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  • 1 Department of Otorhinolaryngology, Head and Neck Surgery, Otto Körner Rostock University Medical Center, Rostock, Germany
  • 2 Institute of Medical Microbiology, Virology and Hygiene, Rostock University Medicical Center, Rostock, Germany
  • 3 Institute of Microbiology, Infectious Diseases and Immunology Charité – University Medicine Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin and Berlin Institute of Health, Berlin, Germany
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Abstract

We report a case of a chronic mesotympanic otitis media with a smelly purulent secretion from both ears and recurrent otalgia over the last five years in a six-year-old girl after swimming in the German Baltic Sea. Besides Staphylococcus aureus a non-O1/non-O139 Vibrio cholerae strain could be isolated from patient samples. An antibiotic therapy with ciprofloxacin and ceftriaxone was administered followed by atticotomy combined with tympanoplasty. We conclude that V. cholerae should not be overlooked as a differential diagnosis to otitis infections, especially when patients present with extra-intestinal infections after contact with brackish- or saltwater aquatic environments.

Abstract

We report a case of a chronic mesotympanic otitis media with a smelly purulent secretion from both ears and recurrent otalgia over the last five years in a six-year-old girl after swimming in the German Baltic Sea. Besides Staphylococcus aureus a non-O1/non-O139 Vibrio cholerae strain could be isolated from patient samples. An antibiotic therapy with ciprofloxacin and ceftriaxone was administered followed by atticotomy combined with tympanoplasty. We conclude that V. cholerae should not be overlooked as a differential diagnosis to otitis infections, especially when patients present with extra-intestinal infections after contact with brackish- or saltwater aquatic environments.

Background

Otitis media is defined as an infectious inflammatory condition of the middle ear, particularly affecting children. Two types of otitis media are typically differentiated [1, 2]. Acute otitis media constitutes a painful inflammation of the middle ear mucous membranes, usually caused by viral or bacterial infection, displaying a rapid onset, often accompanied with otalgia, fever, hearing loss and even a tympanic perforation with otorrhoea [3, 4]. Chronic mesotympanic otitis media is characterized by a persistent central tympanic membrane defect. Despite antibiotic therapy, chronic mesotympanic otitis media may be the result of an acute otitis media [4]. Other factors leading to a chronic mesotympanic otitis media are a tubal occlusion, a mechanical, thermal or chemical injury, a blast trauma or of iatrogenic origin (e.g. drainage of the middle ear by a tympanic tube) [5]. Patients with craniofacial malformations are at increased risk of developing a chronic mesotympanic otitis media. Chronic mesotympanic otitis media is one of the most common chronic infectious diseases worldwide [6] and hearing loss constitutes one of the most common sequelae of chronic mesotympanic otitis media. Life threatening intracranial complications such as brain abscesses and meningitis have also been described [7].

Microbiological analyses are helpful in order to distinguish chronic mesotympanic otitis media from an acute otitis media. Bacterial species causing acute otitis media include Streptococcus pneumoniae, Staphylococcus aureus, Haemophilus influenzae and Moraxella catarrhalis [8]. In case of chronic mesotympanic otitis media, both, aerobic and obligate anaerobic bacteria might be considered as causative infectious agents: Pseudomonas aeruginosa and S. aureus are the most common aerobic microbial species, followed by Proteus vulgaris and Klebsiella pneumoniae [1, 9] whereas anaerobic pathogens including Bacteroides spp., Clostridium spp., Peptococcus spp., Peptostreptococcus spp., Prevetolla melaninogenica and Fusobacterium spp. are rather rarely isolated from patients suffering from chronic mesotympanic otitis media, however [1, 2]. An exacerbation of chronic otitis media may be observed in the course of upper respiratory tract infections or following water penetration through the tympanic membrane into the middle ear during bathing or swimming [1].

Vibrio cholerae are rarely isolated from human patient samples in Germany and if so, usually after having acquired the bacteria abroad in high prevalence countries [10]. V. cholerae consist of more than 200 serogroups. To date best characterized are the cholera toxin producing O1 and O139 serogroups, representing the strains causing epidemic cholera with subsequent diarrhoeal illness [11, 12]. However, infections following a second group of non-O1/non-O139 serogroups are characterized by self-limiting milder gastrointestinal illnesses that are less frequently associated with extra-intestinal infectious manifestations including ear infections, but also wound infections, skin and soft tissue infections, cholangitis, peritonitis, meningitis, and septicaemia [10, 13–17]. Commonly Vibrio bacteria are found as natural inhabitants of brackish- or saltwater aquatic environments in association with chitinous organisms, aquatic plants, phytoplankton and protozoa [15, 18, 19]. The pathogen transmission primarily takes place via non- or insufficient filtered drinking water and contaminated food. Given that high water temperatures facilitate infections with Vibrio spp., peak prevalences of illnesses are documented in the late summer [20, 21]. For the first time we here report a case of chronic otitis media upon infection with non-O1/non-O139 V. cholerae in a six-year-old girl who had acquired the Vibrio strain most probably after swimming in the German Baltic Sea.

Case presentation

In January 2019, a six-year-old girl presented to a tertiary medical centre with clinical signs of a chronic mesotympanic otitis media that was accompanied with smelly purulent secretion from both ears lasting for five years. Due to the recurrent otalgia the patient had undergone an adenectomy and drainage of the middle ear on both sides at the age of one year. In addition, at the age of two, the girl had undergone a prolonged recovery after a mastoiditis treated by a left-side mastoidectomy. Since the otalgia could neither be sufficiently treated by oral nor by intravenous treatment with antibiotics such as penicillin and cefuroxim, the patient had to undergo a mastoidectomy on the right side in 2016. Anamnestic inquiry revealed no travel outside of Germany in the past six years, however, the mother reported frequent travels to the German Baltic sea, last in September 2018. Upon microscopic examination, a granulated central defect could be detected in the two lower tympanic quadrants of the right ear (Fig. 1), whereas in the left ear a kidney-shaped perforation was observed. Furthermore, both ears showed a purulent secretion. The Weber test revealed a lateralized result to the left ear and the Rinne's test was weakly negative. A spontaneous nystagmus was not observed, however. The data obtained in the audiogram matched to a conductive hearing loss (Fig. 2). There was no pain on palpation of the mastoid process.

Fig. 1.
Fig. 1.

(A) Right ear before antimicrobial and surgical treatment (B) CT showed a radical cavity on the right side (C) Otoscopic examination of the right ear after antimicrobial treatment (D) Otoscopic examination of the right ear three months after surgical treatment

Citation: European Journal of Microbiology and Immunology EuJMI 10, 3; 10.1556/1886.2020.00013

Fig. 2.
Fig. 2.

Mean right and left ear pure-tone thresholds showing a conductive deafness on both sides.

Citation: European Journal of Microbiology and Immunology EuJMI 10, 3; 10.1556/1886.2020.00013

As therapy, a bilateral tympanoplasty, starting on the right side, was considered. The pre-interventional computertomography (CT) showed a bilateral mastoid cavity with motion artifacts and a cutis enlargement in the right ear canal. There was no evidence of inflammatory mastoid involvement (Fig. 1). Additionally, an otic swab from the exudate was taken and subjected to microbiological analyses. S. aureus was isolated from both ears, accompanied by common skin bacterial commensals. Remarkably, V. cholera non-O1/non-O139 was additionally isolated in substantial amount from the right ear. Therefore, an inpatient treatment with ciprofloxacin ear drops and intravenous ceftriaxon (2 g once a day) was initiated prior to surgery. Five days later, both isolated pathogens were longer be isolated from a second microbiological swab analysis, and the atticotomy combined with tympanoplasty type III Partial Ossicular Replacement Prosthesis (PORP) could be carried out (Fig. 1). Intraoperatively, a compacted mucosa of the mastoid and tympanum appeared on the right side. The tuba auditiva was intact. The surgical treatment of the left ear followed within the same year.

Discussion and conclusions

V. cholerae constitutes a natural inhabitant of brackish or saltwater aquatic environments [19]. In addition to the best characterized O1 and O139 serogroups responsible for the epidemic cholera, also the non-O1 and non-O139 serogroups with less epidemic potential can be found. These non-O1/non-O139 strains are known to cause milder gastrointestinal infections and other rather non-specific infections in humans [11, 12, 15, 17]. Over the last years the numbers of infections with non-O1 and non-O139 V. cholera strains have been increasing [22]. Most of the case reports describe relatively mild gastrointestinal illness, ear and wound infections, whereas also cases of bacteraemia have been reported, however [13, 16, 20].

In the Western population, and particularly in Germany, V. cholerae infections are rarely documented. Most non-O1 and non-O139 V. cholerae infections diagnosed in Germany result from travelling to foreign countries [20]. In Germany there is no standard screening for V. cholerae infections. In case of chronic mesotympanic otitis media P. aeruginosa and S. aureus are the most common aerobic microbial species [1]. Life-threatening infections with the non-O1 and non-O139 serogroups are commonly reported in immunosuppressed patients, but very rarely in immunocompetent individuals without comorbidities [23]. The here presented patient was suffering from a chronic ear infection. Given potential associations with host and environmental factors (contaminated water supply), it is likely that the chronic ear infection may have facilitated the V. cholerae infection.

Since V. cholerae ear infections can only hardly, if at all, be differentiated from ear infections caused by other pathogens by clinical aspects, a microbiological analysis including isolation and species identification is crucial. The antimicrobial therapy of V. cholerae ear infections should comprise cephalosporins, fluoroquinolones or tetracyclines, if necessary in combination [10]. Whereas non-O1/non-O139 strains are sensitive to most antibiotic agents [24, 25], antimicrobial resistance of V. cholerae isolates has only been reported to aminoglycosides, ampicillin and carbapenems to date [26–28].

In the German coastal regions [29] and lakes but also in other European countries, pathogenic non-O1 and non-O139 V. cholerae isolates have been described (Table 1) [10, 29]. Due to the reported climate change we might experience an increased water temperature in the coastal regions, seas and lakes of central Europe. In consequence, the abundance of V. cholerae in these areas may rise [22] and more patients with V. cholerae infections present to the health services, particularly in hot summer periods. An association of Vibrio infections and increasing water temperature in the Baltic Sea has already been described [21, 22, 30]. High water temperatures (optimal temperature between 20 and 45 °C [31]) alone are not sufficient enough for an optimal propagation of this pathogen, given that salinity and distinct pH-levels (optimal growth conditions at pH between 6.5 and 9.0 [31]) comprise important prerequisites. The lowest salinity levels can be found in rivers and lakes (0.15–0.25%) as well as in the Baltic sea coast (0.8%), whereas the many regions of the Atlantic and the Mediterranean Sea comprise areas with too high levels of salinity (3.5%) [32].

Table 1.

Case reports from the literature of otitis caused by Vibrio cholerae non-O1/O139 strains. Modified after [15]

ReferenceCase reportedAge/gender (m = male, f = female)PlaceEnvironmental
[33]Prolonged middle-ear inflammation10/mSwedenBathing in the Baltic archipelago
[34]Middle ear infection–/–United StatesExposure to salt water
[35]Chronic external otitis12/fBelgiumUnknown
[36]Middle ear infection–/–RomaniaUnknown
[37]Otitis Media20/fBelgiumSwimming in a swimming pool
External otitis one year after eardrum transplant15/mUnknown
[38]Otitis media–/–GermanyUnknown
[39]Chronic recurrent Otitis media8/fAustriaUnknown
Otitis externa14/mSwimming in Lake Neusiedl (year 2000)
Otitis media49/mUnknown
Otitis externa22/mAfter vacation (unknown location)
Otitis media9/mSwimming in Lake Neusiedl (year 2004)
Otitis media9/fSwimming in Lake Neusiedl (year 2005)
[40]Otitis externa64/fMauritiusBathing in the Pacific Ocean
[41]Ear infection–/–United KingdomUnknown
[20]Otitis–/–Germany/AustriaExposure to Coastal regions, Lakes
[42]Otitis externa21/fAustriaSwimming in Lake Neusiedl (year 2015)
[22]Ear-infection with ear secretion–/–Sweden and FinlandExposure to Coastal regions
[15]Otitis media27/mIsraelWater skiing accident on the Murray River in Australia (year 2011)
[43]Acute otitis externa35/mSpainExposure to Mediterranean bathing site
[44]Otitis media11/mFranceSwimming in Lake Apremont
The current studyChronic otitis media5/fGermanyBathing in the German Baltic sea

Most reported patients with non-O1 and non-O139 V. cholerae ear infections presented with otitis externa or acute otitis media, whereas only two cases with a prolonged middle-ear inflammation have been reported to date (Table 1). Notably, i.) most reported non-O1 and non-O139 V. cholerae associated cases were detected in Europe, ii.) almost all patients of different age and gender were not suffering from immunosuppressive comorbidities, and iii.) infections were linked to contaminated water (Table 1). In the present case, the patient presented a mesotympanic otitis media, preexisting for several years. The cases described in the literature often showed an acute event followed by an acute infection without specific previous medical history. The bilateral tympanic perforation described here is most likely the result of a tympanic drainage in infancy leading to a superinfection by V. cholerae. The ear is particularly susceptible to penetrating water. There are favourable conditions for the multiplication of pathogens, especially in combination with S. aureus.

An untreated otitis media may be associated with complications culminating in a permanent damage of the ear. Other known complication are hearing loss, vertigo, facial paralysis, subperiosteal abscess and labyrinthitis [45, 46]. In addition to the intra-cranial complications also extra-cranial complications have been described [47, 48]. Fortunately, the young female patient in the current report did not display such complications.

In conclusion, physicians working in coastal and also high-latitude regions must be aware of non-O1 and non-O139 V. cholerae associated morbidities, especially when patients present with extra-intestinal infections after contact with brackish- or saltwater aquatic environments. Improved diagnostic evidence and clinical awareness of these emerging pathogens is therefore needed [22]. It may be advisable that clinicians alert at‐risk patients. V. cholerae should not be overlooked as a differential diagnosis to otitis infections.

Consent

Written informed consent was obtained from the parents for publication of this case report. A copy of the written informed consent is available for review by the Editor-in-Chief of this journal.

Funding sources

None.

Authors' contributions

SVB analysed and interpreted the patient data and was a major contributor in writing the manuscript. PW performed the microbiological examination and draughted the manuscript. MMH provided constructive advice to the study and the manuscript. All the authors were in agreement on the final version of the manuscript.

Competing interests

Markus M. Heimesaat is a member of the editorial board. The authors declare that they have no competing interests.

Acknowledgements

We thank the Robert Koch-Institute (ZBS 2, Speziallabor für hochpathogene mikrobielle Erreger) for typing the Vibrio cholerae strain.

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  • 1.

    Mittal R, Lisi CV, Gerring R, Mittal J, Mathee K, Narasimhan G, Current concepts in the pathogenesis and treatment of chronic suppurative otitis media. J Med Microbiol 2015;64:110316. https://doi.org/10.1099/jmm.0.000155.

    • Crossref
    • Search Google Scholar
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