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Duration of Effect and Associated Factors of Injection Laryngoplasty

  • Ji Min Yun
    Affiliations
    Department of Otorhinolaryngology-Head and Neck Surgery, Ilsan Paik Hospital, Inje University College of Medicine, Goyang, Republic of Korea
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  • Keun Woo Jung
    Affiliations
    Department of Otorhinolaryngology-Head and Neck Surgery, Ilsan Paik Hospital, Inje University College of Medicine, Goyang, Republic of Korea
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  • Sang Duk Hong
    Affiliations
    Department of Otorhinolaryngology-Head and Neck Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
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  • Yoon Kyoung So
    Correspondence
    Address correspondence and reprint requests to Yoon Kyoung So, Department of Otorhinolaryngology-Head and Neck Surgery, Ilsan Paik Hospital, Inje University College of Medicine, 170 Juhwa-ro, Ilsanseo-gu, Goyang-si, Gyeonggi-do 10380, Republic of Korea.
    Affiliations
    Department of Otorhinolaryngology-Head and Neck Surgery, Ilsan Paik Hospital, Inje University College of Medicine, Goyang, Republic of Korea
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Open AccessPublished:May 03, 2022DOI:https://doi.org/10.1016/j.jvoice.2022.03.017

      Summary

      Objective

      Injection laryngoplasty (IL) has become a mainstay in the treatment of unilateral vocal fold paralysis due to technical ease and avoidance of open surgery. The duration of IL effect depends on the injected material and has not been defined clearly. We aimed to define the effective duration of IL and to investigate the associated factors.

      Methods

      Fifty-nine patients who underwent IL for unilateral vocal fold paralysis were included. IL was performed using a cricothyroid membrane approach under local anesthesia. During follow-up, in cases that developed subjective hoarseness with objective glottic insufficiency, a second IL was performed, and loss of IL effect was recorded. The duration of IL was analyzed using Kaplan-Meier estimates, and the associations between duration of effect and various factors such as postinjection voice therapy, injected material, and cause of paralysis were investigated using log-rank test.

      Results

      Of 59 patients, 20 (33.9 %) received a second IL. The median time interval between the first and second IL was 3.3 months (95% CI, 0.4∼27.8 months). The mean duration of effect after IL was 42.5 months (95% CI, 32.1∼52.9 months), and the rate of persisting effect was 63.4% at 1-year after IL (1-year effect rate) and 59.4% at 2 years after IL. The 1-year effect rate was 80.8% in cases with postinjection voice therapy and 57.8% in those without postinjection voice therapy (P = 0.084). Injected material, DM, HTN, patient age and sex, and cause of paralysis had no effect on the 1-year effect rate.

      Conclusions

      The mean duration of IL effect was 42.5 months, and the rate of persisting effect was 63.4% at 1-year after IL. There were no significant factors affecting the duration of effect, although the duration tended to be slightly longer in cases with postinjection voice therapy. Further study with a prospective, randomized design is needed.

      Key words

      INTRODUCTION

      Glottal insufficiency related to uncompensated unilateral vocal fold paralysis (UVFP) can cause considerable morbidity including voice change, aspiration, and pneumonia.
      • Gardner GM
      • Smith MM
      • Yaremchuk KL
      • et al.
      The cost of vocal fold paralysis after thyroidectomy.
      • Bhattacharyya N
      • Kotz T
      • Shapiro J.
      Dysphagia and aspiration with unilateral vocal cord immobility: incidence, characterization, and response to surgical treatment.
      • Bihari A
      • Meszaros K
      • Remenyi A
      • et al.
      Voice quality improvement after management of unilateral vocal cord paralysis with different techniques.
      Injury to the vagus nerve or recurrent laryngeal nerve (RLN) from neck or cardiothoracic surgery is a frequent cause of UVFP. Malignancies along the course of RLN in the neck, mediastinum, and lung are another major cause, and idiopathic cases are not rare.
      • Rosenthal LH
      • Benninger MS
      • Deeb RH.
      Vocal fold immobility: a longitudinal analysis of etiology over 20 years.
      Various approaches including injection laryngoplasty (IL), medialization thyroplasty, and arytenoid adduction have been tried for UVFP.
      • Siu J
      • Tam S
      • Fung K.
      A comparison of outcomes in interventions for unilateral vocal fold paralysis: a systematic review.
      In the past, IL, which usually is performed with temporary materials such as hyaluronic acids, was considered a temporary procedure before the UVFP was proven to be permanent or recovered. However, it has become a mainstay in the treatment of both transient and temporary UVFP.
      • Courey MS
      • Naunheim MR.
      Injection laryngoplasty for management of neurological vocal fold immobility.
      ,
      • O'Leary MA
      • Grillone GA.
      Injection laryngoplasty.
      However, the natural course after IL is not clear. The duration of IL effect depends on the injected material. The effect of IL generally is considered to last several months, except for that of calcium hydroxyapatite, but has not been defined clearly.
      • Kwon TK
      • Buckmire R.
      Injection laryngoplasty for management of unilateral vocal fold paralysis.
      Recently, several factors such as timing of the procedure after development of UVFP or postprocedural voice therapy have been identified as related to IL effect longevity.
      • Jeong GE
      • Lee DH
      • Lee YS
      • et al.
      Treatment efficacy of voice therapy following injection laryngoplasty for unilateral vocal fold paralysis.
      • Jang JY
      • Lee G
      • Ahn J
      • et al.
      Early voice rehabilitation with injection laryngoplasty in patients with unilateral vocal cord palsy after thyroidectomy.
      • Friedman AD
      • Burns JA
      • Heaton JT
      • et al.
      Early versus late injection medialization for unilateral vocal cord paralysis.
      In this study, we aimed to define the duration of IL effect and to investigate the associated factors.

      METHODS

      Patients

      This retrospective study included patients who underwent IL for UVFP at Ilsan Paik Hospital, Republic of Korea, between March 2014 and December 2020. This study was approved by the Institutional Review Board of Ilsan Paik Hospital (IRB File No. ISPAIK 2021-07-023). Patients with UVFP who had injection laryngoplasty were screened initially (n=82). Those who recovered from UVFP during follow-up after IL were excluded from the study (n = 5). Those who were followed-up for less than three months were also excluded (n = 18), but those who underwent second injection within three months were not excluded. A total of 59 patients was included in this study. Patient age ranged from 13 to 83 years, with a median of 63 years. Of the 59 patients, 31 were male and 28 were female. In terms of etiology of UVFP, surgery-related UVFP was most common (44.1%), followed by UVFP of unknown cause (33.9%). Duration of UVFP was less than six months in 34 patients (57.6%) and greater than six months in 25 patients (42.4%) (Table 1).
      TABLE 1Patient Characteristics
      CharacteristicsValues
      AgeMedian (IQR) (year)63 (53∼72)
      GenderMale: Female31:28
      DM17 (28.8%)
      HTN24 (40.0%)
      Cause of paralysisIdentified39 (66.1%)
       RLN invasion by tumor4 (6.8%)
       RLN injury during operation26 (44.1%)
       Brainstem lesion or surgery2 (3.4%)
       Cranial nerve palsy3 (5.1%)
       Trauma of intubation, TA4 (6.8%)
      Unidentified20 (33.9%)
      Duration of paralysis≤6 mo34 (57.6%)
      >6 mo25 (42.4%)
      Injection materialRestylene38 (64.4%)
      Artesense21 (35.6%)
      Post-injection VT14 (23.7%)
      Reinjection or AA20 (33.9%)
      Follow-up periodMedian (IQR) (mo)7.8 (3.3∼18.9)
      Abbreviations: AA, arytenoid adduction; IQR, interquartile range; TA, traffic accident; VT, voice therapy.

      Injection laryngoplasty (IL)

      In all cases, IL was performed using a cricothyroid membrane approach under local anesthesia. A 23-gauge spinal needle was inserted through the cricothyroid membrane into the paralyzed vocal fold under fiberoptic guidance until the needle tip was observed at the lateral and anterior sides of the vocal process of the arytenoid cartilage. A position deep to the vocal ligament was targeted, and injection was performed until the paralyzed vocal fold was augmented and no glottic gap remained during phonation. The injected material was Restylane (Q-Med Corp, Uppsala, Sweden)) in 38 patients (64.4%) and ArteSense (European Medical Contract Manufacturing B.V., Nijmegen, Netherlands) in 21 patients (35.6%).

      Postinjection voice therapy

      Fourteen patients (23.7%) underwent voice therapy after IL. The average number of sessions was eight, ranging from six to 10. Voice therapy was performed once per week by an experienced speech-language pathologist using direct and indirect voice therapy. Indirect therapy included self-recognition of voice problems and vocal hygiene education. Direct voice therapy encompassed a variety of voice facilitation techniques, including Lax Vox training, yawn-sigh, laryngeal massage, and resonance training. Specific therapeutic techniques were tailored to individual patients.

      Voice analysis

      Perceptual, acoustic, and aerodynamic assessments were performed before and after IL. The Multi-Dimensional Voice Program from the Computerized Speech Lab (CSL, Model 4150B; Kay Elemetrics Corp.) and Phonatory Aerodynamic System were used for acoustic and aerodynamic analyses. Preinjection and postinjection voice analyses were performed in 24 (40.7%) and 12 patients (20.3%), respectively. Each patient was seated in a quiet room, and a microphone was placed 3 cm from the mouth. They were asked to produce continuously the vowel sound /a/ at a comfortable pitch and volume and to read a standardized, phonetically balanced Korean passage (“Sanchek” passage).
      • Jeong OR.
      Speech overall evaluation.
      Fundamental frequency, percentage of jitter and shimmer, noise-to-harmonics ratio (NHR), voice range profile (VRP), and maximum phonation time (MPT) were calculated. The speech-language pathologist assessed patient voice according to the overall grade-roughness-breathiness-asthenia-strain (GRBAS) scale. In addition, patients performed self-assessments using a culturally validated Korean version of the Voice Handicap Index (VHI) questionnaire
      • Kim J-OK
      • Park Sung-Eun
      • et al.
      Validity and reliability of Korean-version of voice handicap index and voice-related quality of life.
      before and after voice therapy.

      Follow-up

      Patients were followed after IL at three- to six-month interval. At each follow-up, laryngoscopic examination and subjective symptoms were assessed. Patients who were lost to follow-up within three months were excluded from this study, but those who underwent a second procedure within three months were not. Those who recovered from UVFP during follow-up also were excluded. The median follow-up period was 7.8 months. During follow-up, in cases where subjective hoarseness developed and objective glottic insufficiency was observed with laryngoscope, a second IL or arytenoid adduction was performed.

      Statistical analysis

      The duration of IL effect was assessed using Kaplan- Meier estimates. The log-rank test was used to assess the factors associated with duration. SPSS software for Windows, version 17.0 (SPSS Inc., Chicago, IL) and R 3.6.1 for Windows were used for statistical analyses. All tests were two-sided, and P < 0.05 was considered statistically significant.

      RESULTS

      After IL, the G score of the GRBAS scale significantly decreased (1.4 ± 0.8) compared to before IL (2.8 ± 0.4, P < 0.001). VHI total score improved after IL (from 60.9 ± 37.1 to 10.1 ± 12.6, P = 0.001), as did maximum phonation time (MPT) (from 5.1 ± 3.5 to 9.7 ± 5.6, P = 0.005). Jitter, shimmer, and NHR showed decreasing tendencies but no statistical significance (Table 2).
      TABLE 2Voice Outcomes after IL for Unilateral VFP
      Before ILAfter ILP-value
      GRBAS G score2.8 ± 0.41.4 ± 0.8<0.001
      GRBAS R score1.3 ± 1.10.5 ± 0.50.055
      GRBAS B score2.7 ± 0.71.2 ± 1.0<0.001
      GRBAS A score0.8 ± 1.30.1 ± 0.30.087
      Jitter4.0 ± 3.02.0 ± 1.70.087
      Shimmer8.3 ± 5.54.8 ± 3.20.154
      NHR0.2 ± 0.20.2 ± 0.10.178
      MPT5.1 ± 3.59.7 ± 5.60.005
      VHI total score60.9 ± 37.110.1 ± 12.60.001
      VHI_F score18.7 ± 14.32.2 ± 3.50.002
      VHI_P score23.3 ± 12.35.2 ± 6.1<0.001
      VHI_E score18.9 ± 12.72.6 ± 3.70.001
      Notes: Values are expressed as mean ± standard deviation. Bold values are statistically significant.
      Abbreviations: IL, injection laryngoplasty; MPT, maximum phonation time; NHR, noise-to-harmonics ratio; VHI, voice handicap index; VHI_E, VHI emotional domain; VHI_F, VHI functional domain; VHI_P, VHI physical domain.
      Of 59 patients, 20 (33.9%) underwent secondary procedures due to recurrence of glottic insufficiency; repeat IL was performed in all cases. After the second procedure, one patient underwent arytenoid adduction. The median time interval between first and second IL was 3.3 months, ranging from 0.4 to 27.8 months. Of the 20 second IL cases, 18 (90%) were performed within 1-year after first IL (Figure 1).
      FIGURE 1
      FIGURE 1Time interval between first and second IL. Second IL was performed in 20 cases (33.9%). The median time interval between first and second IL was 3.3 mo, ranging from 0.4 to 27.8 mo. Of 20 cases, 18 (90%) were performed within one year after first IL. “(For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)”
      When the second IL was defined as the end of the first IL effect and the duration of effect was analyzed using the Kaplan-Meier survival model, the mean duration of effect was 42.5 months (95% CI, 32.1∼52.9 months). The rate of persisting effect was 63.4% at 1-year after IL (1-year effect rate) and 59.4% at 2 years after IL (Figure 2).
      FIGURE 2
      FIGURE 2Duration of effect after IL. The mean duration of effect was 42.5 months (95% CI, 32.1∼52.9 months). Rate of persisting effect was 63.4% at one year after IL (1-y effect rate) and 59.4% at 2-y after IL. “(For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)”
      The 1-year effect rate was 80.8% in cases with postinjection voice therapy and 57.8% in those without postinjection voice therapy (P = 0.084, Figure 3A). Second IL was performed in four of 14 cases (28.6 %) with voice therapy and 16 of 45 cases (35.6%) without voice therapy. In cases with voice therapy, the median time interval between first and second IL was 15.1 months, while it was 2.7 months in those without voice therapy (Figure 3B). The one-year effect rate was 52.7% in male patients and 73.9% in female patients (P = 0.091). Injection material, duration of paralysis, DM, HTN, patient age, and cause of paralysis were not associated with the duration of effect after IL (Table 3).
      FIGURE 3
      FIGURE 3Longevity of IL according to post-injection voice therapy. (A) The 1-y effect rate was 80.8% in cases with post-injection voice therapy and 57.8% in those without (P = 0.084). (B) In cases with voice therapy, the median time interval between first and second IL was 15.1 months, while it was 2.7 mo in those without voice therapy (P = 0.091). “(For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)”
      TABLE 3Duration of Effect According to Various Factors
      One-year effect rateP-value
      Voice therapyPerformed80.8%0.084
      Not performed57.8%
      Injection materialRestylene63.2%0.844
      Artesense67.5%
      Duration≤6 mo56.8%0.291
      >6 mo72.1%
      CauseUnidentified59.1%0.948
      Identified64.4%
      DMAbsent61.9%0.948
      Present68.6%
      HTNAbsent65.2%0.250
      Present58.1%
      GenderMale52.7%0.091
      Female73.9%
      Age (years)≤6063.6%0.878
      <6063.6%

      DISCUSSION

      Since IL first was described by Brunings in 1911, various injection materials such as collagen, hyaluronic acid (HA), autologous fat, and calcium hydroxyapatite have been introduced.
      • Kwon TK
      • Buckmire R.
      Injection laryngoplasty for management of unilateral vocal fold paralysis.
      ,
      • Lisi C
      • Hawkshaw MJ
      • Sataloff RT.
      Viscosity of materials for laryngeal injection: a review of current knowledge and clinical implications.
      ,
      • Sulica L
      • Rosen CA
      • Postma GN
      • et al.
      Current practice in injection augmentation of the vocal folds: indications, treatment principles, techniques, and complications.
      The duration of effect can be different according to injection material. Calcium hydroxyapatite is a long-lasting injection material that is approved by the US Food and Drug Administration.
      • Belafsky PC
      • Postma GN.
      Vocal fold augmentation with calcium hydroxylapatite.
      Rosen et al reported significant improvement and moderate improvement in 67% and 81% of patients, respectively, at 12 months after injection.
      • Rosen CA
      • Gartner-Schmidt J
      • Casiano R
      • et al.
      Vocal fold augmentation with calcium hydroxylapatite: twelve-month report.
      However, a substantive portion of patients was lost to follow-up or unavailable for analysis at 12 months after injection. In many studies, loss to follow-up is the main reason why the duration of IL effect cannot be assessed clearly. HA is a component of the extracellular matrix, and the viscoelastic properties of vocal folds after HA injection are similar to those of the healthy vocal fold in animal studies.
      • Borzacchiello A
      • Mayol L
      • Garskog O
      • et al.
      Evaluation of injection augmentation treatment of hyaluronic acid based materials on rabbit vocal folds viscoelasticity.
      Due to its properties and safety, HA has become another popular injection material for IL. HA is considered a short-lasting material. Although there is debate on the long-term effect of IL with HA, some studies have reported that the effect lasted longer than 12 months in a substantial portion of patients (>50%).
      • Oguz H
      • Demirci M
      • Arslan N
      • et al.
      Long-term voice results of injection with hyaluronic acid-dextranomere in unilateral vocal fold paralysis.
      • Reiter R
      • Brosch S.
      Laryngoplasty with hyaluronic acid in patients with unilateral vocal fold paralysis.
      • Wang CC
      • Wu SH
      • Tu YK
      • et al.
      Hyaluronic acid injection laryngoplasty for unilateral vocal fold paralysis-a systematic review and meta-analysis.
      ArteSense consists of polymethyl methacrylate (PMMA) microspheres and bovine collagen. It was introduced as a relatively long-lasting injection material because PMMA microspheres are not phagocytosed and fosters synthesis of own collagen.
      • Cohen SR
      • Holmes RE.
      Artecoll: a long-lasting injectable wrinkle filler material: report of a controlled, randomized, multicenter clinical trial of 251 subjects.
      ,
      • Lemperle G
      • Morhenn V
      • Charrier U.
      Human histology and persistence of various injectable filler substances for soft tissue augmentation.
      Min et al reported persisting effect at 12 months follow-up in 48% of all patients and 53% of patients with permanent UVFP.
      • Min JY
      • Hong SD
      • Kim K
      • et al.
      Long-term results of Artecoll injection laryngoplasty for patients with unilateral vocal fold motion impairment: safety and clinical efficacy.
      In an in vivo study, the dimension of the augmented region was maintained in the Artecoll group for nine months after injection, while up to 30% of the augmented dimension was resorbed in the HA group.
      • Lim JY
      • Kim HS
      • Kim YH
      • et al.
      PMMA (polymethylmetacrylate) microspheres and stabilized hyaluronic acid as an injection laryngoplasty material for the treatment of glottal insufficiency: in vivo canine study.
      In this study, the 1-year effect rate after IL was 63.4% overall, 63.2% in the HA group, and 67.5% in the ArteSense group, consistent with previous results. Despite the theoretical superiority, there was no statistically significant difference between the two injection materials (P = 0.844). The effect of IL was maintained for longer than 1-year in more than half of patients, although the injection material was not permanent, such as calcium hydroxyapatite.
      The duration of paralysis, timing of injection after onset of UVFP, also can affect the duration of effect. In terms of duration of paralysis, there have been many studies related to the effect on IL. In several studies, the late injection group (>6 months) had a significantly higher rate of open surgery than did those who underwent early injection (<6 months).
      • Friedman AD
      • Burns JA
      • Heaton JT
      • et al.
      Early versus late injection medialization for unilateral vocal cord paralysis.
      ,
      • Alghonaim Y
      • Roskies M
      • Kost K
      • et al.
      Evaluating the timing of injection laryngoplasty for vocal fold paralysis in an attempt to avoid future type 1 thyroplasty.
      In another study on IL after thyroidectomy, acoustic parameters were worse in the late injection group (>3 months) than in early injection group (<3 months).
      • Jang JY
      • Lee G
      • Ahn J
      • et al.
      Early voice rehabilitation with injection laryngoplasty in patients with unilateral vocal cord palsy after thyroidectomy.
      However, in the present study, there was no significant difference in rate of secondary procedures within 1-year (P = 0.291). The 1-year effect rate was 56.8% in the early injection group (<6 months) and 72.1% in the late injection group (>6 months). A previous study has suggested that early injection allows for a better final resting position once synkinetic reinnervation is complete and tactile stimulation from physical contact with the contralateral mobile vocal cord.
      • Friedman AD
      • Burns JA
      • Heaton JT
      • et al.
      Early versus late injection medialization for unilateral vocal cord paralysis.
      However, a recently paralyzed vocal cord is more likely to undergo further laryngeal muscle atrophy than is a vocal cord paralyzed for a long duration. The association between duration of paralysis and duration of effect has not been determined. There could be a selection bias in this kind of non-randomized studies, and significant follow-up losses can reduce the analysis accuracy. In this study, five of 34 patients (14.7%) in the early injection group and nine of 25 patients (36%) in the late injection group underwent second IL.
      We also investigated the association between postinjection voice therapy and duration of IL effect. In a previous study, voice parameters significantly improved after postinjection voice therapy than at one month after IL alone. In patients without postinjection voice therapy, the voice parameters at six months after IL were not significantly different from those at one month after IL.
      • Jeong GE
      • Lee DH
      • Lee YS
      • et al.
      Treatment efficacy of voice therapy following injection laryngoplasty for unilateral vocal fold paralysis.
      Previous studies have reported the efficacy of voice therapy as an intervention for UVFP.
      • Mattioli F
      • Menichetti M
      • Bergamini G
      • et al.
      Results of early versus intermediate or delayed voice therapy in patients with unilateral vocal fold paralysis: our experience in 171 patients.
      • Busto-Crespo O
      • Uzcanga-Lacabe M
      • Abad-Marco A
      • et al.
      Longitudinal voice outcomes after voice therapy in unilateral vocal fold paralysis.
      • Schindler A
      • Bottero A
      • Capaccio P
      • et al.
      Vocal improvement after voice therapy in unilateral vocal fold paralysis.
      After IL, the position of the paralyzed vocal fold is improved for voice therapy. Therefore, the efficacy of voice therapy can improve. Improved vocal contact after IL and postinjection voice therapy could affect the duration of effect after IL. In this study, postinjection voice therapy was performed in 14 of 59 patients (23.7%). The 1-year effect rate tended to be slightly higher (80.8%) in cases with post-injection voice therapy than in those without (57.8%), although there was no statistical significance (P = 0.084). Significance might have been achieved if the study was randomized and the selection bias was controlled. Also, in cases with postinjection voice therapy, the interval between first and second IL treatments was longer. The median time interval between first and second IL was 15.1 months in cases with voice therapy and 2.7 months in those without voice therapy (Figure 3B).
      There were several limitations in this study. First, this was a retrospective cohort study. Parameters such as voice therapy, injection material, and duration of paralysis were not randomized. More information could have been obtained if a prospective, randomized study, blinded to injected materials, had been conducted. Next, a sizeable portion of patients was lost to follow-up. Though this loss could be attributed to absence of discomfort, the lost patients might have moved to another hospital. Therefore, we performed a survival analysis. Nevertheless, if follow-up duration and interval were standardized, data analysis would be more efficient. Lastly, the outcome measurement could be improved with follow-up voice analysis. In this study, the outcome measurement was need for a secondary procedure. With the standardized follow-up, if the outcome measurement was reinforced with follow-up voice analysis, the result would be more reliable.

      CONCLUSION

      IL has become a mainstay of treatment for UVFP due to its relative technical ease and no need for open surgery. However, the duration of effect is not clear. In this study, the mean duration of effect was 42.5 months, and the rate of persisting effect was 63.4% at 1-year after IL. There were no significant factors affecting the duration of effect, although the duration tended to be slightly longer in cases with postinjection voice therapy. Further study with prospective, randomized design is needed.

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