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Acute Bacterial Rhinosinusitis Causes Hyperresponsiveness to Histamine Challenge in Mice

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Acute Bacterial Rhinosinusitis Causes Hyperresponsiveness to Histamine Challenge in Mice ORIGINAL ARTICLE Acute Bacterial Rhinosinusitis Causes Hyperresponsiveness to Histamine Challenge in Mice James J. Klemens, MD; Virat Kirtsreesakul, MD; Thongchai Luxameechanporn, MD; Robert M. Naclerio, MD Objectives: To develop a physiologic test of nasal re- termine whether acute sinusitis causes nasal hyperre- sponsiveness in mice and to evaluate whether mice with sponsiveness to histamine exposure. acute bacterial sinusitis develop nasal hyperresponsive- ness. Results: Nasal histamine challenge led to a reproduc- ible, dose-dependent increase in sneezing and nose rubs. Design: Several experimental studies will be described. The response to histamine exposure was blocked by des- The first was a titration pilot study. The second was a loratadine (PՅ.05). Allergic mice had a significant in- randomized, placebo-controlled study. The remainder crease in responsiveness (PՅ.05) over baseline after ex- were before-and-after trials. posure to antigen. Mice with acute sinusitis had a sustained increase in responsiveness, although less se- Species: BALB/c or C57BL/6 mice. vere than after allergy, compared with baseline values that lasted 12 days after infection (PՅ.05). Interventions: For these experiments, we exposed mice to histamine intranasally, then counted the number of Conclusions: Nasal challenge with histamine is a physi- sneezes and nose rubs as the primary outcome measure ologic test of nasal responsiveness. The hyperrespon- of nasal responsiveness. First, we constructed a dose- siveness of allergic mice to histamine exposure parallels response curve. Second, we treated the mice with des- the response to nonspecific stimuli during the human al- loratadine, a histamine 1 receptor antagonist, prior to his- lergic reaction. In addition, we showed that acute bac- tamine exposure. Third, we challenged, with intranasal terial sinusitis causes nasal hyperresponsiveness in mice. histamine, mice made allergic using 2 techniques. Fourth, we infected mice with Streptococcus pneumoniae to de- Arch Otolaryngol Head Neck Surg. 2005;131:905-910 ASAL HYPERRESPONSIVE- ity. In allergic patients, an increase in the ness to irritants and to re- number of muscarinic receptors has been petitive allergen expo- described by some investigators,5,6 whereas sure is a well-established van Megen et al7 described not only a phenomenon associated decrease in the number of muscarinic re- with allergic rhinitis.1 In humans, hyper- ceptors, but also an increase in their N 6 responsiveness to allergens increases af- sensitivity. Ishibe et al described down- ter an antigen challenge (priming).2 Non- regulation of adrenergic receptors in al- specific hyperresponsiveness to irritants lergic patients. Local changes related to an Author Affiliations: such as histamine, methacholine, brady- increase in the numbers of eosinophils, Department of Surgery, Section kinin, and cold, dry air also increases af- neutrophils, basophils, and lymphocytes of Otolaryngology–Head and 1 Neck Surgery, The University of ter allergen challenge. These laboratory and their released mediators after anti- Chicago Hospitals, Chicago, Ill events correlate with the response of pa- gen exposure have been implicated in the (Drs Klemens, Kirtsreesakul, tients to cold weather and strong odors, development of nasal hyperresponsive- Luxameechanporn, and like that of gasoline. ness.8 Naclerio); Department of How allergic exposure causes nasal hy- When histamine contacts the nasal Otolaryngology, Prince of perresponsiveness is unknown.3 There are mucosa, it causes an increase in vascular Songkla University, Hat Yai, several proposed hypotheses for the un- permeability, dilation of the cavernous Songkla, Thailand derlying mechanism. Increased epithe- sinusoids, and neuronal stimulation.9 (Dr Kirtsreesakul); and lial permeability may allow easier access Increased nasal secretion is caused Department of 4 Otolaryngology–Head and Neck of stimuli to nerve endings. An increase primarily by nerve-mediated parasym- Surgery, Ramathibodi Hospital, in sensitivity or in the number of irritant pathetic glandular secretion and an Mahidol University, Bangkok, receptors, or a decrease in the number or increase in vascular leakage. Nasal con- Thailand responsiveness of sympathetic receptors, gestion is mediated primarily by pooling (Dr Luxameechanporn). may result in increased mucosal sensitiv- of blood in the vascular sinusoids. Nasal (REPRINTED) ARCH OTOLARYNGOL HEAD NECK SURG/ VOL 131, OCT 2005 WWW.ARCHOTO.COM 905 ©2005 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/30/2021 itchiness and sneezing are thought to be secondary to NASAL CHALLENGE WITH HISTAMINE histamine’s actions on the trigeminal nerve.9-11 Clement et al12 showed that allergic patients have increased nasal Because mice are obligate nose breathers, small droplets of so- resistance after topical application of histamine, sug- lution were placed on the external nares of awake mice to be gesting that there is pooling of blood in the cavernous drawn into the nasal passages during inhalation. The nasal chal- sinusoids. However, nasal airway resistance is variable lenge with histamine consisted of intranasal application of 50 µL of various concentrations of histamine (Sigma-Aldrich, St in humans. There is considerable overlap between Louis, Mo) applied gradually over 2 minutes. In our initial ef- healthy and allergic patients in their response to hista- forts, we used 5 different concentrations: a isotonic sodium chlo- mine exposure; thus, it is not a reliable test of hyperre- ride (vehicle for dissolving histamine); 1-, 10-, 30-, and 100mM sponsiveness.3 Numata et al10 found that, although histamine; but, because of the stress on the mice, the chal- patients reported a lesser degree of congestive symp- lenge was changed to 3 exposures of 0.3-, 3.0-, and 30mM his- toms after antihistamine treatment, this did not corre- tamine. late with objective rhinomanometry. Gerth van Wijk et After each exposure, we observed the mice for 10 minutes al13 suggested that measurements of sneezing and secre- and counted the number of sneezes and nose-rubbing epi- tions were more accurate assessments of hyperrespon- sodes. Each count was performed by the same investigator siveness to histamine exposure. (J.J.K.) who was blinded to the treatment groups. From these data, we constructed dose-response curves. We investigated whether acute bacterial rhinosinu- sitis causes nasal hyperresponsiveness to histamine ex- posure in mice. Research on sinusitis in humans is lim- DESLORATADINE GAVAGE ited by access to the sinuses and the types of studies that ethically can be done. Therefore, we developed a mouse Mice were treated with 10 mg/kg of desloratadine by gavage in a methylcellulose vehicle 4 hours prior to nasal challenge with model of acute bacterial rhinosinusitis. histamine. The controls for this experiment were given an Little is known about sinusitis-induced hypersensi- equivalent volume of methylcellulose (Dow Chemical Co, Mid- 14 tivity in humans. Sampaio et al, in an abstract, re- land, Mich), the vehicle for desloratadine, by gavage. ported decreased ipsilateral nasal secretions after intra- nasal histamine challenge in a few patients with chronic ALLERGIC SENSITIZATION sinusitis compared with healthy control subjects and no difference in the contralateral secretory or the sneezing Two techniques were used. For the first technique, mice were response. Whether acute bacterial sinusitis causes dif- sensitized by intraperitoneal (IP) injection of 20 µg of ovalbu- ferences in nasal mucosal hyperresponsiveness has not min (Sigma-Aldrich) together with an aluminum hydroxide been studied. (Pierce Biotechnology, Inc, Rockford, Ill) adjuvant. Eight days To test the hypothesis that acute bacterial sinusitis after the first IP exposure, the mice received a second injec- causes hyperresponsiveness, we needed to develop a non- tion. Two days after the second injection, the animals were ex- specific test of nasal hyperresponsiveness in mice. posed to a 6% ovalbumin solution in 0.1M phosphate- Imamura and Kambara15 used substance P and hista- buffered saline (PBS) (Roche Diagnostics Corporation, mine applied intranasally to measure the sneeze re- Indianapolis, Ind) by intranasal inoculation daily for 5 days. 16 For the second technique, mice were injected with aluminum sponses in guinea pigs. Saito et al applied intranasal his- hydroxide and PBS, but no ovalbumin. These mice were then tamine to study the kinetics of hyperresponsiveness in exposed to either 50 µL of 6% ovalbumin or an equivalent vol- allergic mice. Thus, we chose histamine as a stimulus. ume of PBS daily for the duration of the experiment. We first established a dose-response curve to intra- nasal histamine exposure in healthy mice. We then dem- INDUCTION OF SINUSITIS onstrated that the response to nasal histamine challenge could be blocked by treatment with a histamine Soy broth was used for control animals and soy broth contain- 1–antihistamine, desloratadine (Schering=Plough, Ke- ing Streptococcus pneumoniae for experimental animals. The nilworth, NJ). Next, we histamine-challenged mice that American Tissue Culture Collection, Rockville, Md, strain of had been sensitized to ovalbumin by 2 different meth- S pneumoniae was obtained from the Clinical Microbiology Labo- ods to determine whether mice, like humans, became hy- ratories of the University of Chicago Hospitals. Fifty microli- perresponsive after allergen stimulation. Finally, we ap- ters of 109
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