Predicting extended hospital stay after deep brain stimulation surgery in Parkinson’s patients

Journal of Clinical Neuroscience xxx (xxxx) xxx

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Clinical study

Predicting extended hospital stay after deep brain stimulation surgery in Parkinson’s patients Nicole A. Young a,c,⇑,1, Matthew P. Brown b,c,1, Juan Peng d, David Kline d, Carson Reider c, Milind Deogaonkar b,c a

Department of Neuroscience, Center for Neuromodulation, The Ohio State University Wexner Medical Center, Columbus, OH, USA Department of Neurological Surgery, Center for Neuromodulation, The Ohio State University Wexner Medical Center, Columbus, OH, USA Neuroscience Research Institute, The Ohio State University Wexner Medical Center, Columbus, OH, USA d Center for Biostatistics, The Ohio State University Wexner Medical Center, Columbus, OH, USA b c

a r t i c l e

i n f o

Article history: Received 3 May 2019 Accepted 8 July 2019 Available online xxxx Keywords: Parkinson’s disease Deep brain stimulation Post-surgical outcomes

a b s t r a c t Background: The goal of deep brain stimulation (DBS) is to achieve maximal benefit for the patient while minimizing the likelihood of adverse effects. Currently, no standardized criteria exist that predicts extended hospital stay in DBS patients, although careful patient selection is recognized as a very important step for successful DBS therapy. Objectives and Methods: The objective of this study was to identify eight key factors that predicted extended post-operative hospital stay following DBS lead implantation, in an effort to better identify patients that would require minimal hospital stay, resulting in reduced cost and reduced exposure to hospital- related problems. Univariate logistic regression models were used to examine associations between each factor and patients’ post-surgical outcomes. Results: Using data collected from 183 patients, we found that 53 patients required a hospital stay longer than two days within one month post-procedure. Those who were 70 years or older and those who had frequent falls were significantly more likely to require extended post-surgical care. Patients that scored three points or higher on our eight-factor assessment scale had a greater likelihood of experiencing an event that would require an extended hospital stay following DBS lead placement, regardless of what three factors were present. Conclusions: Any PD patient who is 70 years or older, incurring frequent falls, or with more than three points on our scale, should be carefully screened and cautioned about likely prolonged recovery and extended post-operative hospital stay. Ó 2019 Published by Elsevier Ltd.

1. Introduction Deep brain stimulation (DBS) is an accepted intervention for treating the motor symptoms of Parkinson’s disease (PD) when medical therapy is maximized and is no longer effective. The goal of DBS implantation is to achieve maximal benefit (e.g., symptom relief) for the patient while avoiding or minimizing the likelihood of adverse effects. There are currently no standardized criteria for choosing DBS candidates that are predictive of extended hospital stay although careful patient selection is imperative for successful DBS therapy.

⇑ Corresponding author at: Department of Neuroscience, Center for Neuromodulation, The Ohio State University Wexner Medical Center, Columbus, OH, USA. E-mail address: [email protected] (N.A. Young). 1 Equally contributing first authors.

Potential DBS patients are typically evaluated by a multidisciplinary team that includes a movement disorder neurologist, a neurosurgeon, and a neuropsychologist and/or psychiatrist specializing in behavioral comorbidities associated with movement disorders [1]. Patients’ symptoms and other data are reviewed by the team to determine whether the patient is a candidate for DBS. There is currently no standardized assessment tool in use to help the team evaluate potential candidates. Some groups have created a questionnaire for general neurologists to use for referring potential candidates to DBS specialists [2], but these are not suitable for use by the DBS team proper during patient review. Our objective was to identify key factors that would be useful in predicting extended hospital stay post-DBS surgery, in an effort to better identify patients that have the best chance at successful intervention, and to better predict which patients would require additional support post-surgery. Our criteria were selected to

https://doi.org/10.1016/j.jocn.2019.07.042 0967-5868/Ó 2019 Published by Elsevier Ltd.

Please cite this article as: N. A. Young, M. P. Brown, J. Peng et al., Predicting extended hospital stay after deep brain stimulation surgery in Parkinson’s patients, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.07.042

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N.A. Young et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx

consider existing comorbidities and other variables that could impede patient post-operative recovery. Based on other studies, some of these factors can include, hepatopathy, development of pneumonia, pulmonary embolism, infections, and the presence of other co-morbidities [3,15]. We believe that the following patient criteria will predict extended hospital stay: age 70 or older, on anti-coagulation therapy, behavioral problems unrelated to motor disease, cognitive impairment, requiring/receiving treatment for cardiopulmonary disease or other major systematic disease, frequent falls, poor social support, and need for bilateral treatment of motor disease symptoms.

surgical outcomes. A composite total score was calculated by adding the number of ‘‘yes” answers on the eight proposed predictors. The relationship of this composite score with length of postsurgical hospital stay was also examined using logistic regression. Backward elimination was performed on all eight predictors; elimination proceeded until all remaining variables were significant at the 0.05 level. A two-sided significance level of a = 0.05 was used for all tests. Analyses were performed in SAS version 9.4 (SAS, Cary, NC).

2. Methods

Of the 183 patients, 53 (29%) required a hospital stay longer than two days within one month post-procedure. Using univariate analyses, we found that patients aged 70 or older were significantly more likely to require extended post-surgical care (OR = 2.27, 95% CI = 1.11–4.67) than those who were younger than 70 years. Patients who had frequent falls were also significantly more likely to require extended post-surgical care (OR = 2.58, 95% CI = 1.06–6.28) than patients who did not report frequent falls before surgery (Table 1, Fig. 1). One unit increase in the composite score was significantly associated with a 47% increase (OR = 1.47, 95% CI = 1.13–1.91) in the odds of having an extended hospital stay within one month post-procedure. At the conclusion of backward elimination, only age was associated with patient’s post-surgical extended hospital stay.

2.1. Participants All participants in this study were patients who underwent DBS lead placement surgery at the Center for Neuromodulation at The Ohio State University Wexner Medical Center between December 2010 and August 2015 (n = 183 procedures). The data were collected from 183 procedures targeting the subthalamic nucleus (STN): 160 unilateral DBS lead placements and 23 bilateral DBS lead placements (both hemispheres implanted on same day). This study included both male and female patients. All data had been collected and stored in our General Deep Brain Stimulation Database following previously approved IRB protocol and was analyzed according to IRB protocol specific to this study. All patients consented to collection and use of their information for future unspecified research. Patients were placed in one of two groups: (1) no post-surgical issues reported or (2) required post-surgical hospital stay longer than two days within 30 days of surgery. This clinical evaluation was determined by the neurosurgeon PI. Each patient was additionally evaluated for each of the eight potential predictor variables. Patients earned one point for each positive qualification on our proposed scale. The number of points earned was compared between the two groups. The eight predictors evaluated were defined as follows: 1. Age 70 or older: the patient is 70 years of age or older at time of DBS evaluation 2. Anti-coagulation therapy: the patient is receiving anticoagulation and/or anti-platelet treatment at the time of DBS evaluation 3. Behavioral problems: behavioral disturbances attributed to factors unrelated to Parkinson’s disease 4. Mild cognitive impairment: the patient meets criteria for mild cognitive impairment as determined by pre-surgical neuropsychological evaluation 5. Cardiopulmonary disease or other major systematic disease: the patient is receiving, or requires, treatment for cardiopulmonary disease or other major systematic disease (e.g., diabetes) at the time of DBS evaluation 6. Frequent falls: the patient has fallen more than once per week prior to DBS evaluation 7. Poor social support: the patient lacks family or caregiver support (lives alone, no family or community assistance with care or emotional support) 8. Need for bilateral DBS: the patient requires implantation of DBS leads in both brain hemispheres to sufficiently control motor symptoms. 2.2. Statistical method Univariate logistic regression models were used to examine associations between each predictor criterion and patients’ post-

3. Results

4. Discussion We hypothesized that patients who experienced extended hospital stay following DBS lead placement surgery would score 1 or higher on our eight-factor scale. We found that patients over 70 years or older and those that experienced frequent falls were more likely to experience an extended hospital stay within one month following the DBS lead placement surgery. We believe that our scale is the first step in defining qualitative screening criteria for DBS surgical candidates. 4.1. Cost of care and utility of predicting outcomes Part of the burden of PD is the high cost associated with the use of health care resources and hospital stays beyond the standard expectation following a DBS lead placement surgery. The identification of any factor during the DBS assessment that can predict the likelihood of extended hospital stay, or other extended use of health care resources, would be useful in assessment of the patient. It would also assist the care team with being prepared to adjust the treatment plan to the individual patient’s needs depending on which of the screening criteria were positive. In addition to increased costs, longer stay in hospital means more exposure to hospital acquired problems [13,14]. 4.2. Patients 70 years or older In the present study, we found that patients at 70 years or older at the time of DBS evaluation were more likely to experience a post-surgical event requiring an extended hospital stay. As the population ages, there will be an increasing number of older patients who will require surgery of this kind. More than one third of inpatient operations in the United States are performed on adults aged 65 years or older [4], making it increasingly more important to understand the relationship between age and postsurgical outcomes. Advancing age has been shown to increase post-operative mortality, overall morbidity, and post-operative complications within 30 days of non-emergent general surgery

Please cite this article as: N. A. Young, M. P. Brown, J. Peng et al., Predicting extended hospital stay after deep brain stimulation surgery in Parkinson’s patients, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.07.042

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N.A. Young et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx Table 1 Relationship between preliminary patient criteria and patients’ post-surgical observation (N = 183). Post-surgical observation Variable Age >= 70 <70 Coagulopathy Yes No Behavioral Issues Yes No Mild cognitive impairment Yes No Frequent falls Yes No Poor social support Yes No Need for Bilateral DBS Yes No Major systematic disease Yes No Total scorec a b c

Yes (N = 53)

No (N = 130)

OR (95% CI)a

p-valueb

18 (42.9%) 35 (24.8%)

24 (57.1%) 106 (75.2%)

2.27 (1.11, 4.67) Ref

0.026

25 (32.5%) 28 (26.4%)

52 (67.5%) 78 (73.6%)

1.34 (0.70, 2.55) ref

0.37

13 (36.1%) 40 (27.2%)

23 (63.9%) 107 (72.8%)

1.51 (0.70, 3.27) ref

0.29

11 (32.3%) 42 (28.2%)

23 (67.7%) 107 (71.8%)

1.22 (0.55, 2.72) ref

0.63

11 (47.8%) 42 (26.3%)

12 (52.2%) 118 (73.7%)

2.58 (1.06, 6.28) ref

0.037

4 (66.7%) 49 (27.7%)

2 (33.3%) 128 (72.3%)

n/a

0.059

47 (30.3%) 6 (21.4%)

108 (69.7%) 22 (78.6%)

1.60 (0.61, 4.19) ref

0.34

24 (31.6%) 29 (27.1%) 2.89 ± 1.56

52 (68.4%) 78 (72.9%) 2.28 ± 1.06

1.24 (0.65, 2.37) ref 1.47 (1.13, 1.91)

0.51 0.0037

OR and 95% CI not reported if there was an expected cell count less than 5. If OR provided, p-value is from likelihood ratio test of logistic regression model; if no OR, p-value is from Fisher’s exact test. OR corresponding to one unit increase is reported.

Fig. 1. Estimated OR and 95% CI for preliminary patient criteria using univariate logistic regression with post-surgical complication. Poor social support was not included in the plot due to small cell count.

[5]. This is likely due to older adults having lower physiological reserve associated with aging, which makes them vulnerable to post-surgical complications [5,6]. Age also influences the presence of comorbidities in PD. It has been shown that 4.6% of people in the general population aged 65–74 years are affected by more than four diseases [7], while only 10% of those over 75 years are free of disability [8]. The typical age of onset of PD is between 60 and 70 years of age; therefore, it is likely that patients who receive a PD diagnosis are already receiving treatment for a comorbid condition [9]. In a study that evalu-

ated acute comorbid events in PD patients, patients who experienced the most urgent events (including neurological, nonneurological, and emergency room events) were significantly older, with a mean age of 75 years [9]. 4.3. Frequent falls We found that PD patients with a higher frequency of falls prior to DBS lead placement surgery were significantly more likely to require an extended stay in hospital post-procedure. Falls are more

Please cite this article as: N. A. Young, M. P. Brown, J. Peng et al., Predicting extended hospital stay after deep brain stimulation surgery in Parkinson’s patients, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.07.042

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N.A. Young et al. / Journal of Clinical Neuroscience xxx (xxxx) xxx

likely in PD patients than in the normal population [10], and frequent falling is an indicator of greater severity of PD. Falling can be due to a more marked response to levodopa, more dyskinesias, and more instances of ‘on-off’ motor fluctuations [10], as well as postural instability, gait disturbances, freezing, impaired balance, impaired cognition, reduced muscle leg strength, and reduced proprioception [12]. Frequent falls in PD patients indicate both the physical and cognitive severity of PD, and therefore it is not surprising that this criterion was correlated with the likelihood of an extended hospital stay following DBS lead placement surgery. 4.4. Impact of higher number of positive predictors Our data suggest that patients that score three points or higher on our eight-factor assessment scale have a greater likelihood of experiencing an event that requires an extended hospital stay following DBS lead placement surgery, regardless of which three predictors were positive. We believe this speaks to the importance of an overall health evaluation for potential DBS candidates, as the majority of the criteria on our scale were designed in effort to capture existing comorbid conditions and other variables that could impede patient post-operative recovery follow DBS lead implantation. For example, although it has been shown that patients with cardiopulmonary disorders comorbid with PD experienced ischemic stroke at a rate three times higher than in age-matched, non-PD patients [11], we did not find this variable to be a predictor of extended hospital stay. We attribute this to our qualitative preselection process (see discussion below), and therefore small sample size. Further research using a database with many more patients is warranted and recommended to thoroughly evaluate the effectiveness of the other criteria. 4.5. Limitations The primary limitation of the current study is that patients included were already pre-screened for DBS. This qualitative preselection process can potentially skew the data set, and therefore it may not be randomly distributed. Patients approved for DBS are typically pre-screened by a neurosurgeon, a movement disorder neurologist, and a neuropsychologist and/or psychiatrist [1], as well as nurses, social workers, and other members of the clinical care team. Although there are no set criteria to determine candidacy, cases are reviewed by multiple experts who consider patients’ motor symptoms, overall health, cognition, and social support system. Currently, our team qualitatively determines candidacy based on these principles, but without a clear set of criteria laid out in advance of each evaluation. 5. Conclusions Any PD patient aged 70 years or older, incurring frequent falls, or with a score of 3 or higher on our scale should be carefully screened and cautioned about likely prolonged recovery and extended post-operative hospital stay following DBS lead implantation. Funding sources

Declaration of Competing Interest None Acknowledgments This project has been supported in part by the Neuroscience Research Institute at The Ohio State University. We would like to thank Reghan Borer for editing support. Data Statement Due to the sensitive nature of medical records used in this study, patients were assured raw data would remain confidential and would not be shared. Appendix A. Supplementary material Supplementary data to this article can be found online at https://doi.org/10.1016/j.jocn.2019.07.042. References [1] Machado AG, Deogaonkar M, Cooper MS. Deep brain stimulation for movement disorders: patient selection and technical options, Cleve. Clin J Med 2012;79(Suppl 2):S19–24. [2] Okun MS, Fernandez HH, Pedraza O, Misra M, Lyons KE, Pahwa R, et al. Development and initial validation of a screening tool for Parkinson disease surgical candidates. Neurology 2004;63:161–3. [3] Voges J, Hilker R, Bötzel K, Kiening KL, Kloss M, Kupsch A, et al. Thirty days complication rate following surgery performed for deep-brain-stimulation. Mov Disord 2007;22(10):1486–9. [4] Durso SC, Sullivan GM, editors. Geriatric review syllabus: a core curriculum in geriatric medicine. New York: American Geriatric Society; 2016. [5] Gajdos C, Kile D, Hawn MT, Finlayson E, Henderson WG, Robinson TN. Advancing age and 30-day adverse outcomes after nonemergent general surgeries. J Am Geriatr Soc 2013;61(9):1608–14. https://doi.org/10.1111/ jgs.12401. [6] Buchner DM, Wagner EH. Preventing frail health. Clin Geriatr Med 1992;8:1–17. [7] Abrams M. The health of the very elderly. In: Isaacs B, editors. Recent advances in geriatric medicine;1985. p. 113–21. [8] Horan MA. Presentation of disease in old age. In: Tallis RC, Fillit HM, Brocklehurst JC, editors. Brocklehurst’s textbook of geriatric medicine and gerontology, 5th ed.; 1998. p. 201–6. [9] Martognoni E, Godi L, Citterio A, Zangaglia R, Riboldazzi G, Calandrella D, et al. Comorbid disorders and hospitalization in Parkinson’s disease: a prospective study. Neurol Sci 2004;25:66–71. [10] Ashburn A, Stack E, Pickering RSM, Ward CD. A community-dwelling sample of people with Parkinson’s disease: characteristics of fallers and non-fallers. Ageing 2001;30(1):47–52. [11] Bodenmann P, Ghika J, van Melle G, Bogousslavsky J. Comorbidités neurologiques du parkinsonisme. Rev Neurol (Paris) 2001;157(1):45–54. [12] Paul SS, Sherrington C, Canning CG, Fung VS, Close JC, Lord SR. The relative contribution of physical and cognitive fall risk factors in people with Parkinson’s disease: a large prospective cohort study. Neurorehabil Neural Repair 2014;28(3):282–90. https://doi.org/10.1177/1545968313508470. [13] Tess BH, Glenister HM, Rodrigues LC, Wagner MB. Incidence of hospitalacquired infection and length of hospital stay. Eur J Clin Microbiol Infect Dis 1993;12(2):81–6. [14] Hassan M, Tuckman HP, Patrick RH, Kountz DS, Kohn JL. Hospital length of stay and probability of acquiring infection. Int J Pharm Healthc Mark 2010;4 (4):324–38. https://doi.org/10.1108/17506121011095182. [15] Buhmann C, Huckhagel T, Engle K, Gulberti A, Hidding U, Poetter-Nerger M, et al. Adverse events in deep brain stimulation: a retrospective long-term analysis of neurological, psychiatric and other occurrences. PLoS ONE 2017;12 (970):. https://doi.org/10.1371/journal.pone.0178984e0178984.

This project has been supported in part by the Neuroscience Research Institute at The Ohio State University.

Please cite this article as: N. A. Young, M. P. Brown, J. Peng et al., Predicting extended hospital stay after deep brain stimulation surgery in Parkinson’s patients, Journal of Clinical Neuroscience, https://doi.org/10.1016/j.jocn.2019.07.042