Nasal mucociliary clearance as a factor in nasal drug delivery

Marttin, Emmeline; Schipper, Nicolaas G.M; Verhoef, J.Coos; Merkus, Frans W.H.M

doi:10.1016/s0169-409x(97)00059-8

Cited by 469Advanced Drug Delivery SystemsInhalation and Respiratory Drug DeliverySinusitis and nasal conditions

Nasal mucociliary clearance as a factor in nasal drug delivery

Marttin, Emmeline, Schipper, Nicolaas G.M, Verhoef, J.Coos, Merkus, Frans W.H.M·1998·Advanced Drug Delivery Reviews

DOI 10.1016/s0169-409x(97)00059-8

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Abstract

The nasal mucociliary clearance system transports the mucus layer that covers the nasal epithelium towards the nasopharynx by ciliary beating. Its function is to protect the respiratory system from damage by inhaled substances. Impairment of nasal mucociliary clearance can result in diseases of the upper airways. Therefore, it is important to study the effects of drugs and drug excipients on nasal mucociliary clearance. A large number of methods are used to assess mucociliary clearance. These methods study the effects of drug and excipients on the mucociliary system in vitro or in vivo in animals and humans. In some cases, the results of different in vitro and in vivo measurements do not correlate well. In vitro methods, especially ciliary beat frequency measurements, have been demonstrated to be valuable tools for toxicity screening. However, in vivo studies are essential to confirm the safety of nasal drug formulations. Nasal mucociliary clearance also has implications for nasal drug absorption. Drugs are cleared rapidly from the nasal cavity after intranasal administration, resulting in fast systemic drug absorption. Several approaches are discussed to increase the residence time of drug formulations in the nasal cavity, resulting in improved nasal drug absorption. However, more experimental evidence is needed to support the conclusion that this improved absorption is caused by a longer residence time of the nasal drug formulation.

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Saliva samples taken from 30 minutes onwards cannot reflect spiking.
“Samples taken from 30 minutes onwards, however, cannot reflect spiking, as substances that are not absorbed across the nasal membrane are transported to the back of the throat, and then swallowed within 15 minutes [14].”
From Salivary oxytocin concentrations in males following intranasal administration of oxytocin: a double-blind, cross-over study (2015) · cites this paper as [14]
Taking saliva samples at 15 minutes after intranasal oxytocin creates the risk of collecting saliva spiked with intranasal oxytocin.
“Hence, taking saliva samples at 15 minutes creates the risk of collecting saliva that is ‘spiked’ with IN-OT (indeed this may be why other saliva studies have chosen 30 minutes as their first measurement, as this allows almost double the length of time of average mucociliary transport [14]).”
From Salivary oxytocin concentrations in males following intranasal administration of oxytocin: a double-blind, cross-over study (2015) · cites this paper as [14]
Mucociliary transport from the nasal cavity to the back of the throat takes 12-15 minutes in healthy individuals.
“This process of clearing substances from the nasal cavity to the back of the throat, called mucociliary transport, takes 12–15 minutes in healthy individuals [14].”
From Salivary oxytocin concentrations in males following intranasal administration of oxytocin: a double-blind, cross-over study (2015) · cites this paper as [14]

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Measurement of nasal mucociliary transport rates on the isolated human inferior turbinate
Mason, J. D. T., Aspden, T., ADLER, J., Jones, N. S., Illum, L., & Davis, S. S. (1995) · Clinical Otolaryngology · doi:10.1111/j.1365-2273.1995.tb01595.x · Cited by 19 · see citing works
Simple and precise method for counting ciliary beats directly from the TV monitor screen
Braga, P. C., Dall'Oglio, G., Bossi, R., & Allegra, L. (1986) · Journal of Pharmacological Methods · doi:10.1016/0160-5402(86)90021-5 · Cited by 19 · see citing works
The Effects of Prostaglandins E1E2and F2αon Mucociliary Activity in the Rabbit Maxillary Sinus
Dolata, J., Lindberg, S. I., & Mercke, U. (1989) · Acta Oto-Laryngologica · doi:10.3109/00016488909125530 · Cited by 19 · see citing works
The effects of drugs on ciliary motility III. Local anaesthetics and anti-allergic drugs
van de Donk, H. J. M., van Egmond, A. L. M., Ag, V. D. H., Zuidema, J., & Merkus, F. W. H. M. (1982) · International Journal of Pharmaceutics · doi:10.1016/0378-5173(82)90135-1 · Cited by 19 · see citing works
Nasal mucociliary clearance & mucus pH in patients with diabetes mellitus.
Sachdeva, A., Sachdeva, O. P., Gulati, S., & Kakkar, V. (1993) · PubMed · Cited by 18 · see citing works
Degeneration of human respiratory cell ciliary beat in monolayer cell cultures
Rautiainen, M., Matsune, S., Yoshitsugu, M., & Ohyama, M. (1993) · European Archives of Oto-Rhino-Laryngology · doi:10.1007/bf00179306 · Cited by 18 · see citing works
Influence of sympathetic and parasympathetic substances in clinical concentrations on human nasal ciliary beat.
Ingels, K. J. A. O., Meeuwsen, F., Graamans, K., & Huizing, E. H. (1992) · PubMed · Cited by 18 · see citing works
Viscoelasticity of cellulose polymers and mucociliary transport on frog palates
Lin, S. Y., Amidon, G. L., Weiner, N. D., & Goldberg, A. H. (1993) · International Journal of Pharmaceutics · doi:10.1016/0378-5173(93)90390-2 · Cited by 17 · see citing works
Effect of azelastine on sulphur dioxide induced impairment of ciliary motility in airway epithelium.
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Some Investigations on Nasal Ciliary Activity
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The effects of calcitonin nasal preparations and their excipients on mucociliary clearance in an ex-vivo frog palate test
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Nasal Epithelial Cell Culture as a Tool in Evaluating Ciliary Dysfunction
Gilain, L., Zahm, J., Pierrot, D., Fuchey, C., Peynegre, R., & Puchelle, É. (1993) · Acta Oto-Laryngologica · doi:10.3109/00016489309135899 · Cited by 16 · see citing works
Morphological and Functional Studies of the Mucociliary System during Infections in the Upper Airways
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Effects of morphine on human nasal cilia beat frequency in vitro
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Chapter 41 Quantification of Ciliary Beat Frequency and Metachrony by High-Speed Digital Video
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9 of the 255 references couldn’t be matched to a known paper.

Sorted by citations

Mucoadhesive polymeric platforms for controlled drug delivery
Andrews, G. P., Laverty, T. P., & Jones, D. S. (2008) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2008.09.028 · Cited by 877 · see citing works
“Such factors make the nasal cavity an attractive route for drug delivery, but they also result in nasal mucosa cells being vulnerable to adverse effects of drugs and excipients delivered intranasally ([102].”
Background
Cyclodextrin-based supramolecular architectures: Syntheses, structures, and applications for drug and gene delivery
Li, J., & Loh, X. J. (2008) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2008.02.011 · Cited by 786 · see citing works
“There have been a lot of developments of drug delivery systems based on CDs, which were used in nasal drug delivery [16–18], in peptide and protein delivery [19], in ophthalmic drug delivery [20], and in many other areas [21–27].”
Background
Evaluation of intranasal delivery route of drug administration for brain targeting
Erdő, F., Bors, L. A., Farkas, D., Bajza, Á., & Gizurarson, S. S. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.10.009 · Cited by 756 · see citing works
Mechanism of intranasal drug delivery directly to the brain
Crowe, T. P., Greenlee, M. H. W., Kanthasamy, A. G., & Hsu, W. H. (2018) · Life Sciences · doi:10.1016/j.lfs.2017.12.025 · Cited by 721 · see citing works
“Goblet cells secrete mucin to create the mucus layer, which is turned over at varying rates [30].”
Background
Intranasal Drug Delivery: How, Why and What For?
Pires, A., Fortuna, A., Alves, G., & Falcão, A. (2009) · Journal of Pharmacy & Pharmaceutical Sciences · doi:10.18433/j3nc79 · Cited by 641 · see citing works
Nose-to-brain drug delivery: An update on clinical challenges and progress towards approval of anti-Alzheimer drugs
Agrawal, M., Saraf, S., Saraf, S., Antimisiaris, S. G., Chougule, M. B., Shoyele, S. A., & Alexander, A. (2018) · Journal of Controlled Release · doi:10.1016/j.jconrel.2018.05.011 · Cited by 630 · see citing works
“3(a) the respiratory region consists of four types of cells including the basal cell, goblet cell, ciliated and non-ciliated columnar epithelium cell [79].”
Background
Intranasal drug delivery: opportunities and toxicologic challenges during drug development
Keller, L.-A., Merkel, O. M., & Popp, A. (2021) · Drug Delivery and Translational Research · doi:10.1007/s13346-020-00891-5 · Cited by 613 · see citing works
“In turn, those functions have a disruptive character and can thus lead to adverse side effects, which can be additive [192, 194, 204, 216].”
Background
Advances in biomedical applications of pectin gels
Munarin, F., Tanzi, M. C., & Petrini, P. (2012) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2012.07.002 · Cited by 583 · see citing works
Nasal mucoadhesive drug delivery: Background, applications, trends and future perspectives
Ugwoke, M. I., Agu, R. U., Verbeke, N., & Kinget, R. (2005) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2005.07.009 · Cited by 543 · see citing works
Tailoring Formulations for Intranasal Nose-to-Brain Delivery: A Review on Architecture, Physico-Chemical Characteristics and Mucociliary Clearance of the Nasal Olfactory Mucosa
Gänger, S., & Schindowski, K. (2018) · Pharmaceutics · doi:10.3390/pharmaceutics10030116 · Cited by 447 · see citing works
“Absorption enhancers can have a reversible effect on ciliary beat frequency [93].”
Influential
Intranasal drug delivery: An efficient and non-invasive route for systemic administration
Grassin‐Delyle, S., Buenestado, A., Naline, E., Faisy, C., Blouquit‐Laye, S., Couderc, L., Guen, M. L., Fischler, M., & Devillier, P. (2012) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2012.03.003 · Cited by 428 · see citing works
Permeability issues in nasal drug delivery
Arora, P., Sharma, S., & Garg, S. (2002) · Drug Discovery Today · doi:10.1016/s1359-6446(02)02452-2 · Cited by 426 · see citing works
Progress in brain targeting drug delivery system by nasal route
Khan, A. R., Liu, M., Khan, M. W., & Zhai, G. (2017) · Journal of Controlled Release · doi:10.1016/j.jconrel.2017.09.001 · Cited by 402 · see citing works
“Nasal clearance half life of the formulations is about 12–15 min [147].”
Background
Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research
Guastella, A. J., Hickie, I. B., McGuinness, M. M., Otis, M., Woods, E. A., Disinger, H. M., Chan, H.-K., Chen, T. F., & Banati, R. B. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.11.019 · Cited by 357 · see citing works
“The time between placement and when they first taste the saccharine is recorded as the clearance time (Marttin et al., 1998).”
BackgroundInfluential
Nasal route and drug delivery systems
Türker, S., Onur, E., & Özer, Y. A. (2004) · Pharmacy World & Science · doi:10.1023/b:phar.0000026823.82950.ff · Cited by 354 · see citing works
Surface-Modified Nanocarriers for Nose-To-Brain Delivery: From Bioadhesion to Targeting
Sonvico, F., Clementino, A. R., Buttini, F., Colombo, G., Pescina, S., Stanisçuaski Guterres, S., Raffin Pohlmann, A., & Nicoli, S. (2018) · doi:10.20944/preprints201802.0077.v1 · Cited by 306 · see citing works
“As a consequence, traditional nasal formulations exploit excipients able to increase viscosity and/or provide bioadhesion, such as hydrophilic polymers, to counteract mucociliary clearance, prolong formulation residence time, improve systemic bioavailability, and reduce nasal absorption variability [82].”
Background
Stimuli-responsive In situ gelling system for nose-to-brain drug delivery
Agrawal, M., Saraf, S., Saraf, S., Dubey, S. K., Puri, A., Gupta, U. D., Kesharwani, P., Ravichandiran, V., Kumar, P., Naidu, V. G. M., et al. (2020) · Journal of Controlled Release · doi:10.1016/j.jconrel.2020.07.044 · Cited by 299 · see citing works
Cyclodextrins in nasal drug delivery
Merkus, F. W. H. M. (1999) · Advanced Drug Delivery Reviews · doi:10.1016/s0169-409x(98)00054-4 · Cited by 222 · see citing works
Enhanced bioavailability of metoclopramide HCl by intranasal administration of a mucoadhesive in situ gel with modulated rheological and mucociliary transport properties
Zaki, N. M., Awad, G. A. S., Mortada, N. D., & ElHady, S. S. A. (2007) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2007.08.006 · Cited by 214 · see citing works
Nanotherapeutics for Nose-to-Brain Drug Delivery: An Approach to Bypass the Blood Brain Barrier
Lee, D., & Minko, T. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13122049 · Cited by 219 · see citing works
Recent Advances in Protein and Peptide Drug Delivery: A Special Emphasis on Polymeric Nanoparticles
Patel, A., Patel, M., Yang, X., & Mitra, A. K. (2014) · Protein and Peptide Letters · doi:10.2174/0929866521666140807114240 · Cited by 209 · see citing works
“Cilia along with mucus layer generate a fluctuating movement to clear drug in approximately 12-15 min from nasal cavity [107].”
Background
Physiology and pathophysiology of respiratory mucosa of the nose and the paranasal sinuses
Beule, A. G. (2010) · PubMed Central · doi:10.3205/cto000071 · Cited by 206 · see citing works
“In addition, mechanical activity of cilia destroys drug molecules [37], [220].”
Background
Nasal Drug Delivery in Humans
Bitter, C., Suter, K., & Surber, C. (2011) · Current problems in dermatology · doi:10.1159/000321044 · Cited by 200 · see citing works
In situ gelling, bioadhesive nasal inserts for extended drug delivery: In vitro characterization of a new nasal dosage form
Bertram, U., & Bodmeier, R. A. (2005) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2005.08.005 · Cited by 182 · see citing works
Nasal-nanotechnology: revolution for efficient therapeutics delivery
Kumar, A., Pandey, A. N., & Jain, S. K. (2014) · Drug Delivery · doi:10.3109/10717544.2014.920431 · Cited by 171 · see citing works
“However, high viscosity of formulations hampers the regular functions like ciliary beating or mucociliary clearance and as a consequence modifies the permeability of drugs (Schipper et al., 1991; Merkus & Schusler-van Hees, 1992; Mason et al., 1995; Merkus et al., 1998).”
Background
Advancements in the Pharmaceutical Applications of Probiotics: Dosage Forms and Formulation Technology
Baral, K. C., Bajracharya, R., Lee, S. H., & Han, H. (2021) · International Journal of Nanomedicine · doi:10.2147/ijn.s337427 · Cited by 179 · see citing works
“Likewise, the intranasal delivery of probiotics is affected by various factors such as rapid mucociliary clearance, short retention time, small surface area, and enzymatic degradation.(19,20) In addition, the colonization of probiotic strains on the respiratory epithelium can be affected by the presence of the nasal m…”
Background
A review of intranasal formulations for the treatment of seizure emergencies
Kapoor, M., Cloyd, J. C., & Siegel, R. A. (2016) · Journal of Controlled Release · doi:10.1016/j.jconrel.2016.07.001 · Cited by 167 · see citing works
Nasal route for vaccine and drug delivery: Features and current opportunities
Lobaina, Y. (2019) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2019.118813 · Cited by 156 · see citing works
Nanotechnology for enhanced nose-to-brain drug delivery in treating neurological diseases
Huang, Q., Chen, Y., Zhang, W., Xia, X., Li, H., Qin, M., & Gao, H. (2024) · Journal of Controlled Release · doi:10.1016/j.jconrel.2023.12.054 · Cited by 151 · see citing works
In situ mucoadhesive-thermosensitive liposomal gel as a novel vehicle for nasal extended delivery of opiorphin
Mura, P., Mennini, N., Nativi, C., & Richichi, B. (2017) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2017.10.008 · Cited by 148 · see citing works
Efficacy, Safety and Mechanism of Cyclodextrins as Absorption Enhancers in Nasal Delivery of Peptide and Protein Drugs
Marttin, E., Verhoef, J. C., & Merkus, F. W. H. M. (1998) · Journal of drug targeting · doi:10.3109/10611869808997878 · Cited by 147 · see citing works
Self-citation
Effect of surface charge on the brain delivery of nanostructured lipid carriers in situ gels via the nasal route
Gabal, Y. M., Kamel, A. O., Sammour, O. A., & Elshafeey, A. H. (2014) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2014.07.025 · Cited by 144 · see citing works
Drug Delivery and Targeting to the Brain Through Nasal Route: Mechanisms, Applications and Challenges
Kashyap, K., & Shukla, R. (2019) · Current Drug Delivery · doi:10.2174/1567201816666191029122740 · Cited by 146 · see citing works
Polymeric Nanoparticles for Nasal Drug Delivery to the Brain: Relevance to Alzheimer's Disease
Rabiee, N., Ahmadi, S., Afshari, R., Khalaji, S., Rabiee, M., Bagherzadeh, M., Fatahi, Y., Dinarvand, R., Tahriri, M., Tayebi, L., et al. (2020) · Advanced Therapeutics · doi:10.1002/adtp.202000076 · Cited by 140 · see citing works
PEGylated nanomedicines: recent progress and remaining concerns
Vllasaliu, D., Fowler, R., & Stolnik, S. (2014) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.2014.866651 · Cited by 137 · see citing works
“For example, in the nasal mucosa, the mucociliary mechanism clears 50% of the administered dose (applied as a spray) from its ciliated respiratory mucosa within 15 -- 20 min [119].”
Background
Techniques of Intranasal Steroid Use
Benninger, M. S., Hadley, J. A., Osguthorpe, J. D., Marple, B. F., Leopold, D. A., Jennifer Derebery, M., & Hannley, M. (2004) · Otolaryngology · doi:10.1016/j.otohns.2003.10.007 · Cited by 136 · see citing works
Application of chitosan microspheres for nasal delivery of vaccines
Kang, M. L., Cho, C. S., & Yoo, H. S. (2009) · Biotechnology Advances · doi:10.1016/j.biotechadv.2009.06.007 · Cited by 131 · see citing works
“A substance administered through the nasal cavity is cleared from the nasal membrane in ~21 min through the mucociliary clearance, whereas the normal clearance time in the nasal mucosa of humans has been reported to be 12 to 15 min (Marttin et al., 1998).”
Background
Enhancing the Buccal Mucosal Delivery of Peptide and Protein Therapeutics
Caon, T., Jin, L., Simões, C. M. O., Norton, R. S., & Nicolazzo, J. A. (2014) · Pharmaceutical Research · doi:10.1007/s11095-014-1485-1 · Cited by 131 · see citing works
Pharmacokinetics and Pharmacodynamics of Intranasal Solid Lipid Nanoparticles and Nanostructured Lipid Carriers for Nose-to-Brain Delivery
Nguyen, T., & Maeng, H. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics14030572 · Cited by 131 · see citing works
Ion activated in situ gel of gellan gum containing salbutamol sulphate for nasal administration
Salunke, S. R., & Patil, S. B. (2016) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2016.02.044 · Cited by 126 · see citing works
A Review of Respiratory Anatomical Development, Air Flow Characterization and Particle Deposition
Islam, M. S., Paul, G. E., Ong, H. X., Young, P. M., Gu, Y., & Saha, S. C. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17020380 · Cited by 116 · see citing works
The use of human nasal in vitro cell systems during drug discovery and development
Dimova, S., Brewster, M., Noppe, M., Jorissen, M., & Augustijns, P. (2004) · Toxicology in Vitro · doi:10.1016/j.tiv.2004.07.003 · Cited by 116 · see citing works
Intranasal Delivery of Targeted Nanoparticles Loaded With miR-132 to Brain for the Treatment of Neurodegenerative Diseases
Su, Y., Sun, B., Gao, X., Dong, X., Fu, L., Zhang, Y., Li, Z., Wang, Y., Jiang, H., & Han, B. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.01165 · Cited by 114 · see citing works
Recent Advances in Intranasal Liposomes for Drug, Gene, and Vaccine Delivery
Duong, V., Nguyen, T., & Maeng, H. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15010207 · Cited by 114 · see citing works
Polyrotaxanes for applications in life science and biotechnology
Li, J. J., Zhao, F., & Li, J. (2011) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-010-3037-x · Cited by 108 · see citing works
“CD rings as host molecules, various guest molecules have been investigated to form inclusion complexes (IC) with enhanced physical and biological properties for drug delivery ( Merkus et al. 1998, 1999; Romeo et al. 1998; Uekama et al. 1998; Hirayama and Uekama 1999; Irie and Uekama 1999; Loftssona and Jarvinen 1999),…”
Background
Using the Intranasal Route to Administer Drugs to Treat Neurological and Psychiatric Illnesses: Rationale, Successes, and Future Needs
Lofts, A., Abu-Hijleh, F. A., Rigg, N., Mishra, R. K., & Hoare, T. R. (2022) · CNS Drugs · doi:10.1007/s40263-022-00930-4 · Cited by 108 · see citing works
“IN administration of liquid-based formulations can undergo rapid elimination by MCC in as little as ~ 12–15 min, while an additional (often significant) amount is lost due to drainage down the nasopharynx, which limits the contact time for drug absorption [24, 45].”
Background
Brain targeted rivastigmine mucoadhesive thermosensitive In situ gel: Optimization, in vitro evaluation, radiolabeling, in vivo pharmacokinetics and biodistribution
Abouhussein, D. M. N., Khattab, A., Bayoumi, N. A., Mahmoud, A. F., & Sakr, T. M. (2017) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2017.09.021 · Cited by 105 · see citing works
Drug delivery strategies for Alzheimer's disease treatment
Stefano, A. D., Iannitelli, A., Laserra, S., & Sozio, P. (2011) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.2011.561311 · Cited by 105 · see citing works
“through the mucus layer and cross the epithelial membrane of the nasal cavity, thus bypassing the clearance mechanisms imposed by the mucociliary apparatus, the broad range of metabolic enzymes present in the nasal tissues, and the efflux transporters that reside in the apical area of ciliated epithelial cells and in…”
Background
Nasal Powder Formulations: In-Vitro Characterisation of the Impact of Powders on Nasal Residence Time and Sensory Effects
Trenkel, M., & Scherließ, R. (2021) · Pharmaceutics · doi:10.3390/pharmaceutics13030385 · Cited by 104 · see citing works
“Elasticity was found to be the most important for an efficient transport rate with an optimal elastic modulus of 1–2 Pa [30].”
Background
Effects of N-trimethyl chitosan chloride, a novel absorption enhancer, on Caco-2 intestinal epithelia and the ciliary beat frequency of chicken embryo trachea
Thanou, M., Verhoef, J. C., Romeijn, S. G., Nagelkerke, J. F., Merkus, F. W. H. M., & Junginger, H. E. (1999) · International Journal of Pharmaceutics · doi:10.1016/s0378-5173(99)00126-x · Cited by 104 · see citing works
Drug Transport into the Mammalian Brain: The Nasal Pathway and its Specific Metabolic Barrier
Minn, A., Leclerc, S., Heydel, J., Minn, A.-L., Denizot, C., Cattarelli, M., Netter, P., & Grădinaru, D. (2002) · Journal of drug targeting · doi:10.1080/713714452 · Cited by 104 · see citing works
“Drug administration by the nasal pathway is currently considered as a particular systemic delivery method, allowing either administration of drugs that are poorly absorbed by the oral route, or for the local therapy of nasal–pharyngeal sphere diseases (Marttin et al., 1998).”
Background
Strategies to facilitate or block nose-to-brain drug delivery
Martins, P. P., Smyth, H. D. C., & Cui, Z. (2019) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2019.118635 · Cited by 99 · see citing works
Intranasal administration of carbamazepine to mice: A direct delivery pathway for brain targeting
Serralheiro, A., Alves, G., Fortuna, A. C., & Falcão, A. C. (2014) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2014.04.019 · Cited by 97 · see citing works
“Aware that nasal mucociliary clearance is one of the major limitations for nasal drug delivery (Marttin et al., 1998), the choice of a convenient nasal dosage form that avoids the rapid nasal drainage and promotes the increase of drug residence time within the nasal cavity is fundamental”
Background
Nasalin-situgels for delivery of rasagiline mesylate: improvement in bioavailability and brain localization
Ravi, P. R., Aditya, N., Patil, S. B., & Cherian, L. (2013) · Drug Delivery · doi:10.3109/10717544.2013.860501 · Cited by 95 · see citing works
“The nasal mucosal temperature has been reported to be between 32 and 35 C (Dahl & Mygind, 1998; Merkus et al., 1998) which is significantly different from overall body temperature.”
Background
Salivary oxytocin concentrations in males following intranasal administration of oxytocin: a double-blind, cross-over study
Daughters, K., Manstead, A. S. R., Hubble, K., Rees, A., Thapar, A., & van Goozen, S. H. M. (2015) · PLOS ONE · doi:10.1371/journal.pone.0145104 · Cited by 92 · see citing works
Improved In Vitro Model for Intranasal Mucosal Drug Delivery: Primary Olfactory and Respiratory Epithelial Cells Compared with the Permanent Nasal Cell Line RPMI 2650
Ladel, S., Schlossbauer, P., Flamm, J., Luksch, H., Mizaikoff, B., & Schindowski, K. (2019) · Pharmaceutics · doi:10.3390/pharmaceutics11080367 · Cited by 94 · see citing works
How to characterize a nasal product. The state of the art of in vitro and ex vivo specific methods
Salade, L., Wauthoz, N., Goole, J., & Amighi, K. (2019) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2019.02.026 · Cited by 92 · see citing works
Transmucosal drug administration as an alternative route in palliative and end-of-life care during the COVID-19 pandemic
Lam, J. K. W., Cheung, C. K. C., Chow, M. Y. T., Harrop, E. J., Lapwood, S., Barclay, S. I. G., & Wong, I. C. K. (2020) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2020.10.018 · Cited by 91 · see citing works
Muco-ciliary transport: Effect of mucus viscosity, cilia beat frequency and cilia density
Lee, W. L., Jayathilake, P. G., Tan, Z., Le, D. V., Lee, H. P., & Khoo, B. C. (2011) · Computers & Fluids · doi:10.1016/j.compfluid.2011.05.016 · Cited by 91 · see citing works
Development and Characterization of Mucoadhesive In Situ Nasal Gel of Midazolam Prepared with Ficus carica Mucilage
Basu, S., & Bandyopadhyay, A. K. (2010) · AAPS PharmSciTech · doi:10.1208/s12249-010-9477-x · Cited by 91 · see citing works
“The lowering of gelation temperature with addition of mucoadhesive agents attributed to the fact that the mucoadhesive agents formed hydrogen bonds with Pluronic to promote dehydration leading to increased entanglement of adjacent molecules and thereby enhancing micellar association (32,33).”
Background
Air-Liquid Interface Culture of Serially Passaged Human Nasal Epithelial Cell Monolayer forIn VitroDrug Transport Studies
Lee, M., Yoo, J., Lin, H., Kim, Y.-S., Kim, D., Choi, Y.-M., Park, S., Lee, C. H., & Roh, H. (2005) · Drug Delivery · doi:10.1080/10717540500177009 · Cited by 85 · see citing works
“Mucin was selected as the major mucous secretion in this study to observe the secretory cell differentiation, since drug transport might be affected by mucin on the surface of the epithelial cells (Marttin et al. 1998).”
Method
Solid Lipid Nanoparticles and Nanostructured Lipid Carriers as Smart Drug Delivery Systems in the Treatment of Glioblastoma Multiforme
Jnaidi, R., Almeida, A. J., & Gonçalves, L. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12090860 · Cited by 84 · see citing works
“For instance, mucociliary clearance is one of the significant factors that affects drug nose-to-brain delivery by limiting the residence time of substances administered via the nasal cavity [90].”
Background
Mucoadhesivein situnasal gelling drug delivery systems for modulated drug delivery
Singh, R. M. P., Kumar, A., & Pathak, K. (2012) · Expert Opinion on Drug Delivery · doi:10.1517/17425247.2013.746659 · Cited by 82 · see citing works
“These non-mucoadhesive formulations administered in limited volume of 25 -- 200 μl exhibit short residence time due to mucociliary clearance [28].”
Background
Brain distribution of ribavirin after intranasal administration
Colombo, G., Lorenzini, L., Zironi, E., Galligioni, V., Sonvico, F., Balducci, A. G., Pagliuca, G., Giuliani, A., Calzà, L., & Scagliarini, A. (2011) · Antiviral Research · doi:10.1016/j.antiviral.2011.09.012 · Cited by 80 · see citing works
Advanced formulations for intranasal delivery of biologics
Rohrer, J., Lupo, N., & Bernkop‐Schnürch, A. (2018) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2018.10.029 · Cited by 80 · see citing works
Formulation and Evaluation of In Situ Gelling Systems for Intranasal Administration of Gastrodin
Cai, Z., Song, X., Sun, F., Yang, Z., Hou, S., & Liu, Z. (2011) · AAPS PharmSciTech · doi:10.1208/s12249-011-9678-y · Cited by 79 · see citing works
“An evaluation of the toxicity on nasal cilia is much more convenient; thus, this index was used to evaluate the general nasal toxicity using the toad palate and rat nasal mucociliary method (32).”
Method
Intranasal delivery of interferon-β-loaded nanoparticles induces control of neuroinflammation in a preclinical model of multiple sclerosis: A promising simple, effective, non-invasive, and low-cost therapy
González, L. F., Acuña, E., Arellano, G., Morales, P., Sotomayor, P. C., Oyarzun-Ampuero, F. A., & Naves, R. F. (2020) · Journal of Controlled Release · doi:10.1016/j.jconrel.2020.11.019 · Cited by 79 · see citing works
Preparation and in vitro characterization of thermosensitive and mucoadhesive hydrogels for nasal delivery of phenylephrine hydrochloride
Xu, X., Shen, Y., Wang, W., Sun, C., Li, C., Xiong, Y., & Tu, J. (2014) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2014.08.015 · Cited by 78 · see citing works
“Since the mucocilia clearance was important for protecting the respiratory system, the impact of the formulations on the cilia movement should be analyzed [30].”
Background
Cyclodextrins in Nasal Delivery of Low-Molecular-Weight Heparins: In Vivo and in Vitro Studies
Yang, T., Hussain, A., Paulson, J. R., Abbruscato, T. J., & Ahsan, F. (2004) · Pharmaceutical Research · doi:10.1023/b:pham.0000032998.84488.7a · Cited by 77 · see citing works
“(18), nasally administered drug formulation will be diluted by the mucus and subsequently removed by the mucociliary clearance within a brief period of time.”
Background
Intranasal naloxone delivery is an alternative to intravenous naloxone for opioid overdoses
Merlin, M. A., Saybolt, M., Kapitanyan, R., Alter, S. M., Jeges, J., Liu, J., Calabrese, S., Rynn, K. O., Perritt, R., & Pryor, P. W. (2010) · The American Journal of Emergency Medicine · doi:10.1016/j.ajem.2008.12.009 · Cited by 75 · see citing works
“Certain synthetic opioids and opioid-like substances, such as tramadol and propoxyphene, have a dose-dependent response to naloxone and escape detection from our standard urine toxicologic screens [21].”
Background
Challenges and innovations of drug delivery in older age
Khan, M. S., & Roberts, M. S. (2018) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2018.09.003 · Cited by 77 · see citing works
Advancements in Nanoemulsion-Based Drug Delivery Across Different Administration Routes
Chatzidaki, M. D., & Mitsou, E. (2025) · Pharmaceutics · doi:10.3390/pharmaceutics17030337 · Cited by 74 · see citing works
“However, the nasal mucosa also presents challenges, as its mucus layer traps foreign substances [130] and the rapid removal of formulations occurs through the mucociliary clearance process.”
Application of RPMI 2650 nasal cell model to a 3D printed apparatus for the testing of drug deposition and permeation of nasal products
Pozzoli, M., Ong, H. X., Morgan, L. C., Sukkar, M. B., Traini, D., Young, P. M., & Sonvico, F. (2016) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2016.07.010 · Cited by 74 · see citing works
The delivery site of a monovalent influenza vaccine within the respiratory tract impacts on the immune response
Antoine Minne, A., Louahed, J., Mehauden, S., Baras, B., Renauld, J., & Rita Vanbever, A. (2007) · Immunology · doi:10.1111/j.1365-2567.2007.02641.x · Cited by 73 · see citing works
Brain delivery of intranasal in situ gel of nanoparticulated polymeric carriers containing antidepressant drug: behavioral and biochemical assessment
Kaur, P., Garg, T., Vaidya, B., Prakash, A. K., Rath, G., & Goyal, A. K. (2014) · Journal of drug targeting · doi:10.3109/1061186x.2014.994097 · Cited by 70 · see citing works
“Main problem with nasal delivery is the mucociliary clearance, which facilitates the clearance of nasally applied dosage forms from nose [24].”
Background
Novel mucoadhesive nasal inserts based on chitosan/hyaluronate polyelectrolyte complexes for peptide and protein delivery
Luppi, B., Bigucci, F., Mercolini, L., Musenga, A., Sorrenti, M., Catenacci, L., & Zecchi, V. (2009) · Journal of Pharmacy and Pharmacology · doi:10.1211/jpp.61.02.0003 · Cited by 69 · see citing works
“A major problem of nasal drug delivery is the mucociliary clearance mechanism, which rapidly removes non-mucoadhesive dosage forms from the absorption site.([4]) Mucoadhesive polymers can be used to prevent rapid clearance of the drug formulation, increasing the nasal residence time and thereby allowing longer absorpt…”
Background
Classification of Cilio‐Inhibiting Effects of Nasal Drugs
Merkus, P., Romeijn, S. G., Verhoef, J. C., Merkus, F. W. H. M., & Schouwenburg, P. F. (2001) · The Laryngoscope · doi:10.1097/00005537-200104000-00008 · Cited by 69 · see citing works
“Nasivin® Oxymetazoline, BAC, EDTA 2 (5) 4 (10) Ciliostatic”
Surfactant systems for nasal zidovudine delivery: structural, rheological and mucoadhesive properties
Carvalho, F. C., Barbi, M. D. S., Sarmento, V. H. V., Chiavacci, L. A., Netto, F. M., & Gremião, M. P. D. (2010) · Journal of Pharmacy and Pharmacology · doi:10.1211/jpp.62.04.0004 · Cited by 68 · see citing works
“Nasal mucociliary clearance largely determines the absorption profile of nasal drug delivery, since the residence time of drugs delivered to the nasal cavity is limited by this mechanism.([6,7]) To optimize nasal uptake, bioadhesive drug delivery systems have been studied.”
Background
Nanotechnological Advances for Nose to Brain Delivery of Therapeutics to Improve the Parkinson Therapy
Khatri, D. K., Preeti, K., Tonape, S., Bhattacharjee, S., Patel, M., Shah, S., Singh, P. K., Srivastava, S., Gugulothu, D., Vora, L., et al. (2023) · Current Neuropharmacology · doi:10.2174/1570159x20666220507022701 · Cited by 75 · see citing works
Nasal Vaccine Delivery
Ramvikas, M., Arumugam, M., Chakrabarti, S. R., & Jaganathan, K. S. (2016) · Elsevier eBooks · doi:10.1016/b978-0-323-39981-4.00015-4 · Cited by 67 · see citing works
“• Normal defense mechanisms like mucociliary clearance and ciliary beating affect the permeability of the drug.(15)”
The importance of pre-formulation studies and of 3D-printed nasal casts in the success of a pharmaceutical product intended for nose-to-brain delivery
Deruyver, L., Rigaut, C., Lambert, P., Haut, B., & Goole, J. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2021.113826 · Cited by 67 · see citing works
“It is reported that a mucociliary transit greater than 30 minutes may be considered abnormal and could signify a potential alteration of the nasal mucosa [106].”
Background
Targeted delivery of intranasally administered nanoparticles-mediated neuroprotective peptide NR2B9c to brain and neuron for treatment of ischemic stroke
Li, R., Huang, Y., Chen, L., Zhou, H.-H., Zhang, M., Chang, L., Shen, H. Y., Zhou, M., Su, P., & Zhu, D. (2018) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2018.10.013 · Cited by 67 · see citing works
Antimicrobial Essential Oil Formulation: Chitosan Coated Nanoemulsions for Nose to Brain Delivery
Rinaldi, F., Oliva, A., Sabatino, M., Imbriano, A., Hanieh, P. N., Garzoli, S., Mastroianni, C. M., Angelis, M. D., Miele, M. C., Arnaut, M., et al. (2020) · Pharmaceutics · doi:10.3390/pharmaceutics12070678 · Cited by 66 · see citing works
Nose-to-brain delivery of antipsychotics using nanotechnology: a review
Tan, M. S. A., Parekh, H. S., Pandey, P. M., Siskind, D. J., & Falconer, J. R. (2020) · Expert Opinion on Drug Delivery · doi:10.1080/17425247.2020.1762563 · Cited by 65 · see citing works
“After intranasal liquid or suspension-based drug administration, mucociliary clearance mechanisms are triggered, which typically remove the formulation from mucosa within 15–30 minutes at an average velocity of 5–8 mm per minute [33,34,40].”
Background
Thermally Triggered Mucoadhesive In Situ Gel of Loratadine: β-Cyclodextrin Complex for Nasal Delivery
Singh, R. M. P., Kumar, A., & Pathak, K. (2013) · AAPS PharmSciTech · doi:10.1208/s12249-013-9921-9 · Cited by 65 · see citing works
Mucoadhesive and mucus-penetrating interpolyelectrolyte complexes for nose-to-brain drug delivery
Porfiryeva, N. N., Ивановна, С. И., Анясович, С. И., Moustafine, R. I., & Khutoryanskiy, V. V. (2021) · Nanomedicine Nanotechnology Biology and Medicine · doi:10.1016/j.nano.2021.102432 · Cited by 64 · see citing works
“system, characterised by the presence of a mucus blanket that continuously being reformed through the production of mucins and movement as a result of mucociliary clearance.(49,50) This”
Background
Development and evaluation of in situ nasal gel formulations of loratadine.
Sherafudeen, S. P., & Vasantha, P. V. (2015) · Europe PMC (PubMed Central) · Cited by 63 · see citing works
Spray dried powders for nasal delivery: Process and formulation considerations
Henriques, P., Fortuna, A. C., & Doktorovová, S. (2022) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2022.05.002 · Cited by 64 · see citing works
Mucoadhesive Polymeric Hydrogels for Nasal Delivery of Acyclovir
Alsarra, I. A., Hamed, A. Y., Mahrous, G. M., Maghraby, G. M. E., Al-Robayan, A. A., & Alanazi, F. K. (2008) · Drug Development and Industrial Pharmacy · doi:10.1080/03639040802360510 · Cited by 63 · see citing works
Nanotechnology for CNS delivery of bio-therapeutic agents
Shah, L. K., Yadav, S. K., & Amiji, M. M. (2013) · Drug Delivery and Translational Research · doi:10.1007/s13346-013-0133-3 · Cited by 64 · see citing works
“Another major factor is the mucocilliary clearance which is a self-clearing mechanism where external agents once bound to the mucus are transported to the nasophayrnx and eventually to the gastrointestinal tract [56].”
Brain targeted delivery of mucoadhesive thermosensitive nasal gel of selegiline hydrochloride for treatment of Parkinson's disease
Sridhar, V., Wairkar, S., Gaud, R. S., Bajaj, A., & Meshram, P. V. (2017) · Journal of drug targeting · doi:10.1080/1061186x.2017.1350858 · Cited by 62 · see citing works
“However, intranasal delivery would be effective only when the drug is in contact with nasal epithelium for a sufficient period to diffuse into the olfactory projections [25].”
Background
The Effect of Drugs and Other Compounds on the Ciliary Beat Frequency of Human Respiratory Epithelium
Workman, A. D., & Cohen, N. A. (2014) · American Journal of Rhinology and Allergy · doi:10.2500/ajra.2014.28.4092 · Cited by 60 · see citing works
Lipid emulsions as vehicles for enhanced nasal delivery of insulin
Mitra, R., Pezron, I., Chu, W. A., & Mitra, A. K. (2000) · International Journal of Pharmaceutics · doi:10.1016/s0378-5173(00)00506-8 · Cited by 59 · see citing works
Preparation of ion-activated in situ gel systems of scopolamine hydrobromide and evaluation of its antimotion sickness efficacy
Cao, S., Zhang, Q., & Jiang, X. (2007) · Acta Pharmacologica Sinica · doi:10.1111/j.1745-7254.2007.00540.x · Cited by 58 · see citing works
Enhanced transbuccal salmon calcitonin (sCT) delivery: Effect of chemical enhancers and electrical assistance on in vitro sCT buccal permeation
Oh, D.-H., Chun, K.-H., Jeon, S.-O., Kang, J. W., & Lee, S. K. (2011) · European Journal of Pharmaceutics and Biopharmaceutics · doi:10.1016/j.ejpb.2011.05.010 · Cited by 58 · see citing works
Improved nasal bioavailability of elcatonin by insoluble powder formulation
Ishikawa, F., Katsura, M., Tamai, I., & Tsuji, A. (2001) · International Journal of Pharmaceutics · doi:10.1016/s0378-5173(01)00736-0 · Cited by 58 · see citing works
“In contrast, although the dry powder formulation using water-soluble lactose as a drug carrier is available for the pulmonary dry powder inhalation ( Malcolmson and Embleton, 1998 ), this apparently does not increase the absorption of polar molecules via the nasal route (Nagai et al., 1984; Ugwoke et al., 2000).”
Background
A gellan gum derivative as in-situ gelling cationic polymer for nasal drug delivery
Jelkmann, M., Leichner, C., Zaichik, S., Laffleur, F., & Bernkop‐Schnürch, A. (2020) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2020.04.114 · Cited by 57 · see citing works
Gellan gum-based mucoadhesive microspheres of almotriptan for nasal administration: Formulation optimization using factorial design, characterization, and in vitro evaluation
Abbas, Z., & Marihal, S. (2014) · Journal of Pharmacy And Bioallied Sciences · doi:10.4103/0975-7406.142959 · Cited by 57 · see citing works
“NMCC is one of the most important limiting factor for nasal drug delivery as it severely limits the time allowed for drug absorption to occur and effectively rules out the option of sustained nasal drug administration.[10] Several approaches are discussed in the literature to increase the residence time of drug formul…”
Nasal drug delivery: Design of a novel mucoadhesive and in situ gelling polymer
Menzel, C., Jelkmann, M., Laffleur, F., & Bernkop‐Schnürch, A. (2016) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2016.11.055 · Cited by 57 · see citing works
Intranasal delivery of antipsychotic drugs
Katare, Y. K., Piazza, J. E., Bhandari, J., Daya, R. P., Akilan, K., Simpson, M. J., Hoare, T. R., & Mishra, R. K. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2016.11.027 · Cited by 57 · see citing works

The Nasal Mucociliary Clearance: Relevance to Nasal Drug Delivery
Schipper, N. G. M., Verhoef, J. C., & Merkus, F. W. H. M. (1991) · Pharmaceutical Research · doi:10.1023/a:1015830907632 · Cited by 213 · see citing works
The biopharmaceutical aspects of nasal mucoadhesive drug delivery
Ugwoke, M. I., Verbeke, N., & Kinget, R. (2001) · Journal of Pharmacy and Pharmacology · doi:10.1211/0022357011775145 · Cited by 355 · see citing works
Quantitative Estimation of the Effect of Nasal Mucociliary Function on in Vivo Absorption of Norfloxacin after Intranasal Administration to Rats
Inoue, D., Kimura, S., Kiriyama, A., Katsumi, H., Yamamoto, A., Ogawara, K., Higaki, K., Tanaka, A., Yutani, R., Sakane, T., et al. (2018) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.8b00464 · Cited by 17 · see citing works
Mucociliary clearance and drug delivery via the respiratory tract
Lansley, A. B. (1993) · Advanced Drug Delivery Reviews · doi:10.1016/0169-409x(93)90014-u · Cited by 55 · see citing works
Influence of the nasal mucociliary system on intranasal drug administration.
Wang, J., & Bu, G. (2000) · PubMed · Cited by 4 · see citing works

Authors: Marttin, E., Schipper, N. G. M., Verhoef, J. C., & Merkus, F. W. H. M.
Corresponding author: Merkus, Frans W.H.M
ORCID: Schipper, Nicolaas G.M
Venue: Advanced Drug Delivery Reviews
Publisher: Elsevier BV
Published: 1998-01
Volume: 29
Issue: 1-2
Pages: 13-38
ISSN: 0169-409X (ISSN-L)
DOI: 10.1016/s0169-409x(97)00059-8
OpenAlex: W2089895093
Cited by: 469
References: 255
Citations by year: 2026: 24 · 2025: 45 · 2024: 26 · 2023: 40 · 2022: 32 · 2021: 34 · 2020: 26 · 2019: 16 · 2018: 27 · 2017: 15 · 2016: 18 · 2015: 14 · 2014: 24 · 2013: 17 · 2012: 15
FWCI: 0.51
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Advanced Drug Delivery Reviews (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Pharmacology, Toxicology and Pharmaceutics › Pharmaceutical Science › Advanced Drug Delivery Systems
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Inhalation and Respiratory Drug Delivery
Health Sciences › Medicine › Otorhinolaryngology › Sinusitis and nasal conditions
Keywords: nasal mucociliary clearance, intranasal drug delivery, ciliary beat frequency, mucus transport, pharmaceutical excipients, nasal drug absorption, residence time, toxicity screening, upper airway diseases, in vitro-in vivo correlation

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Nasal mucociliary clearance as a factor in nasal drug delivery

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