Available online at www.sciencedirect.com
American Journal of Otolaryngology–Head and Neck Medicine and Surgery 32 (2011) 124 – 129 www.elsevier.com/locate/amjoto
Effect of fasting on voice in males☆ Abdul-latif Hamdan, MD, FACSa,⁎, Jihad Ashkar, MDb , Abla Sibai, PhDc , Dima Oubarid , Sami Tanbouzi Husseini, MDb a
Department of Otolaryngology, American University of Beirut Medical Center, Lebanon Department of Otolaryngology—Head and Neck Surgery, American University of Beirut Medical Center, Lebanon c Department of Epidemiology and Population Health, Faculty of Health Sciences, American University of Beirut, Lebanon d Specialty Voice Center, Beirut, Lebanon Received 13 May 2009 b
Abstract
Purpose of the study: The aim of the study was to study how fasting between 12 and 14 hours affects voice production. Study design: This is a prospective study of male subjects. Material and method: A total of 26 healthy male subjects were recruited for the study. The age varied between 22 and 50 years with a mean of 28 years. Exclusion criteria included hoarseness at the time of presentation, history of recent upper respiratory tract infection, or microlaryngeal surgery. Subjects were evaluated while fasting and nonfasting. Each subject was asked about vocal fatigue and ease of phonation. This was followed by acoustic analyses and laryngeal videostroboscopy. Results: The incidence of vocal fatigue was not higher while fasting compared to nonfasting (P = 1.00). Phonatory effort was significantly greater during fasting (P b .001). Fifty percent of the subjects had an increase in their phonatory effort. There was a significant decrease in the habitual pitch, voice turbulence index, and noise-to-harmonic ratio (P = .018, .045, and .001, respectively). There were no laryngeal videostroboscopic changes. Conclusion: Fasting in males results in an increase in phonatory effort. These phonatory changes may be secondary to dehydration as well as overall neuromuscular fatigability. © 2011 Elsevier Inc. All rights reserved.
1. Introduction One of the fundamental rituals of Islam is fasting during the month of Ramadan. This month varies across the years and is decided by the lunar calendar. Devotees are supposed to fast from dawn to sunset every day of the month. Fasting means abstaining from eating, drinking, and taking medications as well as intravenous fluids and nutrients. During the month of Ramadan, meals are limited to two: one before sunrise and one shortly after sunset. Hence, meals are exclusively nocturnal and less frequent, with the total ☆
No conflict of interest or financial support in relation to this manuscript. ⁎ Corresponding author. Department of Otolaryngology, American University of Beirut, P.O. Box: 11-0236 Beirut, Lebanon. Tel.: +961 1 746660; fax: +961 1 746660. E-mail addresses:
[email protected],
[email protected] (A. Hamdan). 0196-0709/$ – see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.amjoto.2009.12.001
amount of food intake being generally less [1-6]. Consequently, the total body weight slightly decreases during this month. This has been attributed to a decrease in fluid intake as the total amount of water and vegetable intake has been reported to be less [7-9]. As a result of this intermittent fasting, there are numerous physiologic and chronobiologic changes. Several studies have been undertaken to investigate the effects of fasting in healthy subjects, the results of which are controversial mainly due to variations in the protocols used, differences in nutritional customs and habits, and the seasonal occurrence of the Ramadan month. The hematologic, cardiac, circadian, and hormonal changes have been elucidated in the literature [1-9]. There have been reports showing a 24-hour mean decrease in the glucose level during Ramadan in comparison to the control day before fasting [10]. On the other hand, studies of lipid blood level showed an increase in total cholesterol and a decrease in low-density lipoprotein and low-density lipoprotein–high-density
A. Hamdan et al. / American Journal of Otolaryngology–Head and Neck Medicine and Surgery 32 (2011) 124–129
lipoprotein ratio [11-13]. Concerning serum protein levels, an increase in total proteins was demonstrated, with the most important change being the serum uric acid urea and serum osmolarity [14-16]. These changes were mainly attributed to dehydration. The decrease in water intake has also been reflected in a decrease in the 24-hour urine collection. The urinary output has been shown to decrease and the urinary osmolarity to increase with the effect being more pronounced during the third week of the month [17,18]. Based on a PubMed search, no study has looked at the effect of fasting on voice in males. Voice has been shown to be affected to various degrees by both systemic and local dehydration. However, there are controversies in the literature regarding the extent of these effects [19-24]. Most of the studies with human subjects included a small number of candidates and had a limited number of fasting hours. The authors of this manuscript have previously investigated the effect of fasting on voice in women [25]. Women were chosen initially because they are more prone to certain voice disorders than men. This has been attributed to the presence of less absorbing fluid in their vocal ligaments compared to men. More so there are other differences in the microstructure of the vocal fold in women compared to men. The distribution of hormonal receptors is denser in males, and the lamina propria is larger and contains 3 times more hyaluronic acid [26]. The presence of significant vocal changes while fasting in the female group has prompted this investigation of males while fasting. The purpose was to study the effects on voice of fasting for 12 to 14 hours using a self-reported evaluation, acoustic analyses, and laryngeal stroboscopic examination. The hypothesis was that fasting will result in an increase in phonatory effort, a high prevalence of vocal fatigue, and possibly a decrease in the maximum phonation time. The findings of this study are pertinent to the correlation between water intake and vocal complaints.
2. Material and method A total of 26 healthy male volunteers were recruited for the study. All subjects were nonprofessional voice users and had no knowledge of the impact that fasting might have on voice. The age varied between 22 and 50 years with a mean of 28 years and an SD of 5.46 years. Exclusion criteria included hoarseness at the time of presentation, history of recent upper respiratory tract infection, or recent history of microlaryngeal surgery. An informed consent was signed by all participants. Approval was obtained from the Institutional Review Board at the American University of Beirut (Lebanon). The study was conducted at the Specialty Voice Center (Beirut, Lebanon) where the subjects were evaluated while fasting and while not fasting. None of the subjects reported different voice use while fasting such as voice rest or long periods of prayer. The evaluation was performed 1 to 2 hours before sunset both in the fasting and nonfasting days. The nonfasting
125
procedures were performed a week before Ramadan began, and the fasting procedures were performed within the first 2 weeks of Ramadan. The evaluation consisted of looking for the incidence of vocal fatigue and the degree of phonatory effort as reported by the subject. Vocal fatigue was not graded by the subjects, whereas the ease of phonation was graded from 0 to 3, where 0 stands for no effort, 1 stands for mild effort, 2 for moderate, and 3 for much effort. Then each subject underwent evaluation of their voice using the Kay Elemetric (Bridgewater Lane, Lincoln Park, NJ) VISI Pitch (Model 3300). The test was performed twice, that is, 2 trials were done, while fasting and twice while nonfasting to have a better estimate of the measures. While the subject was seated in a quiet office, the patient's vocal signal was recorded directly into the system using a condenser microphone at a distance of 15 cm from the mouth. The subject was asked to (a) prolong the vowel “a” for 2 seconds, (b) count to 10 in a normal voice, and (c) produce the maximum phonation time by taking a deep breath and sustaining phonation for as long as he can. These utterances were produced twice in each recording and were analyzed using the voice quality assessment module and the pitch and energy tracing module of VISI Pitch software. The following acoustic variables were measured: average fundamental frequency, relative average perturbation, shimmer, noise-toharmonic ratio, voice turbulence index, habitual pitch, and maximum phonation time. The subjects also underwent at that time laryngeal videoendostroboscopy using a 70° rigid telescope coupled to the Karl Storz Laryngostrobe model 8020 and to a 30-mm single chip color Storz endoscopic telecam Dx pal 202320 20 (Storz Laryngostrobe 8020, Karl Storz Endoscopy Ltd, Slough, UK). No topical anesthetic was used during the laryngeal examination. The following parameters were noted: symmetry, amplitude, mucosal waves, periodicity, and closure. The time of evaluation did not exceed 10 to 15 minutes so as not to affect the voice of the participants. The experimenters knew that the participants were fasting during the month of Ramadan but did not know about the effect of fasting on voice. Frequencies and means (SD) were used to describe the sample for categorical and continuous variables, respectively. For each subject, the parameters were collected before and after fasting, and the appropriate statistical analysis for small sample size (Wilcoxon nonparametric paired test) was conducted. The analysis took into consideration the design (before and after) and modality of data collection (paired data). Differences were considered significant for P b .05. All analyses were conducted using SPSS software (SPSS Inc, Chicago, IL). 3. Results 3.1. Phonatory symptoms The incidence of vocal fatigue was not significantly higher while fasting, 23.1%, compared to nonfasting with
126
A. Hamdan et al. / American Journal of Otolaryngology–Head and Neck Medicine and Surgery 32 (2011) 124–129
19.2% (P = 1.00). The reported phonatory effort was significantly affected by fasting (P b .001). Fifty percent of the subjects had an increase in their reported phonatory effort. The increase was more pronounced in those who had mild phonatory effort while nonfasting (5/6 who had mild phonatory effort while nonfasting reported an increase in their phonatory effort). Close to 77% of the subjects indicated no effort while nonfasting, whereas while fasting, the figure dropped significantly to 46.2%. Moreover, 54% of the subjects indicated some level of phonatory effort while fasting vs only 23.1% while nonfasting (Tables 1 and 2). The overall average effort rating increased from 0.23 to 0.73. None of the subjects had reported a change in voice quality. 3.2. Acoustic analysis There was no statistical difference in any of the measurements of the acoustic parameters while fasting vs nonfasting, except for the habitual pitch, voice turbulence index, and noise-to-harmonic ratio that dropped significantly (P = .018, .045, and .001, respectively) (Table 3). There was also a drop in the average maximum phonation time while fasting that was not significant (Table 3). 3.3. Laryngeal videostroboscopic findings There was no statistically significant difference in any of the laryngeal findings. Surprisingly, the incidence of mucus was higher while nonfasting vs fasting (Table 4).
4. Discussion Phonation is a complex process that requires coordination and stability between various systems in the body. Adequate and balanced interaction of these systems is essential for voice production. Good breathing support, proper glottal attack, and malleable vocal fold cover are prerequisites for phonation [27]. Their importance has been thoroughly investigated in the literature with special emphasis on phonotrauma and hydration [28]. No study has looked at the effect of fasting on voice in males, whereas the effect on women has been previously reported [9]. Vocal fatigue was the most common reported complaint (53.6%) in that study, followed by pitch lowering of the voice (21.4%) and harshness (10.2%). Self-reported phonatory effort was significantly affected by fasting (P b .001). Of the 28 female Table 1 Self-perceived phonatory effort Nonfasting
No effort Mild effort Moderate effort Severe effort
Fasting
P
N
%
n
%
20 6 0 0
76.9 23.1 0 0
12 9 5 0
46.2 34.6 19.2 0
b.001
Table 2 Data on vocal fatigue and phonatory effort by fasting status Subject
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26
Vocal fatigue
Phonatory effort
Nonfasting
Fasting
Nonfasting
Fasting
No Yes No No No No No No No No No No No No Yes No No No No Yes No Yes No Yes No No
No Yes No No No No No No No No No No No No Yes No No Yes No Yes No Yes No Yes No No
None Mild effort None None None None None Mild effort None None None None None None Mild effort None None None None Mild effort None Mild effort None Mild effort None None
None Moderate effort None Mild effort Mild effort Mild effort None Moderate effort None None None None None None Moderate effort None None Mild effort Mild effort Moderate effort None Moderate effort Mild effort Mild effort Mild effort Mild effort
subjects, 23 had an increase in their phonatory effort. Vocal acoustic parameters did not change markedly except for the maximum phonation time that decreased significantly. Laryngeal videoendostroboscopy did not reveal any significant changes during fasting. All the stroboscopic parameters were the same except for a decrease in the amplitude of the mucosal waves in one subject and the presence of a posterior chink in 3 subjects. Similarly in this study, the most important finding was the increase in the overall phonatory effort. Fifty percent of the male subjects have reported an increase in their phonatory effort. Almost two thirds of the subjects used mild to moderate phonatory effort while fasting vs less than one third while nonfasting. The phonatory effort average (grade/ number of subjects) increased from 0.23 to 0.82. The prevalence of vocal fatigue in women and the higher prevalence of phonatory effort in women vs men may be attributed to differences in the microstructure of the vocal fold and to possible variations in the phonatory behavior between the 2 sexes. With respect to the acoustic analysis, there was a drop in the maximum phonation time by 2 seconds on average; however, this was not statistically significant. There was a significant drop in the habitual pitch, voice turbulence index, and noise-to-harmonic ratio. Voice turbulence index is a predictor of grade that is defined as the overall degree of deviance of voice. In a study by Bhuta et al, voice turbulence index significantly correlated in first rank order with grade according to the stepwise regression
A. Hamdan et al. / American Journal of Otolaryngology–Head and Neck Medicine and Surgery 32 (2011) 124–129
127
Table 3 Data on acoustic parameters by fasting status Subject Fundamental frequency
Relative average perturbation
Shimmer
Noise-toharmonic ratio
Voice turbulence index
Maximum Phonation time
Habitual pitch
Nonfasting Fasting Nonfasting Fasting Nonfasting Fasting Nonfasting Fasting Nonfasting Fasting Nonfasting Fasting Nonfasting Fasting 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Mean SD P
118.78 141.26 115.39 106.55 124.25 121.20 120.73 102.45 92.35 122.45 135.27 107.55 159.56 92.80 120.14 134.95 98.71 124.80 129.90 114.63 118.12 106.64 133.57 131.36 122.65 115.81 119.69 15.22 .107
116.64 145.80 116.45 106.39 106.99 109.00 129.08 107.89 96.63 124.41 136.60 109.70 169.20 107.00 129.44 122.18 99.42 125.70 126.76 113.30 119.97 109.63 140.60 129.30 132.30 118.07 121.09 15.89
1.40 0.31 0.57 0.44 1.06 0.94 0.31 0.46 1.27 0.35 0.19 0.39 0.43 0.87 1.89 1.82 0.49 1.36 1.36 1.36 1.36 1.36 1.36 1.36 1.36 1.36 0.098 0.52 .075
1.21 0.23 1.51 0.46 1.34 0.46 0.64 0.19 0.83 0.54 1.07 0.27 0.13 0.65 0.56 2.55 0.37 1.69 0.69 0.48 0.45 0.96 0.61 0.38 0.72 1.14 0.77 0.55
3.62 5.17 4.65 3.90 2.97 6.58 2.51 4.26 5.91 2.93 2.51 6.16 2.09 1.70 11.15 7.31 2.87 2.65 4.31 2.97 2.75 3.38 2.88 1.72 2.67 2.53 3.93 2.11 .124
4.79 4.39 0.16 3.02 4.60 6.06 3.34 3.32 3.59 2.70 5.39 3.00 1.64 1.23 2.20 5.16 3.24 2.98 2.61 3.72 3.15 3.42 2.70 2.77 2.23 1.14 3.17 1.36
0.16 0.13
0.14 0.08
0.14 0.14 0.14 0.14 0.14 0.14 0.14 0.13 0.13 0.14 0.14 0.14 0.14 0.14 0.14 0.14 0.14 0.14 0.14 0.14 0.14 0.14 0.14 0.14 0.01 .001
0.13 0.13 0.14 0.14 0.13 0.10 0.10 0.11 0.06 0.13 0.11 0.09 0.13 0.11 0.13 0.13 0.12 0.12 0.07 0.15 0.12 0.11 0.09 0.12 0.02
modality [29]. In this study, the decrease in voice turbulence index means less deviance from normal voice, a fact that can be substantiated by the lack of hoarseness in all of the subjects while fasting and nonfasting. However, the lack of a perceptual evaluation prohibits us from clinically interpreting these acoustic changes. The phonatory results of this investigation might be attributed to 2 main factors: one is dehydration and second is the overall sum of metabolic and physiologic changes. This
Table 4 Laryngeal videostroboscopic findings
Polyp Nodule Edema Cyst Chronic laryngitis Lesions Mucus Granuloma Varix Sulcus NA indicates not applicable.
Nonfasting
Fasting
% present
% present
0 3.8 3.8 3.8 0 0 11.5 0 3.8 0
0 3.8 3.8 3.8 0 0 3.8 0 3.8 0
P
NA 1.00 1.00 1.00 NA NA 1.00 NA 1.00 NA
0.03 0.04 0.05 0.01 0.05 0.04 0.04 0.06 0.03 0.03 0.02 0.07 0.04 0.02 0.03 0.03 0.04 0.03 0.02 0.02 0.03 0.02 0.01 0.03 0.04 0.02 0.032 0.013 .045
0.03 0.04 0.02 0.02 0.02 0.03 0.03 0.04 0.02 0.03 0.03 0.02 0.03 0.02 0.02 0.02 0.02 0.03 0.02 0.03 0.03 0.01 0.03 0.02 0.02 0.03 0.025 0.007
12.17 14.58 14.42 17.87 19.62 26.59 12.49 10.94 30.43 21.30 25.07 14.79 27.57 17.95 31.18 18.11 26.42 20.64 34.78 17.82 13.84 19.01 18.60 33.80 15.00 8.69 20.14 7.24 .155
12.20 16.06 20.19 17.30 17.66 23.94 13.76 13.40 21.79 25.56 24.13 13.52 21.50 19.42 15.11 14.54 19.91 19.50 29.45 17.90 17.90 17.60 15.11 18.68 14.91 13.93 18.27 4.25
129.19 148.89 122.79 111.65 124.80 127.30 118.32 119.21 97.30 129.51 151.39 110.09 157.34 77.37 131.45 133.93 101.37 134.40 130.89 125.03 119.18 118.70 159.46 128.89 137.20 184.22 128.07 21.32 .018
125.70 156.98 116.92 104.50 125.70 121.33 124.79 111.25 103.15 123.43 138.79 107.11 144.89 82.93 123.97 122.92 103.29 129.60 133.31 117.17 115.27 117.38 138.00 133.47 138.63 126.21 122.57 15.39
attribution remains hypothetical in the absence of scientific measures of hydration and/or metabolic changes in our group. Fasting overnight has been shown to lead to fluid deficit measured up to 1 L after 8 hours of abstinence [30]. The intermittent lack of water and food intake during fasting on well-being can lead to metabolic changes and dehydration [31]. Weight loss between 0.1 and 1.4 kg of body weight, and signs of dehydration are invariably encountered [32-34]. This loss of water secondary to fasting itself during the month of Ramadan results in a degree of dehydration that may partly explain the increase in the phonatory effort in men and women and the prevalence of vocal fatigue in women. In addition, other hypotheses behind vocal fatigue in women besides increased vocal fold viscosity may include neuromuscular fatigue, reduced blood circulation, nonmuscular tissue strain, and respiratory muscle fatigue. The second factor that may explain the phonatory results of this study besides dehydration is the sum of the metabolic and physiologic changes occurring during Ramadan. Fasting submits the body to intermittent metabolic changes that affect all the systems in the body [31-34]. The hormonal changes accompanying dehydration while fasting have been shown to affect the cardiorespiratory system as well as circadian rhythm. Consequently, the ventilatory responses and breath support are reduced. As a result, vocal fatigue and
128
A. Hamdan et al. / American Journal of Otolaryngology–Head and Neck Medicine and Surgery 32 (2011) 124–129
an increase in phonatory effort may be more prevalent, especially in strenuous vocal tasks. The sense of effort has also been shown to increase with expiratory and inspiratory muscle loading, indicating that a prolonged strenuous breathing task can result in an increase sense of effort for breathing [35-37]. Hence, the lack of water and food intake while fasting has an effect on both the phonatory and respiratory systems. The resultant respiratory muscle fatigue can be translated as vocal fatigue as shown in the study on women and as an increase in phonatory effort and a decrease in maximum phonation time in both man and women [38,39]. Vocal fatigue has been associated with changes in other acoustic parameters, such as the habitual pitch, fundamental frequency, and perturbation parameters. These acoustic changes are not consistently present in all studies [40-43] and were absent in the study on women. Despite the lack of an increase in the prevalence of vocal fatigue in men, in the investigation here, there was a mild nonsignificant increase in the fundamental frequency and a significant decrease in habitual pitch. The increase in the fundamental frequency can be explained on the basis of dehydration and the known inverse relationship between mass and vocal pitch. The decrease in the maximum phonation time can be explained on the basis of a decrease in the breath support and control often witnessed in cases of vocal fatigue [44]. The laryngostroboscopic findings in this study did not change with fasting, even though an increase in vocal fold viscosity and an increase in the mucus secondary to dehydration would have been anticipated. On the contrary, there was a reduction in the amount of mucus in one subject. Of course this has no significance in view of the scarcity of its occurrence. Stroboscopic changes that are often reported in patients with vocal fatigue [8,45-47] were not present in this study. This could have been attributed to the fact that vocal fatigue was not significantly altered in the study. This study carries 2 limitations: one is the lack of measures of hydration such as weight loss or other parameters and second is the presence of confounding factors such as reflux and metabolic changes that might coexist in subjects while fasting and could affect the variables that we investigated. Nevertheless, this investigation sheds further information on the vocal symptoms associated with abstention of water and food intake while fasting.
5. Conclusion Fasting results in an increase in phonatory effort in males. The increase might be theoretically attributed either to dehydration or to a possible decrease in muscular endurance while fasting. Further studies investigating the level of hydration and metabolic changes while fasting will lead to a better understanding of the changes in patients' reported phonatory effort. People who fast are advised to increase their water intake before fasting and decrease the vocally fatiguing tasks that can predispose to vocal disorders.
References [1] Chan RW, Tayama N. Biomechanical effects of hydration in vocal fold tissues. Otolaryngol Head Neck Surg 2002;126:528-37. [2] Finkelhor BK, Titze IR, Durham PL. The effect of viscosity changes in the vocal folds on the range of oscillation. J Voice 1988;1:320-5. [3] Jiang J, Ng J, Hanson D. The effects of rehydration on phonation in excised canine larynges. J Voice 1999;13:51-9. [4] Jiang JJ, Verdolini KN, Hanson DG. Effects of dehydration on phonation. Annals Otol Rhinol Laryngol 2000;109:568-75. [5] Verdolini K, Titze IR, Fennell A. Dependence of phonatory effort on hydration level. J Speech Hear Res 1994;37:1001-7. [6] Verdolini-Martson K, Titze IR, Druker DG. Changes in phonation threshold pressure with induced conditions of hydration. J Voice 1990;4:142-51. [7] Verdolini K, Min Y, Titze IR, et al. Biological mechanisms underlying voice changes due to dehydration. J Speech Lang Hear Res 2002;45:268-81. [8] Solomon NP, DiMattia MS. Effects of a vocally fatiguing task and systemic hydration on phonation threshold pressure. J Voice 2000;14:341-62. [9] Hamdan AL, Siabi A, Rameh C. Effect of fasting on voice. J Voice 2006;21:495-501. [10] Roky R, Houti I, Moussamih S, et al. Physiological and chronobiological changes during Ramadan intermittent fasting. Ann Nutr Metab 2004;48:296-303. [11] Butler JE, Hammond TH, Gray SD. Gender related differences of hyaluronic acid distribution in the human vocal fold. Laryngoscope 2001;111:907-11. [12] Angel JF, Schwartz NE. Metabolic changes resulting from decreased meal frequency in adult male Muslims during the Ramadan fast. Nutr Rep Int 1975;11:29-38. [13] Frost G, Pirani S. Meal frequency and nutritional intake during Ramadan: A pilot study. Hum Nutr Clin Nutr 1987;41:47-50. [14] Finch GM, Day JE, Razak, et al. Appetite changes under free-living conditions during Ramadan fasting. Appetite 1998;31:159-70. [15] Taoudi-Benchekroun M, Roky R, Toufiq J, et al. Epidemiological study: chronotype and daytime sleepiness before and during Ramadan. Therapie 1999;54:567-72. [16] Born M, Elmadfa I, Schmahl FW. Effects of periodic fluid and food withdrawal. An inquiry conducted during the month of Ramadan in foreign workers. Munch Med Wochenschr 1979;121: 1569-72. [17] Husain R, Duncan MT, Cheah SH, et al. Effects of fasting in Ramadan on tropical Asiatic Moslems. Br J Nutr 1987;58:41-8. [18] El Arnoaty YM, Johnson WA. Nutritional and biochemical changes during Ramadan fasting. FASEB J 1991;5:1665. [19] Sliman NA, Khatib FA. Effect of fasting Ramadan on body weight and some blood constituents of healthy Muslims. Nutr Rep Int 1988;38:1299-306. [20] Takruri HR. Effect of fasting in Ramadan on body weight. Saudi Med J 1989;10:491-4. [21] Iraki L, Bogdan A, Hakkou F, et al. Ramadan diet restrictions modify the circadian time structure in humans. A study on plasma gastrin, insulin, glucose and calcium and on gastric pH. J Clin Endocrinol Metab 1997;82:1261-73. [22] Adlouni A, Ghalim N, Benslimane A, et al. Fasting during Ramadan induces a marked increase in high-density lipoprotein cholesterol and decrease in low-density lipoprotein cholesterol. Ann Nutr Metab 1997;41:242-9. [23] Nagra SA, Rahman ZU, Javaria M, et al. Study of some biochemical parameters in young women as affected by Ramadan fasting. Int J Ramadan Fasting Res 1998;2:1-4. [24] Sarraf-Zadegan N, Atashi M, Naderi GA, et al. The effect of fasting in Ramadan on the values and interrelations between biochemical, coagulation and haematological factors. Ann Saudi Med 2000;20: 377-81.
A. Hamdan et al. / American Journal of Otolaryngology–Head and Neck Medicine and Surgery 32 (2011) 124–129 [25] Nomani MZ, Hallak MH, Siddiqui IP. Effect of Ramadan fasting on plasma uric acid and body weight in healthy men. J Am Diet Assoc 1990;90:1435-6. [26] Cheah SH, Ch'ng SL, Hussain R, et al. Effects of fasting during Ramadan on urinary excretion in Malaysian Muslims. Br J Nutr 1990;63:329-37. [27] Ramadan J, Telahoun G, Al-Zaid NS, et al. Responses to exercise, fluid, and energy balances during Ramadan in sedentary and active males. Nutrition 1999;15:735-9. [28] Zebidi A, Rached S, Dhidah M, et al. Effets du jeune de Ramadan sur certains parameters plasmatiques et urinaires. Tunis Med 1990;68:367-71. [29] Bhuta T, Patrick L, Garnett JD. Perceptula evaluation of voice quality and its correlation with acoustic measurements. J Voice 2004;18: 299-304. [30] Holte K, Kehlet H. Compensatory fluid administration for preoperative dehydration: does it improve outcome? Acta Anaesthesiol Scand 2002;46:1089-93. [31] Sweileh N, Schnitzler A, Hunter GR, et al. Body composition and energy metabolism in resting and exercising Muslims during Ramadan fast. J Sorts Med Phys Fitness 1992;32:156-63. [32] Mosek A, Korczyn AD. Fasting headache, weight loss and dehydration. Headache 1999;39:225-7. [33] Dadeya S, Kamlesh, Shibal F, et al. Effect of religious fasting on intraocular pressure. Eye 2002;16:463-5. [34] Kayikcioglu O, Guler C. Religious fasting and intraocular pressure. J Glaucoma 2000;9:413-4. [35] Suzuki S, Suzuki J, Ishii T, et al. Relationship of respiratory effort sensation to expiratory threshold loading. Am Rev Respir Dis 1992;145:461-6. [36] Gandevia SC, Killian KJ, Campbell EJ. The effect of respiratory muscle fatigue on respiratory sensations. Clin Sci 1981;60:463-6.
129
[37] Supinski GS, Clary SJ, Bark H, et al. Effect of inspiratory muscle fatigue on perception of effort during loaded breathing. J Appl Physiol 1987;62:300-7. [38] McArdle WD, Katch FI, Katch VL. Exercise physiology: energy, nutrition and human performance. 4th ed. Baltimore: Williams & Wilkins; 1996. [39] Titze IR. Principles of voice production. Englewood Cliffs (N.J.): Prentice Hall; 1994. [40] Stone RE, Scharf DJ. Vocal change associated with the use of atypical pitch and intensity levels. Folia Phoniatr 1973;25: 91-103. [41] Neils LR, Yairi E. Effects of speaking in noise on vocal fatigue and vocal recovery. Folia Phoniatr 1987;39:104-12. [42] Vilkman E, Lauri E, Alku P, et al. Effects of prolonged oral reading on Fo, SPL, subglottal pressure, and amplitude characteristics of glottal flow waveforms. J Voice 1999;13:303-15. [43] Verstraete J, Forrez G, Mertens P, et al. The effect of sustained phonation at high and low pitch on vocal jitter and shimmer. Folia Phoniatr 1993;45:223-8. [44] Eustace CS, Stemple JC, Lee L. Objective measures of voice production in patients complaining of laryngeal fatigue. J Voice 1996;10:146-54. [45] Behrman A. Evidence-based treatment of paralytic dysphonia. Otolaryngol Clin N Am 2004;37:75-104. [46] Scherer RC, Titze IR, Raphael BN, et al. Vocal fatigue in a trained and untrained voice user. In: Baer T, Sasaki C, Harris K, editors. Laryngeal function in phonation and respiration. San Diego (CA): Singular Publishing Group; 1991. p. 533-55. [47] Stemple JC, Stanley J, Lee L. Objective measures of voice production in normal subjects following prolonged voice use. J Voice 1995;9: 127-33.