Pulmonary Dysfunction Augmenting Bacterial Aerosols in Leather Tanneries of Punjab, Pakistan

Figures & data

Table 1 Tannery-site characteristics

	Processes	Type
Rawhide treatment	Soaking, liming, dehairing, defleshing, deliming, bating, and pickling	Sheltered
Wet machine operations	Chrome tanning, wet-blue storage, wet finishing (wet back, neutralization, retanning, washing, fat liquoring, dyeing, and washing)	Indoor
Buffing and snuffing	Buffing and snuffing	Indoor
Splitting and shaving	Splitting and shaving	Sheltered
Production unit	—	Indoor
Finishing unit	Hydraulic press, roller cutting, spray plant	Indoor
Packing and sales	Weighing, finished leather trim, sorting, and packing	Indoor

Table 2 Human pulmonary bacterial pathogens isolated from tannery air

	Family	Characteristics	Pulmonary symptoms from literature	References
Noviherbaspirillum autotrophicum	Oxalobacteraceae	Facultatively autotrophic bacterium isolated from rice paddy soil	NA	Ishii et al^Citation33
Alcaligenes spp.	Alcaligenaceae	Opportunistic respiratory pathogens	Adult respiratory distress syndrome	Aisenberg et al^Citation34
			Sepsis syndrome
			Cystic fibrosis
Ochrobactrum pseudogrignonense		Opportunistic respiratory pathogens	Cystic fibrosis	Lundy et al, Chmelař, Holý et al^Citation36,Citation64
			Respiratory failure
		No cross-contamination
			Upper and lower respiratory tract infections
Neisseria bacilliformis	Neisseriaceae	Opportunistic pathogens	Upper respiratory tract infections	Han et al^Citation38
Enterobacter cloacae	Enterobacteriaceae		COPD	Didilescu et al, Miyoshi-Akiyama et al^Citation49,Citation50
			Nosocomial pneumonia
			Lower respiratory tract pneumonia
Alcaligenes faecalis (two strains)	Alcaligenaceae	Pan-drug–resistant organism even to carbapenems, polymyxins, and tigecycline	Respiratory depression (reduced SPO2)	Kavuncuoglu et al, Hasan et al^Citation35,Citation63
			Bloodstream infections
		Respiratory dysfunction synergist
			Acute respiratory distress syndrome
Klebsiella pneumoniae	Enterobacteriaceae	Opportunistic pathogen	Lung and urinary tract infection	Kaur et al^Citation62
			Gastrointestinal diseases
Corynebacterium spp.		Animal-skin flora	Respiratory infections	Díez-Aguilar et al^Citation41
		Human pathogen
Providencia rettgeri	Enterobacteriaceae	—	Urinary tract infections, bacteremia, skin infections, diarrhea, and gastroenteritis	Yoh et al, Tada et al^Citation42,Citation61

Table 3 Site-wise bacteria identified

	RHT	WMO	PU	FU-S	FU-HP	B&S	S&S	P&S
Noviherbaspirillum autotrophicum	x	x	-	-	-	-	x	-
Alcaligenes spp.	x	-	-	-	-	x	x	-
Ochrobactrum pseudogrignonense	x	-	x	x	-	x	-	x
Neisseria bacilliformis		-	-	x	x	x	x	x
Enterobacter cloacae	x	x	-	x	x	x	x	x
Alcaligenes faecalis (two strains)	x	-	-	x	x	-	x	x
Klebsiella pneumoniae	x	x	x	x	x	-	x	x
Corynebacterium spp.	x	-	-	x	x	x	x	x
Providencia rettgeri	x	-	-	x	x	-	x	x
Uncultured bacteria	x	-	-	-	-	-		-

Notes: x, presence; –, absence.

Table 4 Bacterial concentrations, MMAD, and TPED

	RHT	WMO	PU	FU-S	FU-HP	B&S	S&S	P&S
Bacterial concentration (CFU/m^3)	3.6×10^3	2.3×10^2	2.6×10^2	3.2×10^3	3.7×10^3	3.2×10^3	2.8×10^3	2.2×10^3
Tolerable concentrations of airborne microbes in occupational environment: Mesophilic bacteria 100,000 and Gram-negative bacteria 20,000 Suggested standards for respirable aerosols are half those, ie, 50,000 CFU/m^3 for mesophilic bacteria and 10,000 CFU/m^3 for Gram-negative bacteria.^Citation65
MMAD (µm)	7.740	0.741	0.659	7.199	7.050	8.351	7.960	7.265
TPED (CFU/kg)	1,464.4	92.78	104.9	1,295	1,516.9	1,299	1,130	923.9

Notes: Sheltered: (top covered corridor without walls); average work hours 8; average employee weight 70 kg.

Abbreviation: MMAD, median mass aerodynamic diameter; TPED, tannery process–exposure dose.

Table 5 Demographic characteristics of participating workforce (n=250)

Parameter	Tannery workersN=250
Age (years)	35±10.55
BMI	23.73±4.77
Body weight (kg)	70±5.6
Smokers	28.4%
Nonsmokers	71.6%

Figure 1 Process-based comparison of average pulmonary function in tannery workers. (A) PrBD and PoBD forced expiratory volume in one second (FEV₁); (B) PrBD and PoBD peak expiratory flow (PEF); (C) PrBD and PoBD forced vital capacity (FVC).

Abbreviations: PrBD, pre bronchodilation; PoBD, post bronchodilation.

Figure 2 Stagewise (GOLD) distribution of COPD patients among tannery-workier cohorts: difference for smokers and nonsmokers. 0, no disease; 1, GOLD stage 1; 2, GOLD stage 2; 3, GOLD stage 3.

Table 6 Statistical evidence of bacterial aerosol–tannery dust synergy enhancing pulmonary dysfunction

Respiratory symptoms among tannery workers (with and without bacterial infections)
	Cough		Phlegm				Wheeze			Dyspnea			Tachypnea
	DE	DE + BI	DE		DE + BI		DE		DE + BI	DE	DE + BI		DE		DE + BI
% Age	33.2	58.8	34		55.6		9.6		16.4	34.4	49.6		9.6		10.8
P	<0.0001*		<0.0001*				0.02*			<0.0001*			0.66
Forward linear regression model: relationship of pulmonary symptoms with selected potential synergy
				Unstandardized coefficients				Standardized coefficients
Cough				β		SE		β				t		P
Constant				0.438		0.65						0		0
Bacteria numbers				0.30		0.011		0.163				2.604		0.01
Smoking				−0.43		—		—				−1.094		0.99
Department				−0.06		—		—				−0.056		0.852
				Model				F=6.781				P=0.010		^a0.023
Phlegm
Constant				0.287		0.064						4.503		0
Bacteria numbers				0.053		0.011		0.290				4.779		0
Smoking				−0.15		—		—				−0.253		0.800
Department				0.003		—		—				0.051		0.959
				Model				F=22.84				P=0		^a0.08
Wheeze
Constant				0.067		0.049						1.364		0.174
Bacteria numbers				0.019		0.009		0.141				2.235		0.026
Smoking				−0.082		—		—				0.192		0.192
Department				−0.039		—		—				0.573		0.852
				Model				F=4.966				P=0.026		^a0.016
Dyspnea
Constant				0.260		0.065						4.009		0
Bacteria numbers				0.047		0.011		0.253				4.121		0
Smoking				−0.030		—		—				−4.84		0.629
Department				−0.126		—		—				−0.120		0.852
				Model				F=16.986				P=0		^a0.06
Tachypnea
Constant				−0.133		0.068						−0.176		0.860
Departments				0.035		0.009		0.253				3.778		0
Bacteria numbers				0.018		0.008		0.156				2.324		0.021
Smoking				0.038		—		—				0.621		0.535
				Model				F=9.586				0.002		^a0.033

Notes: *P=0.05. ^aAdjusted R². Independent variables: bacteria numbers, smoking status, and department type. P-values in bold indicate maximum influence on pulmonary symptom.

Abbreviations: DE, dust exposure (days); BI, bacterial infection (days).

Ishii S, Ashida N, Ohno H, et al. Noviherbaspirillum denitrificans sp. nov., a denitrifying bacterium isolated from rice paddy soil and Noviherbaspirillum autotrophicum sp. nov., a denitrifying, facultatively autotrophic bacterium isolated from rice paddy soil and proposal to reclassify Herbaspirillum massiliense as Noviherbaspirillum massiliense comb. nov. Int J Syst Evol Microbiol. 2017;67(6):1841–1848.

 PubMed Web of Science ®Google Scholar

Aisenberg G, Rolston KV, Safdar A. Bacteremia caused by Achromobacter and Alcaligenes species in 46 patients with cancer (1989–2003). Cancer. 2004;101(9):2134–2140.

 PubMed Web of Science ®Google Scholar

Lundy F, Tunney M, Taggart C, Elborn J. Human Neutrophil Peptide-1 (HNP-1) and a truncated analogue display antimicrobial activity against respiratory pathogens. J Cystic Fibros. 2009;8:S47.

 PubMedGoogle Scholar

Chmelař D, Holý O, Kasáková I, et al. Antibiotic susceptibility and production of endotoxin by Ochrobactrum anthropi isolated from environment and from patients with cystic fibrosis. Folia Microbiol (Praha). 2019;64(6):861–865.

 PubMed Web of Science ®Google Scholar

Han XY, Hong T, Falsen E. Neisseria bacilliformis sp. nov. isolated from human infections. J Clin Microbiol. 2006;44(2):474–479.

 PubMed Web of Science ®Google Scholar

Miyoshi-Akiyama T, Hayakawa K, Ohmagari N, Shimojima M, Kirikae T. Multilocus sequence typing (MLST) for characterization of Enterobacter cloacae. PLoS One. 2013;8(6):e66358.

 PubMed Web of Science ®Google Scholar

Didilescu AC, Skaug N, Marica C, Didilescu C. Respiratory pathogens in dental plaque of hospitalized patients with chronic lung diseases. Clin Oral Investig. 2005;9(3):141–147.

 PubMed Web of Science ®Google Scholar

Kavuncuoglu F, Unal A, Oguzhan N, Tokgoz B, Oymak O, Utas C. First reported case of Alcaligenes faecalis peritonitis. Peritoneal Dial Int. 2010;30(1):118–119.

 PubMed Web of Science ®Google Scholar

Hasan MJ, Nizhu LN, Rabbani R. Bloodstream infection with pandrug-resistant Alcaligenes faecalis treated with double-dose of tigecycline. IDCases. 2019;18:e00600.

 PubMed Web of Science ®Google Scholar

Kaur CP, Vadivelu J, Chandramathi S. Impact of Klebsiella pneumoniae in lower gastrointestinal tract diseases. J Dig Dis. 2018;19(5):262–271.

 PubMed Web of Science ®Google Scholar

Díez-Aguilar M, Ruiz-Garbajosa P, Fernández-Olmos A, et al. Non-diphtheriae Corynebacterium species: an emerging respiratory pathogen. Eur J Clin Microbiol Infect Dis. 2013;32(6):769–772.

 PubMed Web of Science ®Google Scholar

Tada T, Miyoshi-Akiyama T, Dahal RK, et al. NDM-1 Metallo-β-Lactamase and ArmA 16S rRNA methylase producing Providencia rettgeri clinical isolates in Nepal. BMC Infect Dis. 2014;14(1):56.

 PubMedGoogle Scholar

Yoh M, Matsuyama J, Ohnishi M, et al. Importance of Providencia species as a major cause of travellers’ diarrhoea. J Med Microbiol. 2005;54(11):1077–1082.

 PubMed Web of Science ®Google Scholar

Grzyb J, Lenart-Boroń A. Bacterial bioaerosol concentration and size distribution in the selected animal premises in a zoological garden. Aerobiologia. 2019;35(2):253–268.

 Web of Science ®Google Scholar