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For peer review only Chronic diseases and choking deaths among older adults Journal: BMJ Open Manuscript ID bmjopen-2015-009464 Article Type: Research Date Submitted by the Author: 21-Jul-2015 Complete List of Authors: Wu, Wen-Shiann; Department of Internal Medicine, Chi Mei Medical Center Cheng, Tain-Junn; Department of Neurology, Chi Mei Medical Center Sung, Kuan-Chin; Department of Neurosurgery, Chi Mei Medical Center Lu, Tsung-Hsueh; Institute of Public Health, College of Medicine, National Cheng Kung Universtiy <b>Primary Subject Heading</b>: Epidemiology Secondary Subject Heading: Epidemiology, Respiratory medicine, Medical management, Geriatric medicine, Public health Keywords: Epidemiology < TROPICAL MEDICINE, ACCIDENT & EMERGENCY MEDICINE, GERIATRIC MEDICINE, THORACIC MEDICINE, PUBLIC HEALTH For peer review only - http://bmjopen.bmj.com/site/about/guidelines.xhtml BMJ Open on May 28, 2021 by guest. Protected by copyright. http://bmjopen.bmj.com/ BMJ Open: first published as 10.1136/bmjopen-2015-009464 on 12 November 2015. Downloaded from
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Page 1: BMJ Open · Professor Tsung-Hsueh Lu, Department of Public Health, College of Medicine, National Cheng Kung University, No. 1, Dah Hsueh Road, Tainan 701, Taiwan Page 1 of 17

For peer review only

Chronic diseases and choking deaths among older adults

Journal: BMJ Open

Manuscript ID bmjopen-2015-009464

Article Type: Research

Date Submitted by the Author: 21-Jul-2015

Complete List of Authors: Wu, Wen-Shiann; Department of Internal Medicine, Chi Mei Medical Center

Cheng, Tain-Junn; Department of Neurology, Chi Mei Medical Center Sung, Kuan-Chin; Department of Neurosurgery, Chi Mei Medical Center Lu, Tsung-Hsueh; Institute of Public Health, College of Medicine, National Cheng Kung Universtiy

<b>Primary Subject Heading</b>:

Epidemiology

Secondary Subject Heading: Epidemiology, Respiratory medicine, Medical management, Geriatric medicine, Public health

Keywords: Epidemiology < TROPICAL MEDICINE, ACCIDENT & EMERGENCY MEDICINE, GERIATRIC MEDICINE, THORACIC MEDICINE, PUBLIC HEALTH

For peer review only - http://bmjopen.bmj.com/site/about/guidelines.xhtml

BMJ Open on M

ay 28, 2021 by guest. Protected by copyright.

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Chronic diseases and choking deaths among older adults

Wen-Shiann Wu,1,2 Tain-Junn Cheng,3,4 Kuan-Chin Sung,5 Tsung-Hsueh Lu,6

Wen-Shiann Wu and Tain-Junn Cheng are joint first authors

1Department of Internal Medicine, Chi Mei Medical Center, Tainan, Taiwan

2Department of Pharmacy, Chia Nan University of Pharmacy and Science, Tainan, Taiwan

3Department of Neurology, Occupational Medicine, Management in Medical Records and

Information, Chi Mei Medical Center, Tainan, Taiwan

4Department of Occupational Safety / Institute of Industrial Safety and Disaster Prevention,

College of Sustainable Environment, Chia Nan University of Pharmacy and Science, Tainan,

Taiwan

5Department of Neurosurgery, Chi Mei Medical Center, Tainan, Taiwan

6NCKU Research Center for Health Data and Department of Public Health, College of

Medicine, National Cheng Kung University, Tainan, Taiwan

*Correspondence to

Professor Tsung-Hsueh Lu, Department of Public Health, College of Medicine, National

Cheng Kung University, No. 1, Dah Hsueh Road, Tainan 701, Taiwan

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ABSTRACT

Objectives: To examine whether the strengths of the associations between chronic diseases

and overall choking differ from those of the associations between chronic diseases and only

food-related choking.

Design: This cross-sectional study used nationwide multiple-cause mortality files.

Setting: The United States.

Participants: Older adults aged 65 years or older died between 2009 and 2013.

Main outcome measures: Mortality ratio (observed/expected) of number of deaths with

both causes (chronic diseases and choking) and 95% confidence intervals.

Results: We identified 76 543 deaths for which the death certificates report choking (ICD-10

codes W78, W79, and W80 combined) as a cause of death and only 4974 (6.5%) deaths were

classified as food-related choking (ICD-10 code W79). Schizophrenia, Parkinson’s disease,

Alzheimer’s disease, and oral cancer are four chronic diseases that had significant

associations with both overall and food-related choking. Stroke, larynx cancer, and mood

(affective) disorders had significant associations with overall choking, but not with food-related

choking.

Conclusions: We suggest using overall choking instead of only food-related choking to

better describe the associations between chronic diseases and choking.

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Strengths and limitations of this study

� This study used nationwide population-based dataset.

� This study examined more chronic diseases than previous studies.

� Both chronic diseases and choking might be underreported on the death certificates by

the coroners or medical examiners.

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INTRODUCTION

Many older adults with chronic diseases experience dysphagia (difficulty in swallowing) and

have a higher risk of choking deaths.1-3

By using multiple-cause mortality files, one US study

determined that older adults whose death certificates report chronic diseases (such as Parkinson’s

disease and Alzheimer’s disease) exhibited a higher risk of having food-related choking as a

cause of death.4 However, inconsistent with the current knowledge that suggests that dysphagia

is a common problem among people with stroke,5-7

no significant association between stroke and

food-related choking was noted in that study. One possible explanation, as indicated by the

authors, is that the deaths of many older adults involving food-related choking were misclassified

as obstruction of the respiratory tract by an unspecified object.

Regarding the proper classification of national cause of death statistics, the three categories

related to choking listed in the International Statistical Classification of Diseases and Related

Health Problems, Tenth Revision (ICD-10) are as follows: ICD-10 code W78 “Inhalation of

gastric contents”, ICD-10 code W79 “Inhalation and ingestion of food causing obstruction of

respiratory tract” and ICD-10 code W80 “Inhalation and ingestion of other objects causing

obstruction of respiratory tract”.8 It is highly likely that many food-related choking deaths were

misclassified as ICD-10 code W80 instead of ICD-10 code W79. The problem of

misclassification would bias the estimation of the associations between chronic diseases and

choking deaths. Thus, we examined whether the strengths of the associations between chronic

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diseases and overall choking (ICD-10 codes W78, W79, and W80 combined) might differ from

those of the association between chronic diseases and only food-related choking (ICD-10 code

W79). Furthermore, we added more chronic diseases than those listed in the study of Kramarow

et al.,4 because one systematic review indicated that patients with some psychiatric disorders

have a higher risk of choking deaths.9

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DATA AND METHODS

The number of deaths among older adults in the United States aged 65 years or older for

which various types of chronic diseases and choking are listed on the death certificates for

2009 to 2013 were obtained from the Wide-ranging Online Data for Epidemiologic Research

of the Centers for Disease Control and Prevention (CDC WONDER).10

We used the method

used by Kramarow et al.4 to estimate the strengths of the associations between chronic

diseases and choking. The measure is the ratio of the observed deaths with mention of both

chronic diseases and choking to the expected joint frequency of the deaths with two causes,

assuming the two causes are independent.

The expected number of deaths is calculated as:

(Number of deaths with suffocation) � (Number of deaths with selected cause) / (Total

number of deaths from all causes)

The ratio is calculated as:

(Observed numbers of deaths with both causes) / (Expected numbers of deaths with both

causes)

The higher the ratio is, the stronger the associations between chronic diseases and choking.

According to the Poisson distribution, 95% confidence intervals (95% CIs) of the ratio were

estimated.

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RESULTS

For 76 543 older adults in the United States aged 65 years or older who died between 2009

and 2013, choking was reported as a cause of death (i.e., died with) on the death certificates,

and choking was assigned as the underlying cause of death (i.e., died from) in only one fifth

(21.6%) of the death certificates (Table 1). Furthermore, only 6.5% (4974) of overall choking

occurrences (ICD-10 codes W78, W79, and W80 combined) were classified as food-related

choking (ICD-10 codes W79).

As shown in Table 2, the percentage of death certificates reporting both chronic diseases

and overall choking as causes of death was the highest for patients with schizophrenia

(2.66%), followed by Parkinson’s disease (2.25%), larynx cancer (1.75%), and Alzheimer’s

disease (1.44%). However, the percentage of death certificates reporting both chronic

diseases and food-related choking as causes of death was the highest for patients with

schizophrenia (0.52%), followed by Parkinson’s disease (0.15%), oral cancer (0.09%), larynx

cancer (0.08%), mood (affective) disorders (0.07%), and Alzheimer’s disease (0.07%).

Seven chronic diseases were significantly associated with overall choking, with

significance ratios being higher than one; however, only four chronic diseases had significant

associations with food-related choking (Table 3). Chronic diseases associated with overall

choking at a ratio greater than one were ranked in the following order: schizophrenia,

Parkinson’s disease, larynx cancer, Alzheimer’s disease, oral cancer, stroke, and mood

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(affective) disorders. By contrast, chronic diseases associated with food-related choking were

ranked in the following order: schizophrenia, Parkinson’s disease, oral cancer, larynx cancer,

Alzheimer’s disease, and mood (affective) disorders.

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DISCUSSION

The findings of this study indicate that only 6.5% of all deaths with mention of any type of

choking were classified as food-related choking and nine of ten overall choking occurrences

were classified as obstruction of the respiratory tract by an unspecified object. We also found

that the strengths of the associations between chronic diseases and overall choking differed

from those of the associations between chronic diseases and only food-related choking.

Schizophrenia, Parkinson’s disease, Alzheimer’s disease, and oral cancer are four chronic

diseases that had significant associations with both overall and food-related choking. However,

stroke, larynx cancer, and mood (affective) disorders had significant associations with overall

choking and not with food-related choking.

In forensic studies,11-15

more than 95% of unintentional choking deaths among older adults

were food related and only a few choking deaths were due to foreign bodies other than food,

such as broken teeth or dentures. In other words, most of the cases coded as ICD-10 code

W80 were actually food-related choking cases. These misclassifications would certainly bias

the estimation of the strengths of the associations between chronic diseases and choking, as

indicated in this study. Reports of choking as a cause of death among older adults with stroke,

larynx cancer, and mood (affective) disorders could be overlooked if only food-related

choking is considered in assessments.

In the study of Kramarow et al.,4 only two chronic diseases (Parkinson’s disease and

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Alzheimer’s disease) had significant associations with food-related choking. We did not

include pneumonitis (aspiration pneumonia) and influenza and pneumonia in this study

because these two diagnoses are acute conditions. We identified five more chronic diseases

with significant associations with overall choking. Two of them were psychiatric disorders

(schizophrenia and mood [affective] disorders), two were cancers (oral cancer and larynx

cancer), and one was stroke, which is consistent with current knowledge. The caretakers of

older adults with chronic diseases and a higher risk of death from choking should pay close

attention to food preparation and carefully monitor patients during mealtimes.11

Despite using broader definitions for choking to include more cases in examining the

associations between chronic diseases and choking, this study had some limitations. First, our

analysis depended only on the information reported on the death certificates, and both chronic

diseases and choking might have been underreported by medical certifiers. Many sudden and

unexpected deaths occurring during meals because of accidental occlusion of the airway by

swallowed food might have been incorrectly attributed to acute myocardial infarction (i.e.,

café coronary), resulting in the underreporting of choking deaths.12

A choking death is an

unnatural death and should be certified by medical examiners or coroners. Different medical

examiners or coroners might have different opinions and habits in reporting chronic diseases

as the contributory causes of death. We assume that the underreporting of both choking and

chronic diseases is non-differential misclassification. Second, detailed information relevant to

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injury prevention programme design, such as the types of foods, mealtimes, and places of

injury, was not specifically recorded in the death certificates in most cases.

In conclusion, only a few food-related choking occurrences were correctly classified as

ICD-10 code W79, whereas most of the cases were classified as ICD-10 code W80.

Consequently, to effectively assess the strengths of the associations between chronic diseases

and choking, it is appropriate to use overall choking (i.e., combining ICD-10 codes W78,

W79, and W80) instead of only food-related choking. Moreover, the caretakers of older adults

with chronic diseases (schizophrenia, Parkinson’s disease, larynx cancer, Alzheimer’s disease,

oral cancer, stroke, and mood [affective] disorders) should be alert in preventing choking.

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Acknowledgment The authors thank Ms. Bai-Huan Lin for her efforts in data analyses.

Contributors THL conceived the study, guided the analyses, wrote the article draft, and is the

guarantor or the study. WSW, TJC, and KCS helped conduct the literature review, analysed

the data, interpreted the results, and critically revised the manuscript.

Funding This study was partially funded by the Ministry of Science and Technology of Taiwan

(NSC102-2314-B-006- 054) and partially funded by the Chi Mei & National Cheng Kung

University Joint Program (CMNCKU10410).

Competing interests None

Ethics approval This study was approved by the Institutional Review Board at National

Cheng Kung University.

Provenance and peer review Not commissioned; externally peer reviewed.

Data sharing statement No additional data available.

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REFERENCES

1. Forster A, Samaras N, Gold G, Samaras D. Oropharyngeal dysphagia in older adults:

a review. Eur Geriatr Med 2011;2:356-62.

2. Miller N, Patterson J. Dysphagia: implications for older people. Rev Clin Gerontol

2014;24:41-57.

3. Clave P, Shaker R. Dysphagia: current reality and scope of the problem. Nat Rev

Gastroenterol Hepatol 2015;12:259–70.

4. Kramarow E, Warner M, Chen LH. Food-related choking deaths among the elderly.

Inj Prev 2014;20:200-3.

5. Altman KW, Richards A, Goldberg L, Frucht S, McCabe DJ. Dysphagia in stroke,

neurodegenerative disease, and advanced dementia. Otolaryngol Clin N Am

2013;46:1137-49.

6. Chang CY, Cheng TJ, Lin CY, Chen JY, Lu TH, Kawachi I. Reporting of aspiration

pneumonia or choking as a cause of death in patients who died with stroke. Stroke

2013;44:1182-5.

7. Walshe M. Oropharyngeal dysphagia in neurodegenerative disease. J Gastroenterol

Hepatol Res 2014;3:1265-71.

8. World Health Organization. International Statistical Classification of Diseases and

Related Health Problems, Tenth Revision. Accessed at June 20, 2015,

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http://apps.who.int/classifications/icd10/browse/2015/en

9. Aldridge KJ, Taylor NF. Dysphagia is a common and serious problem for adults with

mental illness: a systematic review. Dysphagia 2012;27:124-37.

10. Centers for Disease Control and Prevention. CDC WONDER. Accessed at June 20,

2015, http://wonder.cdc.gov.

11. Berzlanovich AM, Fazeny-Dorner B, Waldhoer T, Fasching P, Keil W. Foreign body

asphyxia: a preventable cause of death in the elderly. Am J Prev Med 2005;28:65-9.

12. Wick R, Gilbert JD, Byard RW. Café coronary syndrome-fatal choking on food: an

autopsy approach. J Clin Forensic Med 2006;13:135-8.

13. Dolkas L, Stanley C, Smith AM, Vilke GM. Deaths associated with choking in San

Diego County. J Forensic Sci 2007;52:176-9.

14. Boghossian E, Tambuscio S, Sauvageau A. Nonchemical suffocation deaths in

forensic setting: a 6-year retrospective study of environmental suffocation,

smothering, choking, and traumatic/positional asphyxia. J Forensic Sci

2010;55:646-51.

15. Kikutani T, Tamura F, Tohara T, Takahashi N, Yaegaki K. Tooth loss as risk factor for

foreign-body asphyxiation in nursing-home patients. Arch Gerontol Geriatr

2012;54:e431-5.

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Table 1 Number of deaths for which choking was assigned as either the underlying cause of death (COD) or mentioned among older adults aged

65 years or older in the United States according to CDC WONDER for years 2009 to 2013

Underlying COD Mentioned Category of choking (ICD-10 codes) No % No % Overall choking (W78–W80) 16 531 100.0 76 543 100.0 Inhalation of gastric contents (W78) 804 4.9 2617 3.4 Inhalation and ingestion of food causing obstruction of respiratory tract (W79) 3113 18.8 4974 6.5 Inhalation and ingestion of other objects causing obstruction of respiratory tract (W80) 12 614 76.3 68 980 90.1

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Table 2 Number and percentage (%) of deaths with mention of chronic diseases (CDs) and choking on the death certificates among older adults

aged 65 years or older in the United States according to CDC WONDER for 2009 to 2013

Chronic disease (ICD-10 codes) With mention

of a CD With mention of a CD

and overall choking % With mention of a CD and

food-related choking % Oral cancer (C00–C14) 30 469 412 1.35 27 0.09 Esophageal cancer (C15) 49 860 391 0.78 6 0.01 Larynx cancer (C32) 15 391 270 1.75 12 0.08 Diabetes mellitus (E10–E14) 901 854 6329 0.70 430 0.05 Schizophrenia (F20–F29) 13 697 365 2.66 71 0.52 Mood (affective) disorders (F30–F39) 55 508 644 1.16 37 0.07 Parkinson's disease (G20–G21) 178 482 4024 2.25 273 0.15 Alzheimer's disease* (G30, F03) 1 502  141 21 692 1.44 1026 0.07 Heart disease (I00–I09, I11 ,I13 ,I20–I51) 4 441  643 27 398 0.62 1710 0.04 Stroke (I60–I69) 925 559 12 210 1.32 487 0.05 Chronic lower respiratory disease (J40–J47) 1 157  788 8360 0.72 271 0.02 Nephrotic disease (N00–N07, N17–N19, N25–N27) 940 209 6009 0.64 122 0.01 *Alzheimer's disease and related dementia

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Table 3 Number of observed (Obs) deaths, expected (Exp) deaths, and the ratio (Obs/Exp) for both chronic diseases and choking reported on the

death certificates among older adults aged 65 years or older in the United States according to CDC WONDER for 2009 to 2013

Overall choking Food-related choking Chronic disease Obs Exp Obs/Exp (95% CI) Obs Exp Obs/Exp (95% CI) Schizophrenia 365 115 3.19 (2.87–3.53) 71 7 9.54 (7.92–12.8) Parkinson's disease 4024 1492 2.70 (2.61–2.78) 273 97 2.82 (2.49–3.17) Larynx cancer 270 129 2.10 (1.86–2.36) 12 8 1.44 (0.74–2.51) Alzheimer's disease* 21 692 12 559 1.73 (1.70–1.75) 1026 816 1.26 (1.18–1.34) Oral cancer 412 255 1.62 (1.46–1.78) 27 17 1.63 (1.07–2.38) Stroke 12 210 7739 1.58 (1.55–1.61) 487 503 0.97 (0.88–1.06) Mood (affective) disorders 644 464 1.39 (1.28–1.50) 37 30 1.23 (0.87–1.70) Esophageal cancer 391 417 0.94 (0.85–1.04) 6 27 0.22 (0.08–0.49) Diabetes mellitus 6329 7540 0.84 (0.82–0.86) 430 490 0.88 (0.80–0.96) Chronic lower respiratory disease 8360 9680 0.86 (0.85–0.88) 271 629 0.43 (0.38–0.49) Nephrotic disease 6009 7861 0.76 (0.75–0.78) 122 511 0.24 (0.20–0.29) Heart disease 27 398 37 137 0.74 (0.73–0.75) 1710 2413 0.71 (0.68–0.74) *Alzheimer's disease and related dementia

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Associations between chronic diseases and choking deaths among older adults in the United States: a cross-sectional

study using multiple-cause mortality data from 2009 to 2013

Journal: BMJ Open

Manuscript ID bmjopen-2015-009464.R1

Article Type: Research

Date Submitted by the Author: 29-Aug-2015

Complete List of Authors: Wu, Wen-Shiann; Department of Internal Medicine, Chi Mei Medical Center Sung, Kuan-Chin; Department of Neurosurgery, Chi Mei Medical Center Cheng, Tain-Junn; Department of Neurology, Chi Mei Medical Center Lu, Tsung-Hsueh; Institute of Public Health, College of Medicine, National Cheng Kung Universtiy,

<b>Primary Subject Heading</b>:

Epidemiology

Secondary Subject Heading: Epidemiology, Respiratory medicine, Medical management, Geriatric medicine, Public health

Keywords: Epidemiology < TROPICAL MEDICINE, ACCIDENT & EMERGENCY

MEDICINE, GERIATRIC MEDICINE, THORACIC MEDICINE, PUBLIC HEALTH

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1

Associations between chronic diseases and choking deaths among

older adults in the United States: a cross-sectional study using

multiple-cause mortality data from 2009 to 2013

Wen-Shiann Wu,1,2 Kuan-Chin Sung,3 Tain-Junn Cheng,3,5 Tsung-Hsueh Lu,6

Wen-Shiann Wu and Kuan-Chin Sung are joint first authors

1Department of Internal Medicine, Chi Mei Medical Center, Tainan, Taiwan

2Department of Pharmacy, Chia Nan University of Pharmacy and Science, Tainan, Taiwan

3Department of Neurosurgery, Chi Mei Medical Center, Tainan, Taiwan

4Department of Neurology, Occupational Medicine, Management in Medical Records and

Information, Chi Mei Medical Center, Tainan, Taiwan

5Department of Occupational Safety / Institute of Industrial Safety and Disaster Prevention,

College of Sustainable Environment, Chia Nan University of Pharmacy and Science, Tainan,

Taiwan

6NCKU Research Center for Health Data and Department of Public Health, College of

Medicine, National Cheng Kung University, Tainan, Taiwan

*Correspondence to

Dr. Tain-Junn Cheng, Department of Neurology, Chi Mei Medical Center, ,No.901, Zhonghua

Rd., Yongkang Dist., Tainan City 701, Taiwan

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ABSTRACT

Objectives: To examine whether the strengths of the associations between chronic diseases

and overall choking differ from those of the associations between chronic diseases and only

food-related choking.

Design: This cross-sectional study used nationwide multiple-cause mortality files.

Setting: The United States.

Participants: Older adults aged 65 years or older died between 2009 and 2013.

Main outcome measures: Mortality ratio (observed/expected) of number of deaths with

both causes (chronic diseases and choking) and 95% confidence intervals.

Results: We identified 76 543 deaths for which the death certificates report choking (ICD-10

codes W78, W79, and W80 combined) as a cause of death and only 4974 (6.5%) deaths were

classified as food-related choking (ICD-10 code W79). Schizophrenia, Parkinson’s disease,

Alzheimer’s disease, and oral cancer are four chronic diseases that had significant

associations with both overall and food-related choking. Stroke, larynx cancer, and mood

(affective) disorders had significant associations with overall choking, but not with food-related

choking.

Conclusions: We suggest using overall choking instead of only food-related choking to

better describe the associations between chronic diseases and choking.

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Strengths and limitations of this study

� This study used nationwide population-based dataset.

� This study examined more chronic diseases than previous studies.

� Both chronic diseases and choking might be underreported on the death certificates by

the coroners or medical examiners.

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INTRODUCTION

Many older adults with chronic diseases experience dysphagia (difficulty in swallowing) and

have a higher risk of choking deaths.1-3

By using multiple-cause mortality files, one US study

determined that older adults whose death certificates report chronic diseases (such as Parkinson’s

disease and Alzheimer’s disease) exhibited a higher risk of having food-related choking as a

cause of death.4 However, inconsistent with the current knowledge that suggests that dysphagia

is a common problem among people with stroke,5-7

no significant association between stroke and

food-related choking was noted in that study. One possible explanation, as indicated by the

authors, is that the deaths of many older adults involving food-related choking were misclassified

as obstruction of the respiratory tract by an unspecified object.

Regarding the proper classification of national cause of death statistics, the three categories

related to choking listed in the International Statistical Classification of Diseases and Related

Health Problems, Tenth Revision (ICD-10) are as follows: ICD-10 code W78 “Inhalation of

gastric contents”, ICD-10 code W79 “Inhalation and ingestion of food causing obstruction of

respiratory tract” and ICD-10 code W80 “Inhalation and ingestion of other objects causing

obstruction of respiratory tract”.8 It is highly likely that many food-related choking deaths were

misclassified as ICD-10 code W80 instead of ICD-10 code W79. The problem of

misclassification would bias the estimation of the associations between chronic diseases and

choking deaths. Thus, we examined whether the strengths of the associations between chronic

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diseases and overall choking (ICD-10 codes W78, W79, and W80 combined) might differ from

those of the association between chronic diseases and only food-related choking (ICD-10 code

W79). Furthermore, we added more chronic diseases than those listed in the study of Kramarow

et al.,4 because one systematic review indicated that patients with some psychiatric disorders

have a higher risk of choking deaths.9

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DATA AND METHODS

The number of deaths among older adults in the United States aged 65 years or older for

which various types of chronic diseases and choking are listed on the death certificates for

2009 to 2013 were obtained from the Wide-ranging Online Data for Epidemiologic Research

of the Centers for Disease Control and Prevention (CDC WONDER).10

To examine the magnitude of the association between particular chronic disease and

choking we used the ratio method proposed by Israel et al.11

This method consists of

calculating the ratio of the number of observed pairs (O) of causes to the expected number (E)

of pairs of causes based on the assumption of independence. An O/E ratio greater than 1

indicates that more deaths with paired causes were reported than could be expected by

chance if the paired causes were independent. This method has been used by many

scholars.4,12-15

The expected number of deaths is calculated as:

(Number of deaths with mention of choking) � (Number of deaths with mention of

particular chronic disease) / (Total number of deaths from all causes)

The ratio is calculated as:

(Observed numbers of deaths with mention of both particular chronic disease and choking) /

(Expected numbers of deaths with both causes)

We also estimated 95% confidence intervals (95% CIs) of O/E ratio according to the Poisson

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distribution.

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RESULTS

For 76 543 older adults in the United States aged 65 years or older who died between 2009

and 2013, choking was reported as a cause of death (i.e., died with) on the death certificates,

and choking was assigned as the underlying cause of death (i.e., died from) in only one fifth

(21.6%) of the death certificates (Table 1). Furthermore, only 6.5% (4974) of overall choking

occurrences (ICD-10 codes W78, W79, and W80 combined) were classified as food-related

choking (ICD-10 codes W79).

As shown in Table 2, the percentage of death certificates reporting both chronic diseases

and overall choking as causes of death was the highest for patients with schizophrenia

(2.66%), followed by Parkinson’s disease (2.25%), larynx cancer (1.75%), and Alzheimer’s

disease (1.44%). However, the percentage of death certificates reporting both chronic

diseases and food-related choking as causes of death was the highest for patients with

schizophrenia (0.52%), followed by Parkinson’s disease (0.15%), oral cancer (0.09%), larynx

cancer (0.08%), mood (affective) disorders (0.07%), and Alzheimer’s disease (0.07%).

Seven chronic diseases were significantly associated with overall choking, with

significance ratios being higher than one; however, only four chronic diseases had significant

associations with food-related choking (Table 3). Chronic diseases associated with overall

choking at a ratio greater than one were ranked in the following order: schizophrenia,

Parkinson’s disease, larynx cancer, Alzheimer’s disease, oral cancer, stroke, and mood

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(affective) disorders. By contrast, chronic diseases associated with food-related choking were

ranked in the following order: schizophrenia, Parkinson’s disease, oral cancer, larynx cancer,

Alzheimer’s disease, and mood (affective) disorders.

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DISCUSSION

The findings of this study indicate that only 6.5% of all deaths with mention of any type of

choking were classified as food-related choking and nine of ten overall choking occurrences

were classified as obstruction of the respiratory tract by an unspecified object. We also found

that the strengths of the associations between chronic diseases and overall choking differed

from those of the associations between chronic diseases and only food-related choking.

Schizophrenia, Parkinson’s disease, Alzheimer’s disease, and oral cancer are four chronic

diseases that had significant associations with both overall and food-related choking. However,

stroke, larynx cancer, and mood (affective) disorders had significant associations with overall

choking and not with food-related choking.

Some forensic studies, suggested that majority of unintentional choking deaths among

older adults were food related and only a few choking deaths were due to foreign bodies other

than food, such as broken teeth or dentures.16-20

However, using mortality data alone, we

really don’t know what proportion of the deaths coded W80 involve food. Even if most of the

“other objects” are in fact food (which is likely), there could be differences in the rates of

“mis-coding” by various factors (demographic, geographic etc.) that would affect our

interpretation of this misclassification. These misclassifications would certainly bias the

estimation of the strengths of the associations between chronic diseases and choking, as

indicated in this study. Reports of choking as a cause of death among older adults with stroke,

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larynx cancer, and mood (affective) disorders could be overlooked if only food-related

choking is considered in assessments.

In the study of Kramarow et al.,4 only two chronic diseases (Parkinson’s disease and

Alzheimer’s disease) had significant associations with food-related choking. We did not

include pneumonitis (aspiration pneumonia) and influenza and pneumonia in this study

because these two diagnoses are acute conditions. We identified five more chronic diseases

with significant associations with overall choking. Two of them were psychiatric disorders

(schizophrenia and mood [affective] disorders), two were cancers (oral cancer and larynx

cancer), and one was stroke, which is consistent with current knowledge. The caretakers of

older adults with chronic diseases and a higher risk of death from choking should pay close

attention to food preparation and carefully monitor patients during mealtimes.16

However,

caution should be noted on the relative magnitude of these deaths. For example, schizophrenia

was mentioned on death certificates for approximately 2700 deaths per year, while

Alzheimer’s and dementia account for about 300,000 deaths per year. The importance and

public health significance of the connection between particular chronic disease and choking

should be mindful of the absolute numbers as well as the relative associations.

Despite using broader definitions for choking to include more cases in examining the

associations between chronic diseases and choking, this study had some limitations. First, our

analysis depended only on the information reported on the death certificates, and both chronic

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diseases and choking might have been underreported by medical certifiers. Many sudden and

unexpected deaths occurring during meals because of accidental occlusion of the airway by

swallowed food might have been incorrectly attributed to acute myocardial infarction (i.e.,

café coronary), resulting in the underreporting of choking deaths.17

A choking death is an

unnatural death and should be certified by medical examiners or coroners. Different medical

examiners or coroners might have different opinions and habits in reporting chronic diseases

as the contributory causes of death. We assume that the underreporting of both choking and

chronic diseases is non-differential misclassification.

Second, detailed information relevant to injury prevention programme design, such as the

types of foods, mealtimes, and places of injury, was not specifically recorded in the death

certificates in most cases. Furthermore, we did not have information of the level of

dependence on particular chronic disease. The dead with very dependent especially in

degenerative diseases with a high prevalence of dysphagia is difficult to attribute death by

choking food. It is not surprising that the choking are more common in patients with

psychiatric illness (schizophrenia) or Parkinson's disease with low functional dependence.

In conclusion, only a few food-related choking occurrences were correctly classified as

ICD-10 code W79, whereas most of the cases were classified as ICD-10 code W80.

Consequently, to effectively assess the strengths of the associations between chronic diseases

and choking, it is appropriate to use overall choking (i.e., combining ICD-10 codes W78,

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W79, and W80) instead of only food-related choking. Moreover, the caretakers of older adults

with chronic diseases (schizophrenia, Parkinson’s disease, larynx cancer, Alzheimer’s disease,

oral cancer, stroke, and mood [affective] disorders) should be alert in preventing choking.

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Acknowledgment The authors thank Ms. Bai-Huan Lin for her efforts in data analyses.

Contributors THL conceived the study, guided the analyses, wrote the article draft, and is the

guarantor or the study. WSW, TJC, and KCS helped conduct the literature review, analysed

the data, interpreted the results, and critically revised the manuscript.

Funding This study was partially funded by the Ministry of Science and Technology of Taiwan

(NSC102-2314-B-006- 054) and partially funded by the Chi Mei & National Cheng Kung

University Joint Program (CMNCKU10410).

Competing interests None

Ethics approval This study was approved by the Institutional Review Board at National

Cheng Kung University.

Provenance and peer review Not commissioned; externally peer reviewed.

Data sharing statement No additional data available.

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REFERENCES

1. Forster A, Samaras N, Gold G, Samaras D. Oropharyngeal dysphagia in older adults:

a review. Eur Geriatr Med 2011;2:356-62.

2. Miller N, Patterson J. Dysphagia: implications for older people. Rev Clin Gerontol

2014;24:41-57.

3. Clave P, Shaker R. Dysphagia: current reality and scope of the problem. Nat Rev

Gastroenterol Hepatol 2015;12:259–70.

4. Kramarow E, Warner M, Chen LH. Food-related choking deaths among the elderly.

Inj Prev 2014;20:200-3.

5. Altman KW, Richards A, Goldberg L, Frucht S, McCabe DJ. Dysphagia in stroke,

neurodegenerative disease, and advanced dementia. Otolaryngol Clin N Am

2013;46:1137-49.

6. Chang CY, Cheng TJ, Lin CY, Chen JY, Lu TH, Kawachi I. Reporting of aspiration

pneumonia or choking as a cause of death in patients who died with stroke. Stroke

2013;44:1182-5.

7. Walshe M. Oropharyngeal dysphagia in neurodegenerative disease. J Gastroenterol

Hepatol Res 2014;3:1265-71.

8. World Health Organization. International Statistical Classification of Diseases and

Related Health Problems, Tenth Revision. Accessed at June 20, 2015,

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http://apps.who.int/classifications/icd10/browse/2015/en

9. Aldridge KJ, Taylor NF. Dysphagia is a common and serious problem for adults with

mental illness: a systematic review. Dysphagia 2012;27:124-37.

10. Centers for Disease Control and Prevention. CDC WONDER. Accessed at June 20,

2015, http://wonder.cdc.gov.

11. Israel RA, Rosenberg HM, Curtin LM. Analytical potential for multiple cause-of-death

data. Am J Epidemiol 1986;124:161–79.

12. Coste J, Jougla E. Mortality from rheumatoid arthritis in France, 1970-1990. Int J

Epidemiol 1994;23:545-552.

13. Ziade N, Jourgla E, Coste J. Population-level influence of rheumatoid arthritis on

mortality and recent trends: a multiple cause-of-death analysis in France, 1970-2002.

J Rheumatol 2008;35:1950-1957.

14. Ascoli V, Minelli G, Kanieff M, Crialesi R, Frova L, Conti S. Cause-specific mortality in

classic Kaposi’s sarcoma: a population-based study in Italy (1995-2002). Br J Cancer

2009;101:1085-1090.

15. Souza DCC, Santo AH, Sato EI. Mortality profile related to systematic lupus

erythematosus: a multiple cause-of-death analysis. J Rheumatol 2012;39:496-503.

16. Berzlanovich AM, Fazeny-Dorner B, Waldhoer T, Fasching P, Keil W. Foreign body

asphyxia: a preventable cause of death in the elderly. Am J Prev Med 2005;28:65-9.

17. Wick R, Gilbert JD, Byard RW. Café coronary syndrome-fatal choking on food: an

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autopsy approach. J Clin Forensic Med 2006;13:135-8.

18. Dolkas L, Stanley C, Smith AM, Vilke GM. Deaths associated with choking in San

Diego County. J Forensic Sci 2007;52:176-9.

19. Boghossian E, Tambuscio S, Sauvageau A. Nonchemical suffocation deaths in

forensic setting: a 6-year retrospective study of environmental suffocation,

smothering, choking, and traumatic/positional asphyxia. J Forensic Sci

2010;55:646-51.

20. Kikutani T, Tamura F, Tohara T, Takahashi N, Yaegaki K. Tooth loss as risk factor for

foreign-body asphyxiation in nursing-home patients. Arch Gerontol Geriatr

2012;54:e431-5.

.

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Table 1 Number of deaths for which choking was assigned as either the underlying cause of death (COD) or mentioned among older adults aged

65 years or older in the United States according to CDC WONDER for years 2009 to 2013

Underlying COD Mentioned Category of choking (ICD-10 codes) No % No % Overall choking (W78–W80) 16 531 100.0 76 543 100.0 Inhalation of gastric contents (W78) 804 4.9 2617 3.4 Inhalation and ingestion of food causing obstruction of respiratory tract (W79) 3113 18.8 4974 6.5 Inhalation and ingestion of other objects causing obstruction of respiratory tract (W80) 12 614 76.3 68 980 90.1

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Table 2 Number and percentage (%) of deaths where choking was mentioned* among the deaths aged 65 years or older where the particular

chronic disease was mentioned in the United States according to CDC WONDER for 2009 to 2013

Chronic disease (ICD-10 codes)

Particular chronic disease was mentioned

Particular chronic disease and overall choking were both

mentioned %

Particular chronic disease and food-

related choking were both mentioned %

Oral cancer (C00–C14) 30 469 412 1.35 27 0.09 Esophageal cancer (C15) 49 860 391 0.78 6 0.01 Larynx cancer (C32) 15 391 270 1.75 12 0.08 Diabetes mellitus (E10–E14) 901 854 6329 0.70 430 0.05 Schizophrenia (F20–F29) 13 697 365 2.66 71 0.52 Mood (affective) disorders (F30–F39) 55 508 644 1.16 37 0.07 Parkinson's disease (G20–G21) 178 482 4024 2.25 273 0.15 Alzheimer's disease (G30, F03) 1 502  141 21 692 1.44 1026 0.07 Heart disease (I00–I09, I11 ,I13 ,I20–I51) 4 441  643 27 398 0.62 1710 0.04 Stroke (I60–I69) 925 559 12 210 1.32 487 0.05 Chronic lower respiratory disease (J40–J47) 1 157  788 8360 0.72 271 0.02 Nephrotic disease (N00–N07, N17–N19, N25–N27) 940 209 6009 0.64 122 0.01 * “Mention” can be as either an underlying or a contributory cause of death

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Table 3 Number of observed (Obs) deaths, expected (Exp) deaths, and the ratio (Obs/Exp) of deaths where particular chronic disease and

choking were both mentioned* among the deaths aged 65 years or older where the particular chronic disease was mentioned in the United

States according to CDC WONDER for 2009 to 2013

Overall choking Food-related choking Chronic disease Obs Exp Obs/Exp (95% CI) Obs Exp Obs/Exp (95% CI) Schizophrenia 365 115 3.19 (2.87–3.53) 71 7 9.54 (7.92–12.8) Parkinson's disease 4024 1492 2.70 (2.61–2.78) 273 97 2.82 (2.49–3.17) Larynx cancer 270 129 2.10 (1.86–2.36) 12 8 1.44 (0.74–2.51) Alzheimer's disease* 21 692 12 559 1.73 (1.70–1.75) 1026 816 1.26 (1.18–1.34) Oral cancer 412 255 1.62 (1.46–1.78) 27 17 1.63 (1.07–2.38) Stroke 12 210 7739 1.58 (1.55–1.61) 487 503 0.97 (0.88–1.06) Mood (affective) disorders 644 464 1.39 (1.28–1.50) 37 30 1.23 (0.87–1.70) Esophageal cancer 391 417 0.94 (0.85–1.04) 6 27 0.22 (0.08–0.49) Diabetes mellitus 6329 7540 0.84 (0.82–0.86) 430 490 0.88 (0.80–0.96) Chronic lower respiratory disease 8360 9680 0.86 (0.85–0.88) 271 629 0.43 (0.38–0.49) Nephrotic disease 6009 7861 0.76 (0.75–0.78) 122 511 0.24 (0.20–0.29) Heart disease 27 398 37 137 0.74 (0.73–0.75) 1710 2413 0.71 (0.68–0.74) * “Mention” can be as either an underlying or a contributory cause of death

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STROBE Statement—Checklist of items that should be included in reports of cross-sectional studies

Item

No Recommendation

Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the abstract

(b) Provide in the abstract an informative and balanced summary of what was done

and what was found

Introduction

Background/rationale 2 Explain the scientific background and rationale for the investigation being reported

Objectives 3 State specific objectives, including any prespecified hypotheses

Methods

Study design 4 Present key elements of study design early in the paper

Setting 5 Describe the setting, locations, and relevant dates, including periods of recruitment,

exposure, follow-up, and data collection

Participants 6 (a) Give the eligibility criteria, and the sources and methods of selection of

participants

Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders, and effect

modifiers. Give diagnostic criteria, if applicable

Data sources/

measurement

8* For each variable of interest, give sources of data and details of methods of

assessment (measurement). Describe comparability of assessment methods if there is

more than one group

Bias 9 Describe any efforts to address potential sources of bias

Study size 10 Explain how the study size was arrived at

Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If applicable,

describe which groupings were chosen and why

Statistical methods 12 (a) Describe all statistical methods, including those used to control for confounding

(b) Describe any methods used to examine subgroups and interactions

(c) Explain how missing data were addressed

(d) If applicable, describe analytical methods taking account of sampling strategy

(e) Describe any sensitivity analyses

Results

Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially

eligible, examined for eligibility, confirmed eligible, included in the study,

completing follow-up, and analysed

(b) Give reasons for non-participation at each stage

(c) Consider use of a flow diagram

Descriptive data 14* (a) Give characteristics of study participants (eg demographic, clinical, social) and

information on exposures and potential confounders

(b) Indicate number of participants with missing data for each variable of interest

Outcome data 15* Report numbers of outcome events or summary measures

Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and

their precision (eg, 95% confidence interval). Make clear which confounders were

adjusted for and why they were included

(b) Report category boundaries when continuous variables were categorized

(c) If relevant, consider translating estimates of relative risk into absolute risk for a

meaningful time period

Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and

sensitivity analyses

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Discussion

Key results 18 Summarise key results with reference to study objectives

Limitations 19 Discuss limitations of the study, taking into account sources of potential bias or

imprecision. Discuss both direction and magnitude of any potential bias

Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations,

multiplicity of analyses, results from similar studies, and other relevant evidence

Generalisability 21 Discuss the generalisability (external validity) of the study results

Other information

Funding 22 Give the source of funding and the role of the funders for the present study and, if

applicable, for the original study on which the present article is based

*Give information separately for exposed and unexposed groups.

Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and

published examples of transparent reporting. The STROBE checklist is best used in conjunction with this article (freely

available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at

http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is

available at www.strobe-statement.org.

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Associations between chronic diseases and choking deaths among older adults in the United States: a cross-sectional

study using multiple-cause mortality data from 2009 to 2013

Journal: BMJ Open

Manuscript ID bmjopen-2015-009464.R2

Article Type: Research

Date Submitted by the Author: 15-Oct-2015

Complete List of Authors: Wu, Wen-Shiann; Department of Internal Medicine, Chi Mei Medical Center Sung, Kuan-Chin; Department of Neurosurgery, Chi Mei Medical Center Cheng, Tain-Junn; Department of Neurology, Chi Mei Medical Center Lu, Tsung-Hsueh; Institute of Public Health, College of Medicine, National Cheng Kung Universtiy,

<b>Primary Subject Heading</b>:

Epidemiology

Secondary Subject Heading: Respiratory medicine, Medical management, Geriatric medicine, Public health

Keywords: Epidemiology < TROPICAL MEDICINE, ACCIDENT & EMERGENCY

MEDICINE, GERIATRIC MEDICINE, THORACIC MEDICINE, PUBLIC HEALTH

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Associations between chronic diseases and choking deaths among

older adults in the United States: a cross-sectional study using

multiple-cause mortality data from 2009 to 2013

Wen-Shiann Wu,1,2 Kuan-Chin Sung,3 Tain-Junn Cheng,3,5 Tsung-Hsueh Lu,6

Wen-Shiann Wu and Kuan-Chin Sung are joint first authors

1Department of Internal Medicine, Chi Mei Medical Center, Tainan, Taiwan

2Department of Pharmacy, Chia Nan University of Pharmacy and Science, Tainan, Taiwan

3Department of Neurosurgery, Chi Mei Medical Center, Tainan, Taiwan

4Department of Neurology, Occupational Medicine, Management in Medical Records and

Information, Chi Mei Medical Center, Tainan, Taiwan

5Department of Occupational Safety / Institute of Industrial Safety and Disaster Prevention,

College of Sustainable Environment, Chia Nan University of Pharmacy and Science, Tainan,

Taiwan

6NCKU Research Center for Health Data and Department of Public Health, College of

Medicine, National Cheng Kung University, Tainan, Taiwan

*Correspondence to

Dr. Tain-Junn Cheng, Department of Neurology, Chi Mei Medical Center, ,No.901, Zhonghua

Rd., Yongkang Dist., Tainan City 701, Taiwan

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ABSTRACT

Objectives: To examine whether the strengths of the associations between chronic diseases

and overall choking differ from those of the associations between chronic diseases and only

food-related choking.

Design: This cross-sectional study used nationwide multiple-cause mortality files.

Setting: The United States.

Participants: Older adults aged 65 years or older died between 2009 and 2013.

Main outcome measures: Mortality ratio (observed/expected) of number of deaths with

both causes (chronic diseases and choking) and 95% confidence intervals.

Results: We identified 76 543 deaths for which the death certificates report choking (ICD-10

codes W78, W79, and W80 combined) as a cause of death and only 4974 (6.5%) deaths were

classified as food-related choking (ICD-10 code W79). Schizophrenia, Parkinson’s disease,

Alzheimer’s disease, and oral cancer are four chronic diseases that had significant

associations with both overall and food-related choking. Stroke, larynx cancer, and mood

(affective) disorders had significant associations with overall choking, but not with food-related

choking.

Conclusions: We suggest using overall choking instead of only food-related choking to

better describe the associations between chronic diseases and choking.

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Strengths and limitations of this study

� This study used nationwide population-based dataset.

� This study examined more chronic diseases than previous studies.

� Both chronic diseases and choking might be underreported on the death certificates by

the coroners or medical examiners.

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INTRODUCTION

Many older adults with chronic diseases experience dysphagia (difficulty in swallowing) and

have a higher risk of choking deaths.1-3

By using multiple-cause mortality files, one US study

determined that older adults whose death certificates report chronic diseases (such as Parkinson’s

disease and Alzheimer’s disease) exhibited a higher risk of having food-related choking as a

cause of death.4 However, inconsistent with the current knowledge that suggests that dysphagia

is a common problem among people with stroke,5-7

no significant association between stroke and

food-related choking was noted in that study. One possible explanation, as indicated by the

authors, is that the deaths of many older adults involving food-related choking were misclassified

as obstruction of the respiratory tract by an unspecified object.

Regarding the proper classification of national cause of death statistics, the three categories

related to choking listed in the International Statistical Classification of Diseases and Related

Health Problems, Tenth Revision (ICD-10) are as follows: ICD-10 code W78 “Inhalation of

gastric contents”, ICD-10 code W79 “Inhalation and ingestion of food causing obstruction of

respiratory tract” and ICD-10 code W80 “Inhalation and ingestion of other objects causing

obstruction of respiratory tract”.8 It is highly likely that many food-related choking deaths were

misclassified as ICD-10 code W80 instead of ICD-10 code W79. The problem of

misclassification would bias the estimation of the associations between chronic diseases and

choking deaths. Thus, we examined whether the strengths of the associations between chronic

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diseases and overall choking (ICD-10 codes W78, W79, and W80 combined) might differ from

those of the association between chronic diseases and only food-related choking (ICD-10 code

W79). Furthermore, we added more chronic diseases than those listed in the study of Kramarow

et al.,4 because one systematic review indicated that patients with some psychiatric disorders

have a higher risk of choking deaths.9

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DATA AND METHODS

The number of deaths among older adults in the United States aged 65 years or older for

which various types of chronic diseases and choking are listed on the death certificates for

2009 to 2013 were obtained from the Wide-ranging Online Data for Epidemiologic Research

of the Centers for Disease Control and Prevention (CDC WONDER).10

To examine the magnitude of the association between particular chronic disease and

choking we used the ratio method proposed by Israel et al.11

This method consists of

calculating the ratio of the number of observed pairs (O) of causes to the expected number (E)

of pairs of causes based on the assumption of independence. An O/E ratio greater than 1

indicates that more deaths with paired causes were reported than could be expected by

chance if the paired causes were independent. This method has been used by many

scholars.4,12-15

The expected number of deaths is calculated as:

(Number of deaths with mention of choking) � (Number of deaths with mention of

particular chronic disease) / (Total number of deaths from all causes)

The ratio is calculated as:

(Observed numbers of deaths with mention of both particular chronic disease and choking) /

(Expected numbers of deaths with both causes)

We also estimated 95% confidence intervals (95% CIs) of O/E ratio according to the Poisson

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distribution.

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RESULTS

For 76 543 older adults in the United States aged 65 years or older who died between 2009

and 2013, choking was reported as a cause of death (i.e., died with) on the death certificates,

and choking was assigned as the underlying cause of death (i.e., died from) in only one fifth

(21.6%) of the death certificates (Table 1). Furthermore, only 6.5% (4974) of overall choking

occurrences (ICD-10 codes W78, W79, and W80 combined) were classified as food-related

choking (ICD-10 codes W79).

As shown in Table 2, the percentage of death certificates reporting both chronic diseases

and overall choking as causes of death was the highest for patients with schizophrenia

(2.66%), followed by Parkinson’s disease (2.25%), larynx cancer (1.75%), and Alzheimer’s

disease (1.44%). However, the percentage of death certificates reporting both chronic

diseases and food-related choking as causes of death was the highest for patients with

schizophrenia (0.52%), followed by Parkinson’s disease (0.15%), oral cancer (0.09%), larynx

cancer (0.08%), mood (affective) disorders (0.07%), and Alzheimer’s disease (0.07%).

Seven chronic diseases were significantly associated with overall choking, with

significance ratios being higher than one; however, only four chronic diseases had significant

associations with food-related choking (Table 3). Chronic diseases associated with overall

choking at a ratio greater than one were ranked in the following order: schizophrenia,

Parkinson’s disease, larynx cancer, Alzheimer’s disease, oral cancer, stroke, and mood

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(affective) disorders. By contrast, chronic diseases associated with food-related choking were

ranked in the following order: schizophrenia, Parkinson’s disease, oral cancer, larynx cancer,

Alzheimer’s disease, and mood (affective) disorders.

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DISCUSSION

The findings of this study indicate that only 6.5% of all deaths with mention of any type of

choking were classified as food-related choking and nine of ten overall choking occurrences

were classified as obstruction of the respiratory tract by an unspecified object. We also found

that the strengths of the associations between chronic diseases and overall choking differed

from those of the associations between chronic diseases and only food-related choking.

Schizophrenia, Parkinson’s disease, Alzheimer’s disease, and oral cancer are four chronic

diseases that had significant associations with both overall and food-related choking. However,

stroke, larynx cancer, and mood (affective) disorders had significant associations with overall

choking and not with food-related choking.

Some forensic studies, suggested that majority of unintentional choking deaths among

older adults were food related and only a few choking deaths were due to foreign bodies other

than food, such as broken teeth or dentures.16-20

We did not have autopsy data to determine the

proportion of choking deaths been classified as ICD-10 code W80. However, according to

previous forensic studies,16-20

many of deaths been classified as ICD-10 code W80 were in

actually involving food. Furthermore, the misclassification would vary by characteristics of

the deceased and certifiers. These misclassifications would certainly bias the estimation of the

strengths of the associations between chronic diseases and choking, as indicated in this study.

Reports of choking as a cause of death among older adults with stroke, larynx cancer, and

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mood (affective) disorders could be overlooked if only food-related choking is considered in

assessments.

In the study of Kramarow et al.,4 only two chronic diseases (Parkinson’s disease and

Alzheimer’s disease) had significant associations with food-related choking. We did not

include pneumonitis (aspiration pneumonia) and influenza and pneumonia in this study

because these two diagnoses are acute conditions. We identified five more chronic diseases

with significant associations with overall choking. Two of them were psychiatric disorders

(schizophrenia and mood [affective] disorders), two were cancers (oral cancer and larynx

cancer), and one was stroke, which is consistent with current knowledge. The caretakers of

older adults with chronic diseases and a higher risk of death from choking should pay close

attention to food preparation and carefully monitor patients during mealtimes.16

However, we

should not concern only the relative associations but also the absolute number of deaths, as

number of deaths with mention Alzheimer’s disease were 100 times more than the number of

deaths with mention schizophrenia, in which the public health implications are quite different.

Despite using broader definitions for choking to include more cases in examining the

associations between chronic diseases and choking, this study had some limitations. First, our

analysis depended only on the information reported on the death certificates, and both chronic

diseases and choking might have been underreported by medical certifiers. Many sudden and

unexpected deaths occurring during meals because of accidental occlusion of the airway by

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swallowed food might have been incorrectly attributed to acute myocardial infarction (i.e.,

café coronary), resulting in the underreporting of choking deaths.17

A choking death is an

unnatural death and should be certified by medical examiners or coroners. Different medical

examiners or coroners might have different opinions and habits in reporting chronic diseases

as the contributory causes of death. We assume that the underreporting of both choking and

chronic diseases is non-differential misclassification.

Second, detailed information relevant to injury prevention programme design, such as the

types of foods, mealtimes, and places of injury, was not specifically recorded in the death

certificates in most cases. Furthermore, we did not have information of the level of

dependence on particular chronic disease. The dead with very dependent especially in

degenerative diseases with a high prevalence of dysphagia is difficult to attribute death by

choking food. It is not surprising that the choking are more common in patients with

psychiatric illness (schizophrenia) or Parkinson's disease with low functional dependence.

In conclusion, only a few food-related choking occurrences were correctly classified as

ICD-10 code W79, whereas most of the cases were classified as ICD-10 code W80.

Consequently, to effectively assess the strengths of the associations between chronic diseases

and choking, it is appropriate to use overall choking (i.e., combining ICD-10 codes W78,

W79, and W80) instead of only food-related choking. Moreover, the caretakers of older adults

with chronic diseases (schizophrenia, Parkinson’s disease, larynx cancer, Alzheimer’s disease,

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oral cancer, stroke, and mood [affective] disorders) should be alert in preventing choking.

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Acknowledgment The authors thank Ms. Bai-Huan Lin for her efforts in data analyses.

Contributors THL conceived the study, guided the analyses, wrote the article draft, and is the

guarantor or the study. WSW, TJC, and KCS helped conduct the literature review, analysed

the data, interpreted the results, and critically revised the manuscript.

Funding This study was partially funded by the Ministry of Science and Technology of Taiwan

(NSC102-2314-B-006- 054) and partially funded by the Chi Mei & National Cheng Kung

University Joint Program (CMNCKU10410).

Competing interests No, there are no competing interests.

Ethics approval This study was approved by the Institutional Review Board at National

Cheng Kung University.

Provenance and peer review Not commissioned; externally peer reviewed.

Data sharing statement No additional data available.

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REFERENCES

1. Forster A, Samaras N, Gold G, Samaras D. Oropharyngeal dysphagia in older adults:

a review. Eur Geriatr Med 2011;2:356-62.

2. Miller N, Patterson J. Dysphagia: implications for older people. Rev Clin Gerontol

2014;24:41-57.

3. Clave P, Shaker R. Dysphagia: current reality and scope of the problem. Nat Rev

Gastroenterol Hepatol 2015;12:259–70.

4. Kramarow E, Warner M, Chen LH. Food-related choking deaths among the elderly.

Inj Prev 2014;20:200-3.

5. Altman KW, Richards A, Goldberg L, Frucht S, McCabe DJ. Dysphagia in stroke,

neurodegenerative disease, and advanced dementia. Otolaryngol Clin N Am

2013;46:1137-49.

6. Chang CY, Cheng TJ, Lin CY, Chen JY, Lu TH, Kawachi I. Reporting of aspiration

pneumonia or choking as a cause of death in patients who died with stroke. Stroke

2013;44:1182-5.

7. Walshe M. Oropharyngeal dysphagia in neurodegenerative disease. J Gastroenterol

Hepatol Res 2014;3:1265-71.

8. World Health Organization. International Statistical Classification of Diseases and

Related Health Problems, Tenth Revision. Accessed at June 20, 2015,

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http://apps.who.int/classifications/icd10/browse/2015/en

9. Aldridge KJ, Taylor NF. Dysphagia is a common and serious problem for adults with

mental illness: a systematic review. Dysphagia 2012;27:124-37.

10. Centers for Disease Control and Prevention. CDC WONDER. Accessed at June 20,

2015, http://wonder.cdc.gov.

11. Israel RA, Rosenberg HM, Curtin LM. Analytical potential for multiple cause-of-death

data. Am J Epidemiol 1986;124:161–79.

12. Coste J, Jougla E. Mortality from rheumatoid arthritis in France, 1970-1990. Int J

Epidemiol 1994;23:545-552.

13. Ziade N, Jourgla E, Coste J. Population-level influence of rheumatoid arthritis on

mortality and recent trends: a multiple cause-of-death analysis in France, 1970-2002.

J Rheumatol 2008;35:1950-1957.

14. Ascoli V, Minelli G, Kanieff M, Crialesi R, Frova L, Conti S. Cause-specific mortality in

classic Kaposi’s sarcoma: a population-based study in Italy (1995-2002). Br J Cancer

2009;101:1085-1090.

15. Souza DCC, Santo AH, Sato EI. Mortality profile related to systematic lupus

erythematosus: a multiple cause-of-death analysis. J Rheumatol 2012;39:496-503.

16. Berzlanovich AM, Fazeny-Dorner B, Waldhoer T, Fasching P, Keil W. Foreign body

asphyxia: a preventable cause of death in the elderly. Am J Prev Med 2005;28:65-9.

17. Wick R, Gilbert JD, Byard RW. Café coronary syndrome-fatal choking on food: an

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autopsy approach. J Clin Forensic Med 2006;13:135-8.

18. Dolkas L, Stanley C, Smith AM, Vilke GM. Deaths associated with choking in San

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19. Boghossian E, Tambuscio S, Sauvageau A. Nonchemical suffocation deaths in

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20. Kikutani T, Tamura F, Tohara T, Takahashi N, Yaegaki K. Tooth loss as risk factor for

foreign-body asphyxiation in nursing-home patients. Arch Gerontol Geriatr

2012;54:e431-5.

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Table 1 Number of deaths for which choking was assigned as either the underlying COD or mentioned among older adults aged 65 years or older

in the United States according to CDC WONDER for years 2009 to 2013

UUUUnderlyingnderlyingnderlyingnderlying CODCODCODCOD MMMMentionentionentionentionedededed CategoryCategoryCategoryCategory of choking (ICDof choking (ICDof choking (ICDof choking (ICD----10 codes)10 codes)10 codes)10 codes) NoNoNoNo %%%% NoNoNoNo %%%% Overall choking (W78–W80) 16 531 100.0 76 543 100.0 Inhalation of gastric contents (W78) 804 4.9 2617 3.4 Inhalation and ingestion of food causing obstruction of respiratory tract (W79) 3113 18.8 4974 6.5 Inhalation and ingestion of other objects causing obstruction of respiratory tract (W80) 12 614 76.3 68 980 90.1 COD, cause of death; CDC WONDER,

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Table 2 Number and percentage (%) of deaths where choking was mentioned* among the deaths aged 65 years or older where the particular

chronic disease was mentioned in the United States according to CDC WONDER for 2009 to 2013

Chronic disease (ICDChronic disease (ICDChronic disease (ICDChronic disease (ICD----10 codes)10 codes)10 codes)10 codes)

Particular Particular Particular Particular chronic disease chronic disease chronic disease chronic disease was mentionedwas mentionedwas mentionedwas mentioned

Particular chronic Particular chronic Particular chronic Particular chronic disease disease disease disease andandandand overall overall overall overall chokingchokingchokingchoking were both were both were both were both

mentionedmentionedmentionedmentioned %%%%

Particular chronic Particular chronic Particular chronic Particular chronic disease disease disease disease and and and and foodfoodfoodfood----

relatedrelatedrelatedrelated chokingchokingchokingchoking were were were were both mentionedboth mentionedboth mentionedboth mentioned %%%%

Oral cancer (C00–C14) 30 469 412 1.35 27 0.09 Esophageal cancer (C15) 49 860 391 0.78 6 0.01 Larynx cancer (C32) 15 391 270 1.75 12 0.08 Diabetes mellitus (E10–E14) 901 854 6329 0.70 430 0.05 Schizophrenia (F20–F29) 13 697 365 2.66 71 0.52 Mood (affective) disorders (F30–F39) 55 508 644 1.16 37 0.07 Parkinson's disease (G20–G21) 178 482 4024 2.25 273 0.15 Alzheimer's disease (G30, F03) 1 502  141 21 692 1.44 1026 0.07 Heart disease (I00–I09, I11 ,I13 ,I20–I51) 4 441  643 27 398 0.62 1710 0.04 Stroke (I60–I69) 925 559 12 210 1.32 487 0.05 Chronic lower respiratory disease (J40–J47) 1 157  788 8360 0.72 271 0.02 Nephrotic disease (N00–N07, N17–N19, N25–N27) 940 209 6009 0.64 122 0.01 * “Mention” can be as either an underlying or a contributory cause of death

CDC WONDER, Wide-ranging Online Data for Epidemiologic Research of the Centers for Disease Control and Prevention

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Table 3 Number of obs deaths, exp deaths, and the Obs/Exp ratio of deaths where particular chronic disease and choking were both

mentioned* among the deaths aged 65 years or older where the particular chronic disease was mentioned in the United States according to

CDC WONDER for 2009 to 2013

Overall chokingOverall chokingOverall chokingOverall choking FoodFoodFoodFood----related chokingrelated chokingrelated chokingrelated choking ChroniChroniChroniChronic diseasec diseasec diseasec disease ObsObsObsObs ExpExpExpExp Obs/ExpObs/ExpObs/ExpObs/Exp (95% CI)(95% CI)(95% CI)(95% CI) ObsObsObsObs ExpExpExpExp Obs/ExpObs/ExpObs/ExpObs/Exp ((((95% CI95% CI95% CI95% CI)))) Schizophrenia 365 115 3.19 (2.87–3.53) 71 7 9.54 (7.92–12.8) Parkinson's disease 4024 1492 2.70 (2.61–2.78) 273 97 2.82 (2.49–3.17) Larynx cancer 270 129 2.10 (1.86–2.36) 12 8 1.44 (0.74–2.51) Alzheimer's disease* 21 692 12 559 1.73 (1.70–1.75) 1026 816 1.26 (1.18–1.34) Oral cancer 412 255 1.62 (1.46–1.78) 27 17 1.63 (1.07–2.38) Stroke 12 210 7739 1.58 (1.55–1.61) 487 503 0.97 (0.88–1.06) Mood (affective) disorders 644 464 1.39 (1.28–1.50) 37 30 1.23 (0.87–1.70) Esophageal cancer 391 417 0.94 (0.85–1.04) 6 27 0.22 (0.08–0.49) Diabetes mellitus 6329 7540 0.84 (0.82–0.86) 430 490 0.88 (0.80–0.96) Chronic lower respiratory disease 8360 9680 0.86 (0.85–0.88) 271 629 0.43 (0.38–0.49) Nephrotic disease 6009 7861 0.76 (0.75–0.78) 122 511 0.24 (0.20–0.29) Heart disease 27 398 37 137 0.74 (0.73–0.75) 1710 2413 0.71 (0.68–0.74) * “Mention” can be as either an underlying or a contributory cause of death

Obs, observed; Exp, expected; CDC WONDER, Wide-ranging Online Data for Epidemiologic Research of the Centers for Disease Control and Prevention

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STROBE Statement—Checklist of items that should be included in reports of cross-sectional studies

Item

No Recommendation

Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the abstract

(b) Provide in the abstract an informative and balanced summary of what was done

and what was found

Introduction

Background/rationale 2 Explain the scientific background and rationale for the investigation being reported

Objectives 3 State specific objectives, including any prespecified hypotheses

Methods

Study design 4 Present key elements of study design early in the paper

Setting 5 Describe the setting, locations, and relevant dates, including periods of recruitment,

exposure, follow-up, and data collection

Participants 6 (a) Give the eligibility criteria, and the sources and methods of selection of

participants

Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders, and effect

modifiers. Give diagnostic criteria, if applicable

Data sources/

measurement

8* For each variable of interest, give sources of data and details of methods of

assessment (measurement). Describe comparability of assessment methods if there is

more than one group

Bias 9 Describe any efforts to address potential sources of bias

Study size 10 Explain how the study size was arrived at

Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If applicable,

describe which groupings were chosen and why

Statistical methods 12 (a) Describe all statistical methods, including those used to control for confounding

(b) Describe any methods used to examine subgroups and interactions

(c) Explain how missing data were addressed

(d) If applicable, describe analytical methods taking account of sampling strategy

(e) Describe any sensitivity analyses

Results

Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially

eligible, examined for eligibility, confirmed eligible, included in the study,

completing follow-up, and analysed

(b) Give reasons for non-participation at each stage

(c) Consider use of a flow diagram

Descriptive data 14* (a) Give characteristics of study participants (eg demographic, clinical, social) and

information on exposures and potential confounders

(b) Indicate number of participants with missing data for each variable of interest

Outcome data 15* Report numbers of outcome events or summary measures

Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and

their precision (eg, 95% confidence interval). Make clear which confounders were

adjusted for and why they were included

(b) Report category boundaries when continuous variables were categorized

(c) If relevant, consider translating estimates of relative risk into absolute risk for a

meaningful time period

Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and

sensitivity analyses

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2

Discussion

Key results 18 Summarise key results with reference to study objectives

Limitations 19 Discuss limitations of the study, taking into account sources of potential bias or

imprecision. Discuss both direction and magnitude of any potential bias

Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations,

multiplicity of analyses, results from similar studies, and other relevant evidence

Generalisability 21 Discuss the generalisability (external validity) of the study results

Other information

Funding 22 Give the source of funding and the role of the funders for the present study and, if

applicable, for the original study on which the present article is based

*Give information separately for exposed and unexposed groups.

Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and

published examples of transparent reporting. The STROBE checklist is best used in conjunction with this article (freely

available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at

http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is

available at www.strobe-statement.org.

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