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 Table of Contents  
ORIGINAL ARTICLE
Year : 2017  |  Volume : 19  |  Issue : 2  |  Page : 108-113

A study of alteration of nasal bacterial flora during diving


1 Department of ENT, INHS Kalyani, Visakhapatnam, Andhra Pradesh, India
2 Department of ENT, INHS Asvini, Mumbai, Maharashtra, India

Date of Web Publication13-Feb-2018

Correspondence Address:
Dr. Anil Kaul
Department of ENT, INHS Asvini, Colaba, Mumbai - 400 005, Maharashtra
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jmms.jmms_47_17

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  Abstract 


Context: Recent times have heralded increased underwater activities both for professional and recreational purposes. There is little data regarding alteration of the nasal bacterial flora during wet and dry diving. In view of these, this study was undertaken to study the effect of diving on the bacterial flora of human nose. Aim: The aim of this study was to determine bacterial flora present in the nose of divers and changes occurring due to the effect of pressure and humidity as a consequence of diving activity. Setting and Design: A prospective observational study was carried out in a Naval Medical Center to determine bacterial flora present in the nose of divers and any alteration occurring in the flora as a consequence of diving. Materials and Methods: The participants were divided into four groups: Group I (nonswimmers); Group II (swimmers); Group III (compressed air divers); and Group IV (wet divers). Bacteriological specimens were taken from the anterior nares of all subjects as per laid down the schedule and were examined for evidence of bacterial growth and the colony characteristics were noted. Statistical analysis used was Chi-square test (Epi InfoTM). Results: Gram-positive organisms again predominated in the bacteria isolated in the various groups. Staphylococcus epidermidis predominated the nasal flora. Few Gram-negative bacteria were also isolated during the course of the study. Conclusions: There is increase in nasal flora commensals, with Gram-positive bacteria being predominant, on exposure to diving.

Keywords: Dry diving, nasal bacterial flora, wet diving


How to cite this article:
Malhotra T, Kaul A, Saxena N. A study of alteration of nasal bacterial flora during diving. J Mar Med Soc 2017;19:108-13

How to cite this URL:
Malhotra T, Kaul A, Saxena N. A study of alteration of nasal bacterial flora during diving. J Mar Med Soc [serial online] 2017 [cited 2019 Oct 19];19:108-13. Available from: http://www.marinemedicalsociety.in/text.asp?2017/19/2/108/225276




  Introduction Top


Exploration of newer environments is a constant habit of human beings. The modern diver equipped with specially developed gears that are products of burgeoning technology is an inheritor of centuries of exploration and invention that made undersea work possible. Recent times have heralded increased underwater activities both for professional and recreational purposes. The surface tissues of the body are continuously contaminated by microorganisms from the environment. Many fail to colonize, being unable to compete successfully with the highly adapted indigenous flora. The complex population of microorganisms regularly present is variously called the 'natural'/'indigenous'/'resident'/'normal' microbiota. In general, they do not cause obvious signs of ill-health unless the balance is disturbed by chemotherapy or disease. However, problems of rhinosinusitis and otitis externa are recognized infections in divers.

Bacteriology of Otitis externa is well documented. However, there is little data regarding alteration of nasal bacterial flora during diving. Straker et al[1] studied the relative frequency of three species Streptococcus pneumoniae, Hemolytic streptococci, and Haemophilus influenzae and compared them with the frequency of Gram-negative cocci in the nose, nasopharynx, and oropharynx. It was found that the four species were less frequent in the nose than in the nasopharynx. This difference is particularly striking for Gram-negative cocci, but there is less tendency for pathological species to colonise in the nose than in the nasopharynx. As per Se idler et al[2] there was no change in the species of the bacteria forming the normal flora of the anterior nares in any of the divers observed during the period of their study.

This study was conducted with the aim to determine any alteration occurring in the bacterial flora present in the nose of divers as a consequence of diving activities.


  Materials and Methods Top


It was a prospective observational study. Four groups of 20 healthy males in the age group of 18–32 years, each were selected by random sampling as follows:

  1. Group I (controls): This was the control group and consisted of nonswimmers. They were taken from the naval sailors undergoing training at a Naval Institute
  2. Group II (swimmers): This group participants were being taught swimming as a part of their training and had to subsequently spend considerable time in the swimming pool daily
  3. Group III (compressed air divers): Participants of this group consisted of active trained divers of the Navy
  4. Group IV (wet divers): Participants for this group were also drawn from among active trained divers of the Navy.


Any participants with a history of any significant otorhinolaryngological problems in the past or any ear, nose, or throat problems a month before the conduct of the study were excluded from the study. Before the commencement of the study, necessary clearance was obtained from the Institutional Ethical committee. Written informed consent was obtained from all the selected participants. All individuals from the four study groups were subjected to a general medical examination, and a detailed ENT examination before they were selected for the study. The results of this initial examination and subsequent examinations were recorded on a proforma.

All individuals were disallowed swimming 15 days before the conduct of the study. Group I (control) participants continued with their normal daily activities but were disallowed swimming. Nasal swabs (with due aseptic precautions) were taken from both nares of this group daily for 15 days. Group II (swimmers) spent 1½ h daily in the demarcated swimming pool. The swimming pool was supplied with water from the municipal drinking water supply and purified by a continuous filtration and purification system. Nasal swabs were taken from both nares of these individuals 1-day before the conduct of the and at the end of the day's swimming activities daily for 15 days. Group III comprised of divers, who undertook dry dives in a hyperbaric chamber. During the test conditions of the study, they were placed five men at a time in a chamber and pressurized to a depth of 20 m using compressed air. They spent 40 min at this pressure and were subsequently decompressed over 45 min. Thus, each individual spent 85 min in the chamber under hyperbaric conditions every day for 15 days. The breathing mixture used was compressed air and the temperature and humidity within the chamber were maintained at 27°C and 60%, respectively. Nasal swabs were taken from both nares of all the individuals 1-day before the conduct of the study and on days 1–15 during the course of study (at the end of each day's diving activities). Group IV dived in fresh water to a depth of 20 m where they spent 40 min. Dives were performed twice a day. All divers used SCUBA sets using compressed air as breathing mixture. The SCUBA sets used were earmarked for specific divers during the study, and the face and nose masks were thoroughly cleaned after use daily. Nasal swabs were taken as for Groups II and III. All personnel were examined daily. The specimens were collected using cotton-tipped nasal swabs soaked in sterile normal saline. In all cases, the anterior nares were swabbed, and the swabs placed immediately in air-tight sterile test tubes. The swabs were then placed on two separate culture plates of Blood Agar and MacConkey's media. The culture plates were then incubated in the laboratory at 37°C for 24 h. At the end of this period, the plates were examined for evidence of bacterial growth and the colony characteristics were noted. Slides were then prepared from samples of the bacterial colonies and stained with Gram's-stain and examined microscopically. Water samples were collected from the swimming pool and the diving site on days 1, 5, 10, and 15 and analyzed for bacterial flora.


  Results Top


It is seen from [Table 1] that the bacteria isolated from Group I consisted of Gram-positive organism with Staphylococcus epidermidis being predominant among them (70%). There was no significant change in the bacterial flora during the period of study. Of the total specimens taken from the control group during the study, 62 showed no growth on culture. However, the bacteria isolated in this group were all known commensals except for Staphylococcus aureus isolated from one participant. No one from this group developed Rhinitis during the period of the study.
Table 1: Bacteria isolated from the anterior nares of non-swimmers (Group I)

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Gram-positive organisms again dominated (with S. epidermidis being predominant) in the bacteria isolated from all the test groups [Table 2], [Table 3], [Table 4]. It was further observed that the colony counts of the Gram-positive organisms increased in the Divers' groups. More important Gram-negative organisms were identified during the course of the study with the first specimens appearing on the 4th day (in Groups III and IV). The main Gram-negative bacteria isolated were H. influenzae and Proteus. None of the participants in these groups (except for four in the swimmers group who had mild rhinitis) developed any significant otorhinolaryngological problems during the study. The swimming pool water samples revealed bacterial colony counts within the permissible limits and with no coliforms being isolated on all occasions. The main bacteria isolated were S. epidermidis and Micrococcus with few Gram-negative bacteria detected in couple of samples. The water samples from the diving site showed mainly Actinobacteria and Cyanobacteria with few Gram-negative bacteria isolated from some of the samples.
Table 2: Bacteria isolated from the nose of swimmers (Group II)

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Table 3: Bacteria isolated from the nose of divers (dry) (Group III)

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Table 4: Bacteria isolated from the nose of divers (wet) (Group IV)

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  Discussion Top


In the human upper respiratory tract, bacterial colonization is a dynamic process, in which bacteria are acquired, eliminated, and reacquired many times during a human life and can be influenced by various factors such as host age, immune status, exposure to antibiotics, smoking, and overcrowded living condition.[3],[4],[5]

In this study, the effort has been made to subject individuals from the study groups to environment similar to the operational environment, in which most divers work in the Navy.

Gweltany and Hayden [6] and Linton et al.[7] stated that bacterial microbiota of nasal passages differs in several respects from that of the nasopharynx. As determined by direct plating swabs it is less copious. Moreover, Gram-positive bacteria including Corynebacterium bacilli and staphylococci – both S. epidermidis and S. aureus are far more frequent in the nose than nasopharynx, whereas alpha hemolytic and nonhemolytic Streptococci and Gram-negative bacteria are far less frequent.

In our study, it was observed that Gram-positive bacteria were the dominant flora isolated from the anterior nares in both the nonswimmers and the test Groups (swimmers and divers) [Figure 1]. However, Gram-negative bacteria were isolated in all the three test Groups after few days of exposure to the changed test environment. Among the Gram-positive bacteria, S. epidermidis was predominant. The other Gram-positive bacteria grown were S. aureus, Micrococcus, Streptococci, and Corynebacterium. The Gram-negative bacteria isolated in the three test groups were mainly H. influenzae and Proteus. Further, there was no significant difference in the number of participants among the various test groups from whose nasal swabs anaerobes were isolated, though no anaerobes were isolated from the Diver groups after few days into the study.
Figure 1: Profile of nasal bacteria detected in the various groups of participants

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Among the group of swimmers who were exposed to swimming pool water daily day for 15 days period of study, four participants developed mild rhinitis. Men of this group were exposed to repeated water entry which leads to tissue maceration and infection. Divers are also subjected to the exposure to water like swimmers, but the direct contact of water with the nose will generally be of the limited period as for the duration that they are underwater mouth and nose breathing masks are used.

In group of Divers subject to high pressure along with controlled humidity and temperature (Group III), due to increased pressure, alteration of humidity and temperature, there is probably interference of ciliary activity producing altered pattern of bacterial flora of nose. Group IV, which consisted of divers subjected to wet diving, also showed increased colony count of Gram-positive bacteria though less than Group III (subjected to dry diving). Further, S. aureus was isolated in more specimens in the Swimmer and Diver groups as compared to the Control group. The alteration of nasal bacterial flora in the case of Dry Diving' vis-à-vis 'Wet Diving' is influenced by the period of exposure to hyperbaric environment along with the altered humidity. Rhinitis occurring in all three groups was of minor severity with no significant increase in severity in participants exposed to hyperbaric environment.

Hallman [8] and McFarlan [9] demonstrated high S. aureus carrier rates in hospital patients and healthy adults, respectively, and it became clear that potent pathogenic staphylococci are part of normal microbiota of anterior nares. As per the previous studies on bacteriology of nose, it was found that normal flora consisted mainly of S. epidermidis, Corynebacterium, S. aureus, and anaerobes. In this study, Gram-positive organism again predominated in the nasal bacterial flora of swimmers and divers (both dry and wet) with some Gram-negative bacteria found in the Swimmers and Divers [Figure 2].
Figure 2: Relative preponderance of the common bacterial flora isolated in the study participants

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Applying the Chi-square test (Epi Info ) with 95% confidence levels, the significance with the odds and risks ratios for the common bacterial flora isolated were calculated. For S. epidermidis growth, comparison between swimmers (including divers) and nonswimmers showed odds ratio of 15.78, risk ratio of 3.58, and P < 0.05 (0.00001) which is significant. For S. aureus growth, comparison between swimmers (including Divers) and nonswimmers showed odds ratio of 3.5, risk ratio of 1.75, and P > 0.0 5 (0.11) which is not significant. For Micrococcus growth, comparison between swimmers (including Divers) and nonswimmers showed odds ratio of 1.49, risk ratio of 1.176, and P > 0.05 (0.27) which is not significant. For Streptococcus growth, comparison between swimmers (including Divers) and nonswimmers showed odds ratio of 13.5, risk ratio of 6, and P < 0.05 (0.005) which is significant. For Corynebacterium growth, comparison between swimmers (including Divers) and nonswimmers showed odds ratio of 12, risk ratio of 3.2, and P < 0.05 (0.0003) which is significant.

This study is important as there is no report available of there being any other related study involving these many numbers of divers undertaking diving activities over such a period. The sample size had to be limited as the diving community is quite restricted and availability of larger number of participants was not feasible. The other possible limitations in this study are the limited diving depth and the duration of diving, especially when one thinks of deep-sea saturation diving; the quality of the water, including whether fresh water or sea water, or polluted water where diving is undertaken may also affect the results. However, as per Jones and Davis,[10] there was no change in the species of the bacteria forming the normal flora of the anterior nares in any of the three divers observed in their study involving saturation diving. Further studies may also be undertaken to determine the viral and fungal nasal flora in divers and any alteration occurring due to diving.

Although knowledge is limited, a change of colonization pattern of potential pathogens in the upper respiratory tract may have an effect on both the development of disease and the spread of pathogens in an individual. Thus, the composition of the various nasal potential pathogens is crucial in understanding bacterial interactions and determining measures to prevent and control the spread of infections involving these pathogens.


  Conclusions Top


There is an increase in commensal nasal flora, with Gram-positive bacteria being predominant, and appearance of Gram-negative bacteria on successive days on exposure to swimming/diving (wet/dry). Most probable cause of altered flora in swimmers is direct contact with water causing tissue maceration and infection. Further alteration of nasal flora occurs on exposure to the hyperbaric and humid environment in the case of divers. Several predisposing factors working together have been observed to bring about the altered bacterial flora and associated infections – stress, humid and hyperbaric environment, interference with ciliary activity barotrauma causing microhemorrhage in nasal mucosa, and serous exudation increasing the susceptibility to bacterial colonization by compromising the mucociliary barrier in the nose.

Acknowledgements

School of Naval Medicine, INHS Asvini, Mumbai, Maharashtra. Department of Pathology and Microbiology, INHS Asvini, Mumbai, Maharashtra.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Straker E, Hill AB, Lovell R. Report on Public Health and Medical Subjects. Vol. 90. London: Min of Health, His Majesty's Stationary Office; 1939. p. 56-8.  Back to cited text no. 1
    
2.
Seidler RJ, Allen DA, Lockman H, Colwell RR, Joseph SW, Daily OP, et al. Isolation, enumeration, and characterization of aeromonas from polluted waters encountered in diving operations. Appl Environ Microbiol 1980;39:1010-8.  Back to cited text no. 2
    
3.
Marchisio P, Gironi S, Esposito S, Schito GC, Mannelli S, Principi N, et al. Seasonal variations in nasopharyngeal carriage of respiratory pathogens in healthy Italian children attending day-care centres or schools. J Med Microbiol 2001;50:1095-9.  Back to cited text no. 3
    
4.
García-Rodríguez JA, Fresnadillo Martínez MJ. Dynamics of nasopharyngeal colonization by potential respiratory pathogens. J Antimicrob Chemother 2002;50 Suppl S2:59-73.  Back to cited text no. 4
    
5.
Chen CJ, Huang YC, Su LH, Lin TY. Nasal carriage of Streptococcus pneumoniae in healthy children and adults in Northern Taiwan. Diagn Microbiol Infect Dis 2007;59:265-9.  Back to cited text no. 5
[PUBMED]    
6.
Gwaltney JM Jr., Hayden FG. The nose and infection. In: Proctor DF, Andersen I, editors. The Nose, Upper Airway Physiology and the Atmospheric Environment. 1st ed. Amsterdam: Elsevier Biomedical Press; 1982. p. 399-422.  Back to cited text no. 6
    
7.
Linton AH, Topley WWC, Wilson GS. Principles of Bacteriology, Virology and Immunology. 8th ed. London: Publishers Edward and Arnold; 1990. p. 311-6.  Back to cited text no. 7
    
8.
Hallman FA. Proceedings of the Society for Experimental Biology. Vol. 36. New York: Publishers Blackwell Scientific; 1937. p. 789.  Back to cited text no. 8
    
9.
McFarlan AM. Pathogenic staphylococci in the nose. Br Med J 1938;2:939-41.  Back to cited text no. 9
[PUBMED]    
10.
Jones DM, Davis P. Upper respiratory tract and aural flora of saturation divers. J Clin Pathol 1978;31:721-3.  Back to cited text no. 10
    


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