Understanding pathogen transmission on inanimate surfaces: Insights from respiratory fluid droplet composition and drying dynamics

Abstract

This study investigates how pathogen-laden respiratory droplets transfer diseases via inanimate surfaces. Respiratory fluid ejections containing pathogens pose a significant health threat, especially in high-traffic areas such as hospitals, public transport, restaurants, and schools. When these droplets dry on surfaces, they form deposits that can transfer pathogens to healthy individuals through contact and can be ingested via the oral or nasal route. The study examined the effects of varying salt and mucin concentrations in respiratory fluid droplets containing Pseudomonas aeruginosa. Results showed that P. aeruginosa viability increased 10-fold at elevated mucin concentrations, while changes in salt concentration had minimal impact. Adhesive properties of the deposits were analyzed using atomic force spectroscopy and scotch tape test. Pathogen transfer from the deposit to a fingerprint patterned model thumb at different relative humidity (RH) levels was assessed using confocal microscopy, showing significant pathogen transfer at elevated RH. Out of 10⁶ CFU/mL pathogens in deposits, 17%‒38% are potentially transferable, with most of the transfer occurring from the droplet's edge deposits. The study demonstrated that the combined variation in salt and mucin concentrations significantly influences the evaporation, flow, and precipitation dynamics of droplets. These changes, in turn, affect the solutal deposition and distribution of pathogens within the droplet, ultimately altering the survivability and transmissibility of the pathogen.

References

[1] Chaudhuri S, Basu S, Kabi P, Unni VR, Saha A. Modeling the role of respiratory droplets in Covid-19 type pandemics. Phys Fluids. 2020; 32:063309.

[2] Tellier R, Li Y, Cowling BJ, Tang JW. Recognition of aerosol transmission of infectious agents: a commentary. BMC Infect Dis. 2019; 19:101.

[3] Wang CC, Prather KA, Sznitman J, et al. Airborne transmission of respiratory viruses. Science. 2021; 373:eabd9149.

[4] Leung NHL. Transmissibility and transmission of respiratory viruses. Nat Rev Micro. 2021; 19: 528-545.

[5] Basak M, Mitra S, Bandyopadhyay D. Pathways to community transmission of COVID-19 due to rapid evaporation of respiratory virulets. J Colloid Interface Sci. 2022; 619: 229-245.

[6] Marks PJ, Vipond IB, Carlisle D, Deakin D, Fey RE, Caul EO. Evidence for airborne transmission of Norwalk-like virus (NLV) in a hotel restaurant. Epidemiol Infect. 2000; 124: 481-487.

[7] Stephens B, Azimi P, Thoemmes MS, Heidarinejad M, Allen JG, Gilbert JA. Microbial exchange via fomites and implications for human health. Curr Pollut Rep. 2019; 5: 198-213.

[8] Rogers M, Weinstock DM, Eagan J, Kiehn T, Armstrong D, Sepkowitz KA. Rotavirus outbreak on a pediatric ontology floor: possible association with toys. Am J Infect Control. 2000; 28: 378-380.

[9] Guo L, Wang M, Zhang L, et al. Transmission risk of viruses in large mucosalivary droplets on the surface of objects: a time-based analysis. Infect Dis Now. 2021; 51: 219-227.

[10] Xie X, Li Y, Zhang T, Fang HHP. Bacterial survival in evaporating deposited droplets on a teflon-coated surface. Appl Microbiol Biotechnol. 2006; 73: 703-712.

[11] Vejerano EP, Marr LC. Physico-chemical characteristics of evaporating respiratory fluid droplets. J R Soc Interface. 2018; 15:20170939.

[12] Rasheed A, Sharma S, Kabi P, Saha A, Chaudhuri S, Basu S. Precipitation dynamics of surrogate respiratory sessile droplets leading to possible fomites. J Colloid Interface Sci. 2021; 600: 1-13.

[13] Rasheed A, Parmar K, Jain S, Chakravortty D, Basu S. Weather-related changes in the dehydration of respiratory droplets on surfaces bolster bacterial endurance. J Colloid Interface Sci. 2024; 674: 653-662.

[14] Gurrala P, Katre P, Balusamy S, Banerjee S, Sahu KC. Evaporation of ethanol‒water sessile droplet of different compositions at an elevated substrate temperature. Int J Heat Mass Transf. 2019; 145:118770.

[15] Fukatani Y, Orejon D, Kita Y, Takata Y, Kim J, Sefiane K. Effect of ambient temperature and relative humidity on interfacial temperature during early stages of drop evaporation. Phys Rev E. 2016; 93:043103.

[16] Girard F, Antoni M, Faure S, Steinchen A. Influence of heating temperature and relative humidity in the evaporation of pinned droplets. Colloids Surf A Physicochem Eng Asp. 2008; 323: 36-49.

[17] Sharma S, Jain S, Saha A, Basu S. Evaporation dynamics of a surrogate respiratory droplet in a vortical environment. J Colloid Interface Sci. 2022; 623: 541-551.

[18] Patil ND, Bange PG, Bhardwaj R, Sharma A. Effects of substrate heating and wettability on evaporation dynamics and deposition patterns for a sessile water droplet containing colloidal particles. Langmuir. 2016; 32: 11958-11972.

[19] Cameron JM, Butler HJ, Palmer DS, Baker MJ. Biofluid spectroscopic disease diagnostics: a review on the processes and spectral impact of drying. J Biophoton. 2018; 11:e201700299.

[20] Sefiane K. On the formation of regular patterns from drying droplets and their potential use for bio-medical applications. J Bionic Eng. 2010; 7: S82–S93.

[21] Easo GJ, Paul D. Dried blood patterns for diagnosis of non-communicable and infectious diseases. In: Borse V, Chandra P, Srivastava R, eds. BioSensing, Theranostics, and Medical Devices: From Laboratory to Point-of-Care Testing. Springer; 2022: 299-316.

[22] Lim MD. Dried blood spots for global health diagnostics and surveillance: opportunities and challenges. Am J Trop Med Hyg. 2018; 99: 256-265.

[23] Mukhopadhyay M, Ray R, Ayushman M, et al. Interfacial energy driven distinctive pattern formation during the drying of blood droplets. J Colloid Interface Sci. 2020; 573: 307-316.

[24] Majee S, Chowdhury AR, Pinto R, et al. Spatiotemporal evaporating droplet dynamics on fomites enhances long term bacterial pathogenesis. Commun Biol. 2021; 4:1173.

[25] Zhou M, Zou J. A dynamical overview of droplets in the transmission of respiratory infectious diseases. Phys Fluids. 2021; 33:031301.

[26] Hegde O, Chatterjee R, Rasheed A, Chakravortty D, Basu S. Multiscale vapor-mediated dendritic pattern formation and bacterial aggregation in complex respiratory biofluid droplets. J Colloid Interface Sci. 2022; 606: 2011-2023.

[27] Basu S, Kabi P, Chaudhuri S, Saha A. Insights on drying and precipitation dynamics of respiratory droplets from the perspective of COVID-19. Phys Fluids. 2020; 32:123317.

[28] Henderson AG, Ehre C, Button B, et al. Cystic fibrosis airway secretions exhibit mucin hyperconcentration and increased osmotic pressure. J Clin Invest. 2014; 124: 3047-3060.

[29] Lapierre SG, Phelippeau M, Hakimi C, et al. Cystic fibrosis respiratory tract salt concentration: an exploratory cohort study. Medicine. 2017; 96:e8423.

[30] Widdicombe JH. Altered NaCl concentration of airway surface liquid in cystic fibrosis. Pflugers Arch. 2001; 443: S8–S10.

[31] Soulié V, Karpitschka S, Lequien F, et al. The evaporation behavior of sessile droplets from aqueous saline solutions. Phys Chem Chem Phys. 2015; 17: 22296-22303.

[32] Misyura SY. Evaporation of a sessile water drop and a drop of aqueous salt solution. Sci Rep. 2017; 7:14759.

[33] Ozdemir O, Karakashev SI, Nguyen AV, Miller JD. Adsorption and surface tension analysis of concentrated alkali halide brine solutions. Miner Eng. 2009; 22: 263-271.

[34] Mikos AG, Peppas NA. Measurement of the surface tension of mucin solutions. Int J Pharma. 1989;53:1-5.

[35] Maheshwari R, Dhathathreyan A. Mucin at solution/air and solid/solution interfaces. J Colloid Interface Sci. 2006; 293: 263-269.

[36] Pham T, Kumar S. Drying of droplets of colloidal suspensions on rough substrates. Langmuir. 2017; 33: 10061-10076.

[37] Hu H, Larson RG. Evaporation of a sessile droplet on a substrate. J Phys Chem B. 2002; 106: 1334-1344.

[38] Marin A, Karpitschka S, Noguera-Marín D, et al. Solutal Marangoni flow as the cause of ring stains from drying salty colloidal drops. Phys Rev Fluids. 2019; 4:41601.

[39] Shao X, Hou Y, Zhong X. Intense jet flow with symmetric vortices induced by saline concentration gradient at free surface of a drying saline droplet. Int Commun Heat Mass Transfer. 2021; 128:105573.

[40] Pathak B, Christy J, Sefiane K, Gozuacik D. Complex pattern formation in solutions of protein and mixed salts using dehydrating sessile droplets. Langmuir. 2020; 36: 9728-9737.

[41] Huang Q, Wang W, Vikesland PJ. Implications of the coffee-ring effect on virus infectivity. Langmuir. 2021; 37: 11260-11268.

[42] Rasheed A, Hegde O, Chatterjee R, Sampathirao SR, Chakravortty D, Basu S. Physics of self-assembly and morpho-topological changes of Klebsiella pneumoniae in desiccating sessile droplets. J Colloid Interface Sci. 2023; 629: 620-631.

[43] Deleplace M, Dallagi H, Dubois T, et al. Structure of deposits formed by drying of droplets contaminated with Bacillus spores determines their resistance to rinsing and cleaning. J Food Eng. 2022; 318:110873.

[44] Çetiner U, Rowe I, Schams A, et al. Tension-activated channels in the mechanism of osmotic fitness in Pseudomonas aeruginosa. J Gen Physiol. 2017; 149: 595-609.

[45] Aspedon A, Palmer K, Whiteley M. Microarray analysis of the osmotic stress response in Pseudomonas aeruginosa. J Bacteriol. 2006; 188: 2721-2725.

[46] Agrawal A, Gopu M, Mukherjee R, Mampallil D. Microfluidic droplet cluster with distributed evaporation rates as a model for bioaerosols. Langmuir. 2022; 38: 4567-4577.

[47] Seyfert C, Rodríguez-Rodríguez J, Lohse D, Marin A. Stability of respiratory-like droplets under evaporation. Phys Rev Fluids. 2022; 7:023603.

[48] Dabrowska AK, Rotaru GM, Derler S, et al. Materials used to simulate physical properties of human skin. Skin Res Technol. 2016; 22: 3-14.

[49] Eudier F, Savary G, Grisel M, Picard C. Skin surface physico-chemistry: characteristics, methods of measurement, influencing factors and future developments. Adv Colloid Interface Sci. 2019; 264: 11-27.

[50] Ranamukhaarachchi SA, Schneider T, Lehnert S, et al. Development and validation of an artificial mechanical skin model for the study of interactions between skin and microneedles. Macromol Mater Eng. 2016; 301: 306-314.

[51] Ashbaugh DR. Quantitative-Qualitative Friction Ridge Analysis : An Introduction to Basic and Advanced Ridgeology. CRC Press; 1999.

[52] Aldien Y, Welcome D, Rakheja S, Dong R, Boileau PE. Contact pressure distribution at hand-handle interface: role of hand forces and handle size. Int J Ind Ergon. 2005; 35: 267-286.

[53] Dhyani A, Repetto T, Bartikofsky D, et al. Surfaces with instant and persistent antimicrobial efficacy against bacteria and SARS-CoV-2. Matter. 2022; 5: 4076-4091.

[54] Susarrey-Arce A, Marin A, Massey A, et al. Pattern formation by Staphylococcus epidermidis via droplet evaporation on micropillars arrays at a surface. Langmuir. 2016; 32: 7159-7169.

[55] Mhatre NV, Kumar S. Pinning-depinning transition of droplets on inclined substrates with a three-dimensional topographical defect. Soft Matter. 2024; 20: 3529-3540.

[56] Mhatre NV, Kumar S. Shear-induced depinning of thin droplets on rough substrates. J Fluid Mech. 2024; 990:A14.

RIGHTS & PERMISSIONS

2025 The Author(s). Droplet published by Jilin University and John Wiley & Sons Australia, Ltd.