vestibular nerve. However, the small but highly significant difference found in latency should not be neglected: the gravitational axis in the upright position may have some special effect on tonic excitation of the saccule. Objectives. To evaluate the effect of head positions on vestibular evoked myogenic potentials (VEMPs) with toneburst stimuli. Materials and methods. VEMPs were recorded with short tonebursts of 500 Hz in 14 normal subjects in 5 head positions (upright, nose up, ear up, nose down, and ear down). The three parameters analyzed were: 1) latency of p13, 2) latency of n23, and 3) corrected amplitude of p13-n23 (CA p13-n23). Results. One-way repeated measures ANOVA showed significant effects on both p13 (p=0.0245) and n23 (p<0.0001) latencies, but not on CA p13-n23. Bonferroni's post hoc test demonstrated that there were significant differences in n23 latency between the upright position and all other head positions leaning on the bed.     

The Role of Neck Dissection in the Treatment of Supraglottic Laryngeal Cancer

Objectives - Vestibular compensation, the recovery that follows unilateral vestibular deafferentation (UVD), is a model for central nervous system plasticity. Recovery from the static symptoms of UVD may involve temperature-dependent processes that modulate the immediate effects of UVD and/or the capability of the central nervous system to undergo adaptive plasticity. In this study we investigated changes in oculomotor and postural vestibular symptoms resulting from low body temperature during UVD. Material and methods - To study the effect of low temperatures at the time of UVD on vestibular compensation, we compared the rate of compensation and peak values for postural [roll head tilt (RHT) and yaw head tilt (YHT)] and oculomotor [spontaneous nystagmus (SN)] symptoms in three groups of guinea pigs. Animals in Group 1 (n=6) were maintained at 38°C throughout unilateral labyrinthectomy (UL). Animals in Group 2 (n=6) were not temperature-controlled and animals in Group 3 (n=4) were cooled with ice to 25°C throughout UL. Results - Cooled animals showed significantly higher rates of SN upon recovery from anaesthesia and took a significantly longer time to compensate. Cooled animals were also slower to compensate for postural symptoms (RHT and YHT), with 2 animals showing no compensation for RHT 52 h after UL. Conclusion - Hypothermia (25°C) during UVD surgery exacerbates postural and oculomotor symptoms following UL and significantly slows recovery.