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  Table of Contents  
ORIGINAL ARTICLE
Year : 2014  |  Volume : 51  |  Issue : 2  |  Page : 184-188
 

Microbial colonization of Provox voice prosthesis in the Indian scenario


1 Department of Surgical Oncology, Head and Neck Services, Parel, Mumbai, India
2 Department of Microbiology, Tata Memorial Hospital, Parel, Mumbai, India

Date of Web Publication7-Aug-2014

Correspondence Address:
P V Pawar
Department of Surgical Oncology, Head and Neck Services, Parel, Mumbai
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0019-509X.138303

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 » Abstract 

Introduction: Tracheoesophageal speech using the voice prosthesis is considered to be the "gold standard" with success rates as high as 90%. Despite significant developments, majority eventually develop dysfunction due to microbial deterioration. We did a pilot study of 58 laryngectomy patients who developed prosthesis dysfunction. Materials and Methods: A total of 58 laryngectomy patients who had their dysfunctional prosthesis removed were included in this study. Dysfunctional prostheses were removed and examined. Esophageal and tracheal flanges were examined separately. After obtaining pure fungal and bacterial cultures, the yeast strains were identified. Bacteria were identified with the light microscope and gram staining. We analyzed prosthesis lifespan and probable factors affecting it. Results: Central leak was found in 43% cases while in 57% peri-prosthetic leakage was the most common reason for prosthesis replacement. Microbial analysis revealed a combination of yeast and bacteria in approximately 55% culture samples. Out of these, almost 90% had the presence of single yeast species with bacteria. Pure fungal culture was identified in rest of the 45% cultures while none detected pure bacterial forms. Candida tropicalis was the solitary yeast in 81% while Candida albicans was seen in 10% as the solitary yeast. Bacterial isolates revealed Klebsiella pneumonia in 19%, Escherichia coli in 8% while Staphylococcus aureus was grown in 1% cultures. The consumption of curd (P = 0.036, 95% confidence intervals [CI]: 2.292-64.285) to have a significant correlation of the mean prosthesis lifespan. Consumption of curd (P = 0.001, 95% CI: 0.564-2.008) and history of prior radiotherapy (P = 0.015, 95% CI: 0.104-0.909) had a significant bearing on the Provox prosthesis lifespan. Conclusions: Candida is the most common organism grown on voice prosthesis in Indian scenario. Consumption of curd and history of prior radiotherapy significantly affect Provox prosthesis lifespan.


Keywords: Dietary habits, Indian scenario, microbial colonization, postlaryngectomy, voice rehabilitation, voice prosthesis


How to cite this article:
Chaturvedi P, Syed S, Pawar P V, Kelkar R, Biswas S, Datta S, Nair D, Chaukar D, D'cruz A K. Microbial colonization of Provox voice prosthesis in the Indian scenario. Indian J Cancer 2014;51:184-8

How to cite this URL:
Chaturvedi P, Syed S, Pawar P V, Kelkar R, Biswas S, Datta S, Nair D, Chaukar D, D'cruz A K. Microbial colonization of Provox voice prosthesis in the Indian scenario. Indian J Cancer [serial online] 2014 [cited 2019 Aug 21];51:184-8. Available from: http://www.indianjcancer.com/text.asp?2014/51/2/184/138303



 » Introduction Top


Tracheoesophageal speech using the voice prosthesis is considered to be the "gold standard" with success rates as high as 90%. [1] Although, there have been significant developments in the design of the silicon indwelling voice prosthesis majority of them eventually develop dysfunction due to microbial deterioration. [2],[3],[4] This leads to a shortened lifespan of the prostheses causing frequent replacements and adds up to the financial burden and above all deteriorating the quality-of-life of patient. In the published literature the average lifespan of voice prosthesis is around 4-8 months. [4] This data predominantly includes studies, which have evaluated western population. It has been our general observation that Indian patients have a longer prosthesis lifespan, i.e. 30 months (range: 7-144 months) (article in press).

Microbial biofilm formation on voice prosthesis depends on a variety of factors both endogenous and exogenous, which lead to the development of biofilms having different compositions of bacteria and yeast [Table 1]. [5] In Indian population, a substantial proportion of the diet comprise of milk and dairy products (curd and butter milk). On the basis of this anecdotal evidence, we surmise that there exists a relation in the dietary habits and prosthesis lifetime. In this pilot study, 58 laryngectomy patients who developed prosthesis dysfunction and required replacements were evaluated with an aim to;

  • Analyze the microbial composition of the voice prosthesis
  • Study the factors affecting the Provox prosthesis lifespan.
Table 1: Factors suggested influencing prosthesis lifespan in laryngectomy patients

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 » Materials and Methods Top


Patients and patient-related factors

During a voice rehabilitation workshop all registered voice prosthetic replacements carried out at the head neck services in our tertiary cancer hospital were included in the study. A standardized voice prosthesis questionnaire capturing information related to the prosthesis replacement was developed [Table 2].
Table 2: Voice prosthesis related questionnaire

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Microbial composition evaluation

Laryngectomees using the Provox indwelling low pressure voice prosthesis (Atos medicals, Horby, Sweden) that required replacements due to complications had their prosthesis removed was divided into two equal halves, which were placed immediately in a Trypticose soy broth (enrichment medium). The prosthesis was kept in the enrichment medium for 24 h after which cultures were obtained from the tracheal and esophageal flange of the prosthesis by the method of swabbing. The samples were cultured on blood agar, MacConkeys agar, Saborauds dextrose agar (SDA) slants. Blood and MacConkey's agar plates were incubated at 37°C for 18 h and SDA slants were incubated at 30°C for 72 h. After obtaining pure fungal and bacterial cultures, the yeast strains were identified by growing them on Corn meal agar followed subsequently by a slide culture and carbohydrate fermentation/assimilation test, and the bacteria were identified with light microscope and gram staining.

Statistical analysis

Statistical analysis was carried out using the PASW version 19 (IBM corporation). Voice prosthesis lifespan was evaluated with respect to influencing variables. We used backward multiple linear regressions to identify the factors significantly affecting the prosthesis lifetime. The in situ prosthesis lifespan was used as a dependent variable while age, sex, comorbidities, dietary factors, gastroesophageal reflux, use of antacids, tumor related factors (site and grade of tumor), pre-operative treatment, surgery related factors (type of reconstruction, neck dissection, myotomy, and neurectomy), post-operative complications (pharyngocutaneous leak), and adjuvant radiotherapy/chemoradiotherapy were taken as independent variables. Pearson correlation test was used to evaluate the microbial compositions correlation between the tracheal and esophageal flanges. Furthermore, to provide more information we attempted to categorize the patient into two different categories based on the median prosthesis lifespan. A 5% significance level was used (P = 0.05).


 » Results Top


Patient demographics

A total of 58 laryngectomy patients who required prosthesis replacements were evaluated. The study group included 57 men (98%) and 1 woman (2%). The mean age of the population was 56 years (median age 55 years, range: 35-74 years). Comorbidities were seen in 32 (55%) patients. 6 (10%) received prior radiotherapy while only 1 (2%) received prior concomitant chemoradiation and were salvaged by total laryngectomy.

Tumor and surgery-related factors

The most common tumor site was the hypopharynx (48%), followed by the supraglottis (27%) and glottis (25%). The primary tumors were classified as T1 in 2% of the cases as T2 in 4%, T3 in 10% and T4 in 86% of the cases. 36 patients (62%) had nodal metastasis. All the patients were loco regionally controlled at the time of evaluation.

Upfront total laryngectomy was performed in 51 (88%) while a salvage surgery in seven cases (12%). In all patients, neck dissection was performed (41 Bilateral [B/L] Level II-IV, 17 B/L Modified Radical Neck Dissection. Primary tracheoesophageal puncture and 8 mm Provox 1 voice prosthesis insertion was carried out in all patients as a primary procedure. Cricopharyngeal myotomy was carried out in 47 (81%) patients while neurectomy was carried out in 7 (12%) patients. Primary closure of the remnant pharyngeal mucosa was carried out in 53 (91%) patients while 5 (9%) patients required reconstruction (four Pectoralis major myocutaneous flap, one free radial artery forearm flap. Post-operative pharyngocutaneous leak was seen in 9 (15%) patients (2 major, 7 minor).

Adjuvant treatment

Among the 58 patients, 36 (62%) received concomitant chemoradiotherapy while 15 (26%) received adjuvant radiotherapy.

Lifespan of voice prostheses and reasons for replacement

In patient population, the mean prosthesis lifespan was 18 months (median 9 months, range: 1-87 months). Of the 58 voice prosthetic replacements carried out in the patient population, in 25 (43%) patients the reason was central leak (leakage through the prosthesis) while in 33 (57%) patient's peri-prosthetic leakage (leakage around the prosthesis) was the most common reason.

Microbial composition of the biofilms

Microbial analysis revealed a combination of yeast and bacteria in approximately 55% culture samples. Out of these, almost 90% had the presence of single yeast species with bacteria. Pure fungal culture was identified in rest of the 45% cultures while none detected pure bacterial forms [Table 3]a yeast isolates from the culture revealed, Candida tropicalis as the solitary yeast in 81% while Candida albicans was seen in 10% as the solitary yeast. Nearly, 9% of the fungal cultures had more than one species of yeast [Table 3]b. Bacterial isolates revealed Klebsiella pneumonia. In 19%, Escherichia coli in 8% while Staphylococcus aureus was grown in 1% cultures [Table 3]c. 45% of the cultures isolated did not have bacteria as the component. There was a significant correlation (P = 0.001) between the microbial colonization between the tracheal and the esophageal ends. Although, no significant correlation (P = 0.342) was seen between reason for prosthesis change and microbial colonization.
Table 3:

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Influence of various factors on prosthesis lifespan

By using backward multiple linear regressions in order to identify the various factors influential on the lifespan of Provox voice prostheses. We found the consumption of curd (P = 0.036, 95% confidence intervals [CI] 2.292-64.285) to have a significant correlation of the mean prosthesis lifespan [Table 4]. Whereas, after categorizing the patients based on the median prosthesis lifespan (9 months) both factors, i.e. consumption of curd (P = 0.001, 95% CI: 0.564-2.008) and history of prior radiotherapy (P = 0.015, 95% CI: 0.104-0.909) had a significant bearing on the Provox prosthesis lifespan [Table 4]. On the other hand, none of the variables (age, sex, comorbidities, dietary factors, tumor related factors [site and grade of tumor], surgery related factors [type of reconstruction, neck dissection, myotomy and neurectomy], post-operative complications [pharyngocutaneous leak], and adjuvant radiotherapy/chemoradiotherapy) showed a significant correlation with the mean lifetime of Provox prostheses [Table 4].
Table 4: Provox prosthesis lifespan as determined by various authors

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 » Discussion Top


Post laryngectomy voice rehabilitation using the voice prosthesis is considered the "gold standard" with a success rate as high as 90%. [1] Although, we continue our efforts in providing our patients with a device, which last for longer duration majority of patients develop device dysfunction and require a change within 6-8 months. [2],[3],[4] Biofilm development has been considered the most important reason for silicon degradation and prosthesis related dysfunction. The prosthesis is colonized by the microorganisms (bacteria + yeast strains) from the 1 st min it's placed in the trachesoesophageal puncture. The presence of tracheostoma and neopharyngeal environment provides an ideal situation for the organisms to adhere and flourish on the prosthesis. There have been multiple efforts to study this microbial flora, which has led to the development of newer devices, which promise an extended prosthesis lifespan, but these devices are costly and hence do not have a widespread use. [3],[4],[5],[6],[7] There still is a need to embark on methods, which are cost-effective and easy to incorporate in the patient's daily life-style. It has been our general observation that our laryngectomy population have a longer prosthesis lifespan 30 months (range: 7-144 months) (article in press). We investigated our patient population dietary habits with an aim to determine the factors, which lead to a longer prosthesis lifespan.

In our pilot study of 58 explanted voice prosthesis form patients requiring prosthesis change, the microorganisms isolated were both bacteria and yeast, but the latter predominated the mixed cultures with pure fungal isolates present in 47% cultures. C. tropicalis was the most common fungi isolated followed by C. albicans. This finding contradicts the previous studies, which showed a predominance of C. albicans in the majority of fungal isolates. [2],[3],[4],[5],[6] C. tropicalis is a commensal of the upper aero digestive tract and the predominance of this organism suggests a role of altered microbial flora due to dietary or immunosuppression caused due to radiotherapy. The presence of single yeast isolates from the dysfunctional prosthesis proves the phenomenon of silicon degradation caused by these organisms. In contrary, we were not able to isolate single bacterial cultures from the dysfunctional prosthesis and the bacteria isolated were found to be associated with fungi in these prosthesis. This is contradictory to the work of Palmer et al. who suggested an independent role of bacteria in silicon degradation. [8] Palmer et al. found 50% of failed prosthesis within first 60 days of implantation had S. aureus cultured from the esophageal flanges along with the shaft and tracheal side of the prostheses. [8] Whereas, in the present study, it was K. pneumonia was the predominant bacterium found in combination with the fungi while S. aureus was isolated in only 1% isolates. Staphylococci have been known to adhere to the silicon surface causing its degradation. [8] We were able to isolate Pseudomonas aeruginosa in 7% of the culture isolates. Pseudomonas is known to form biofilms, but whether it can degrade the silicon rubber is still a concept under evaluation.

There was a significant correlation between the tracheal and the esophageal microbial colonization. This we implicate to the frequent use of Provox brush for cleaning the prosthesis lumen, which leads to the soiling of the tracheal side of prosthesis. This can provide us with a rather easy method of microbial specimen collection for future studies using the Provox brush itself. Biofilm is composed of a microenvironment formed by the organisms and extracellular polymeric substance matrix in a specific architecture. This scenario provides an optimal environment for growth and exchange of nutrition and genetic material between the different organisms. [9] Due to logistic reasons we did not employ the electron microscope for better understanding the biofilm architecture; but, suggest its use for future studies for better understanding the biofilm microarchitecture.

In this study, we statistically analyzed the effect of a wide variety of factors both endogenous and exogenous on the lifespan of Provox prosthesis. Regular consumption of curd and radiotherapy were the only factors found to have a significant bearing on the prosthesis lifespan. In the Indian subcontinent consumption of dairy products in the form of Buttermilk, yoghurt is widely prevalent. There is some anecdotal evidence that consumption of yoghurt and butter1milk effectively reduces biofilm formation on indwelling prostheses, possibly due to the presence of Streptococcus thermophilus and Lactobacillus in the yoghurt. [10],[11],[12] Buttermilk is rich in lactoferrin, which has bactericidal and fungicidal activities against a number of oral pathogenic organisms such as C. albicans, Actinobacillus actinomycetemcomitans, and Streptococcus mutans. [13],[14],[15],[16] Majority of the studies evaluating the role of dairy products and probiotics in prolonging prosthesis lifespan had a common finding of reduction in the growth of C. albicans. [13],[14],[15],[16] C. albicans has been proven to produce enzymes, which can degrade the silicon biomaterial and cause prosthesis dysfunction. [9],[10],[11] Although, our population had a poor microbial yield of C. albicans as compared to C. tropicalis we suggest C. tropicalis to be less toxic in causing silicon degradation. Does C. tropicalis produce a biofilm, which is less toxic to the silicon material than the one produced by C. albicans? This concept needs to be studied further.

Radiotherapy is a known factor to known to affect the oral and esophageal microflora. Post radiotherapy decreased salivary secretion, which reduces the histatin level in the oral cavity and diminishes the antifungal activity of the saliva. [17] We found a prolonged prosthesis lifespan in patients who received radiotherapy as compared with chemoradiotherapy (21 months vs. 17 months) although not statistically significant. The predominance of non-albicans species (C. tropicalis, Candida glabrata, Candida krusei), which also are commensal of the upper aero-digestive tract mucosal lining suggests the role of immunosuppression in patients who have received adjuvant chemoradiation. [18] In the era of organ preservation protocols, there is a rising need for salvage laryngectomy and hence the authors propose further studies in this context.

In summary, this study adds to the literature the Indian perspective of microbial colonization on Provox voice prosthesis and provides useful insights to the likely reasons for prolonged prosthesis lifespan [Table 4]. The regular consumption of curd is likely to provide a longer prosthesis lifespan and prevent frequent prosthesis replacements. This method is extremely cost effective, efficacious, and easy to incorporate in regular life-style of the patient.

 
 » References Top

1.Stafford FW. Current indications and complications of tracheoesophageal puncture for voice restoration after laryngectomy. Curr Opin Otolaryngol Head Neck Surg 2003;11:89-95.  Back to cited text no. 1
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2.Mahieu HF, van Saene JJ, den Besten J, van Saene HK. Oropharynx decontamination preventing Candida vegetation on voice prostheses. Arch Otolaryngol Head Neck Surg 1986;112:1090-2.  Back to cited text no. 2
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3.Mahieu HF, van Saene HK, Rosingh HJ, Schutte HK. Candida vegetations on silicone voice prostheses. Arch Otolaryngol Head Neck Surg 1986;112:321-5.  Back to cited text no. 3
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4.Izdebski K, Ross JC, Lee S. Fungal colonization of tracheoesophageal voice prosthesis. Laryngoscope 1987;97:594-7.  Back to cited text no. 4
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5.Elving GJ, van der Mei HC, Busscher HJ, van Weissenbruch R, Albers FW. Comparison of the microbial composition of voice prosthesis biofilms from patients requiring frequent versus infrequent replacement. Ann Otol Rhinol Laryngol 2002;111:200-3.  Back to cited text no. 5
    
6.Buijssen KJ, Harmsen HJ, van der Mei HC, Busscher HJ, van der Laan BF. Lactobacilli: Important in biofilm formation on voice prostheses. Otolaryngol Head Neck Surg 2007;137:505-7.  Back to cited text no. 6
    
7.Soolsma J, van den Brekel MW, Ackerstaff AH, Balm AJ, Tan B, Hilgers FJ. Long-term results of Provox ActiValve, solving the problem of frequent candida - and "underpressure"- related voice prosthesis replacements. Laryngoscope 2008;118:252-7.  Back to cited text no. 7
    
8.Palmer MD, Johnson AP, Elliott TS. Microbial colonization of Blom-Singer prostheses in postlaryngectomy patients. Laryngoscope 1993;103:910-4.  Back to cited text no. 8
    
9.Free RH, Busscher HJ, Elving GJ, van der Mei HC, van Weissenbruch R, Albers FW. Biofilm formation on voice prostheses: In vitro influence of probiotics. Ann Otol Rhinol Laryngol 2001;110:946-51.  Back to cited text no. 9
    
10.Havenaar R, Huis in ′t Veld JH. Probiotics: A general view. In: Wood BJ, editor. The Lactic Acid Bacteria in Health and Disease. London: Elsevier; 1992. p. 151-70.  Back to cited text no. 10
    
11.Busscher HJ, van Hoogmoed CG, Geertsema-Doornbusch GI, van der Kuijl-Booij M, van der Mei HC. Streptococcus thermophilus and its biosurfactants inhibit adhesion by Candida spp. on silicone rubber. Appl Environ Microbiol 1997;63:3810-7.  Back to cited text no. 11
    
12.Sanders ME. Lactic acid bacteria and human health. In: Fuller R, Heidt PJ, Rusch V, Van der Waaij D, editors. Probiotics: Prospects of Use in Opportunistic Infections. Germany: Institute for Microbiology and Biochemistry, Herborn-Dill; 1995. p. 126-40.  Back to cited text no. 12
    
13.Johanson B. Isolation of an iron-containing red protein from human milk. Acta Chem Scand 1960;14:510-4.  Back to cited text no. 13
    
14.Kalmar JR, Arnold RR. Killing of Actinobacillus actinomycetemcomitans by human lactoferrin. Infect Immun 1988;56:2552-7.  Back to cited text no. 14
    
15.Soukka T, Lumikari M, Tenovuo J. Combined inhibitory effect of lactoferrin and lactoperoxidase system on the viability of Streptococcus mutans, serotype c. Scand J Dent Res 1991;99:390-6.  Back to cited text no. 15
    
16.Soukka T, Tenovuo J, Lenander-Lumikari M. Fungicidal effect of human lactoferrin against Candida albicans. FEMS Microbiol Lett 1992;69:223-8.  Back to cited text no. 16
    
17.Tsai H, Bobek LA. Human salivary histatins: Promising anti-fungal therapeutic agents. Crit Rev Oral Biol Med 1998;9:480-97.  Back to cited text no. 17
    
18.Capoor MR, Nair D, Deb M, Verma PK, Srivastava L, Aggarwal P. Emergence of non-albicans Candida species and antifungal resistance in a tertiary care hospital. Jpn J Infect Dis 2005;58:344-8.  Back to cited text no. 18
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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