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 ~ Subjects and Methods
 ~ Results
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  Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 38  |  Issue : 3  |  Page : 299-306
 

A systematic review and meta-analysis of different diagnostic procedures to detect gonococcus infection in resource-limited scenario


1 Department of Biotechnology, Amity University, Kolkata, West Bengal, India
2 Regional STI Laboratory, Institute of Serology, Kolkata, West Bengal, India
3 Department of Health Promotion and Education, All India Institute of Hygiene and Public Health, Kolkata, West Bengal, India

Date of Submission07-Jul-2020
Date of Decision04-Aug-2020
Date of Acceptance17-Sep-2020
Date of Web Publication4-Nov-2020

Correspondence Address:
Dr. Nibedita Das
Institute of Serology, 3 Kyd Street, Kolkata - 700 016, West Bengal
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijmm.IJMM_20_312

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 ~ Abstract 


Context: Neisseria gonorrhoeae is a Gram-negative diplococcus, an obligate human pathogen, and the etiologic agent of the sexually transmitted infection (STI), gonorrhoea. culture is the standard procedure for diagnosis, which may be supported by nucleic acid tests and microscopy. Aims: To determine the best possible method of diagnosis for Gonococcus infection in resource-limited settings. Settings and Design: The meta-analyses were designed to determine the difference in diagnosis between Culture and nucleic acid amplification tests (NAATs) and also between the different Amplification Tests and widely available Roche COBAS AMPLICOR test. Subjects and Methods: Databases searched were Pubmed, Medline, Google Scholar and Cochrane reviews. Risk ratio (RR) with 95% confidence intervals was estimated for the dichotomous outcomes. The random-effect model was applied for all the studies in the analysis. Statistical Analysis Used: The meta-analysis was computed in RevMan Version 5.3, Copenhagen, Denmark. Results: In the first analysis, NAATs significantly improved the chances of detection in comparison to the standard culture and final RR was 1.24 (1.05–2.51), which put the diamond on the right of no-effect axis, indicating more positives by NAATs. In the second analysis, AMPLICOR had the more positive results, which may have indicated better detection rate, as well as less specificity and final RR was 0.809 (0.737–0.888), which put the diamond on the left of the non-effect axis, indicating more positives by AMPLICOR. Conclusions: In a resource-limited scenario like India, the syndromic management of STIs are considered to be the norm. A positive diagnosis is only given if the tests are confirmed by Culture, as it is still considered to be the gold standard of diagnosis. However, in many cases, due to suboptimal transportation and lack of proper handling, culture in unable to grow even if the patient is infected. In such cases, Nucleic Acid Tests should be able to detect an infection.


Keywords: Diagnostic procedures, meta-analysis, Neisseria gonorrhoeae


How to cite this article:
Mallik A, Das N, Mukherjee S, Datta S. A systematic review and meta-analysis of different diagnostic procedures to detect gonococcus infection in resource-limited scenario. Indian J Med Microbiol 2020;38:299-306

How to cite this URL:
Mallik A, Das N, Mukherjee S, Datta S. A systematic review and meta-analysis of different diagnostic procedures to detect gonococcus infection in resource-limited scenario. Indian J Med Microbiol [serial online] 2020 [cited 2020 Nov 24];38:299-306. Available from: https://www.ijmm.org/text.asp?2020/38/3/299/299832





 ~ Introduction Top


Neisseria gonorrhoeae is a Gram-negative diplococcus, an obligate human pathogen, and the etiologic agent of the sexually transmitted infection (STI), gonorrhoea.[1] Humans are the only natural host of this organism and infections caused by it are usually localised to the mucosal surfaces, where the host is initially exposed to the organism (e.g., Urethra of males causing acute urethritis and chronic urethritis leading to strictures, urethra and cervix uteri of females, anorectal area and conjunctiva.).[2] It is generally a non-complicated mucosal infection with a purulent discharge. More severe sequellae include salpingitis and pelvic inflammatory disease, which may lead to sterility/ectopic pregnancy.[1]

Gonorrhoea is a global infection. The WHO estimates that 106 million cases occur annually with approximately two-thirds of these cases reported from developing countries.[3]

An estimated 3 crore episodes of STI/reproductive tract infection occur every year in the country.[4]

In a study conducted from 2015 to 2017 in the Department of Microbiology, Jawaharlal Nehru (J. N.) Medical College, Aligarh, N. gonorrhoeae was detected in 7.19% cases.[5] According to the NMJI, Review Article (2004) in India, the prevalence of gonorrhoea among STI clinic attendees in different regions varied from 3% to 19%. A steady decline in the prevalence was observed in Chandigarh, Delhi and Patiala, while a marginal increase was reported from Rohtak and Ahmedabad.[6]

The principle strategy for the control of gonorrhoea involves the diagnosis and treatment of symptomatic cases together with contact tracing and treatment of sexual partners.[7] Currently, tools of gonorrhoea diagnosis include microscopy, culture and various non-culture tests.[8]

However, the high proportion of asymptomatic infections (10% in men and 50%–80% in women), absence of sensitive and specific tests suitable for mass screening, along with requirements of invasive samples for tests and social stigma attached, the disease goes under-diagnosed and under-reported.[9],[10] Moreover, delay in the availability of results causes the patients to not return to collect their results.[7],[9] Syndromic Management introduced by the WHO, although satisfactory in symptomatic men lacks both sensitivity (30%–80%) and specificity (40%–80%) for women with vaginal discharge[11],[12],[13] and misses asymptomatic patients.[14],[15]

While Culture is considered the Gold Standard of diagnosis of Gonorrhoea, it is by no means a perfect method. Each method consists of their own pros and cons, different sensitivity and specificity, as well as different limitations.

The aim of this Review Article is to compare different methods of diagnosis of N. gonorrhoeae that are currently available or being developed to determine the most suitable method of detection in a resource-limited setting and analysing each method to determine its practicality in the same.

Aims and objective

  1. To analyse the diagnostic procedures for Gonococcus infection
  2. To determine the best possible method of diagnosis in resource-limited settings scenario.



 ~ Subjects and Methods Top


Search strategy

Studies were identified using electronic databases such as PubMed, Medline, Google Scholar and Cochrane databases throughout May–June, 2019. As the diagnostic procedures in consideration were Microscopy, Culture, Serological Tests, Nucleic Acid Tests. The studies pertaining to these subjects were reviewed. The search process was carried out by the following combination of terms:

  • Gonococcal diagnosis OR gonorrhoea diagnosis
  • Gonococcus AND diagnosis
  • N. gonorrhoeae AND diagnosis.


Inclusion criteria

Studies targeted towards a variety of methods of Gonococcus diagnosis available in different settings and scenarios were included. No discrimination was made in terms of geographical distribution or population. In the absence of more recent studies regarding the diagnostic systems of Gonococcus infection, older studies were also included. Studies and review articles alike were included and more studies were obtained by following the references of each paper.

Exclusion criteria

Studies that were incomplete or studies for which full papers could not be obtained were excluded from this review. Studies that focused on Antimicrobial resistance of Gonococcus and treatment procedures were excluded.

Variable determination for each diagnostic procedure

Data was obtained from the selected papers, which included information on the following variables:

  1. Different types of diagnostic methods to detect Gonococcus infection
  2. Sensitivity and specificity of each method
  3. Time and resources required for each method
  4. The practicality of each method
  5. Limitations of each method.


Data extraction

All four authors searched the databases independently. The studies fulfilling the inclusion criteria were again reviewed by all the authors. Data were collected based on the above variables along with information on the author and year of publication of the included studies and reviews. Information under each variable was written and tabulated separately.

Methodology for the meta-analysis

Two separate meta-analysis was conducted for the following purposes.

  1. Nucleic acid amplification tests (NAATs) versus Culture method for the diagnosis of N. gonorrhoeae. Since culture is currently the most widely accepted method for the diagnosis of Gonococcus, it was considered to be the 'standard' in the said meta-analysis while NAAT is the method used for comparison
  2. Comparison of different types of NAATs for the diagnosis of N. gonorrhoeae. AMPLICOR system is the most widely used NAAT; hence it was preferably considered to be the standard, in the absence of which In-house PCR is considered to be the standard.


Search strategy

Author AM computed the meta-analysis, which was reviewed by all the authors. At first, papers studied for the review were re-evaluated for their significance in each of the above analysis. The papers with significantly clear data and relevance were considered for the meta-analysis.

Inclusion criteria

For (A) any study comprising a comparison between the conventional culture method and NAAT were included. No discrimination was made in regards to the type of nucleic acid tests, as long as they were amplifying in nature. Studies that included this comparison as a part of larger data were also included, as long as the required values could be worked out easily from the given data.

For (B) any study comprising of multiple NAATs were included. Multiple comparisons were collected from the same study if required. Studies that included these comparisons as a part of larger data were also included.

In both cases, older studies (until 1999) were included.

No other discriminations were made in terms of procedures as long as the required methods were said to be followed.

Exclusion criteria

Studies that contain obscure or complex data were excluded to promote the simplicity of the analysis. Studies for which full papers and data could not be obtained were excluded.

For (A), studies that had extremely low positive values for Culture method were excluded-for example, studies by Sood et al.[16] and Budkaew et al.[17] were excluded.

For (B), no studies were excluded for low positive values. However, studies describing Nucleic Acid Methods without Amplification were excluded. Studies that did not contain data for AMPLICOR were excluded.

Statistical analysis

The random-effects model was applied for all studies in the analysis. The Forest Plot was prepared in software RevMan Version 5.3 Copenhagen, Denmark for A and B separately with risk ratio as the Effect Size for continuous data presented with 95% Confidence Interval (CI).


 ~ Results Top


From the variety of studies that were reviewed, the average sensitivity and specificity of each diagnostic method were determined as follows:

Microscopy

The sensitivity and specificity for Gram-stain for symptomatic males (i.e., males with urethritis) are as high as 95% and 99%. For asymptomatic males, sensitivity is 40%–60%, while for women, sensitivity drops to 37%–70%.[18],[19]

Assuming the specificity of microscopy for symptomatic males being 99%,[8] the ranges of sensitivity for each patient are represented via a bar chart in [Figure 1].
Figure 1: Graphical representation of sensitivity of different types of patients in microscopy method

Click here to view


Culture

Diagnosis of Gonococcal infection by culture on selective media has a sensitivity of 85% to 95% for acute infection and around 50% for asymptomatic cases.[20],[21]

Considering the specificity of culture to be 100% under optimal conditions,[18],[22] the sensitivities are represented by a bar chart in [Figure 2].
Figure 2: Graphical representation of varying sensitivities of different types of patients in Culture

Click here to view


Nucleic acid tests (with or without amplification)

Different types of Nucleic Acid Tests have varying levels of accuracy in terms of sensitivity and specificity. The observed accuracy in specific sample size is tabulated[23] and plotted on a scatter diagram below.

Meta analysis

Culture versus nucleic acid amplification tests as a tool for gonococcus diagnosis

A total of nine studies met the inclusion criteria and were included in the analysis.

The total number of patients tested for gonococcus was 26572 for culture and 35368 for NAAT. The studies ranged from 2000 to 2015.

The sample size for each study varied from 216 to 27585.

The forest plot [Figure 3] is prepared according to [Table 1].
Figure 3: Forest plot depicting nucleic acid amplification tests versus culture (left-favours culture; right-favours nucleic acid amplification tests). Represented at 95% confidence interval

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Table 1: Information of studies included in nucleic acid amplification test versus culture meta-analysis

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Different types of nucleic acid amplification tests as tools for diagnosis of gonococcus

A total of four studies met with the inclusion criteria and were included in the current analysis. The total number of patients tested was 2015. AMPLICOR was considered to be the standard. Sample Size varied from 172 to 1224. Each patient was tested by COBAS AMPLICOR and one or more other Amplification Tests. In the case of two studies by Tabrizi et al.[32] and Sachdev et al.[33] data were extracted twice because of more than one comparisons.

Forest Plot [Figure 4] is prepared according to [Table 2].
Figure 4: Forest plot depicting AMPLICOR versus other nucleic acid amplification tests (left-favours AMPLICOR; right-favours other nucleic acid amplification tests) represented at 95% confidence interval

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Table 2: Information on the studies included in intra-nucleic acid amplification test meta-analysis

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 ~ Discussion Top


From [Table 3] and [Figure 1], [Figure 2], 5, it was observed that NAATs had the highest amount of sensitivity in comparison to other diagnostic procedures. However, Culture was said to have more specificity in comparison to Nucleic Acid Tests. The culture method was highly effective in the case of symptomatic patients; however, this effectiveness decreased significantly in the case of asymptomatic patients. Microscopy was only really considered to be a full-proof test in the case of symptomatic male patients while testing urethral discharge.
Table 3: Sensitivity and specificity of different types of nucleic acid tests (amplifying and non-amplifying)

Click here to view


In the case of Nucleic Acid Tests, AMPLICOR was the most widely used test for its high sensitivity, but it was also prone to giving false positives due to somewhat low specificity. In a study conducted for understanding the rate of false-positive results in NAATs, it was found that COBAS AMPLICOR had a 14.1% false-positive rate.[39] STIs are associated with significant adverse social and internal stigma in the people of India and other developing countries. This can lead to lower quality of life, discrimination and reluctance to seek health care. For this reason, false-positive diagnosis can be detrimental to the well-being of the patient.[40] Hence, a supplementary NAAT has been recommended at all times to lower the instances of false-positives.[41]

In [Table 4], a comparative data of all the diagnostic procedures are provided according to the previously shown plots and this implies that while NAATs are the tests with highest accuracy, they required a larger start-up cost than the other two procedures, which is likely to be impractical when resources are limited.
Table 4: Comparison of the three methods

Click here to view


In Meta-analysis A, Culture was considered to be the standard which was compared against any NAAT throughout eleven studies [Table 1] and [Figure 3]. The final diamond was plotted on the right side of 'no effect' axis. As the resultant diamond shape does not touch the line of 'no effect', the difference between the two diagnostic approaches was statistically significant with the P < 0.05 at 95% CI. Thus, NAATs were seen to give more positive results than culture, thus having higher sensitivity. However, in some cases, they were also considered to give false positives. All in all, NAAT was shown to give a better outcome.

In meta-analysis B, i.e., the intra-NAAT analysis, AMPLICOR was considered to be the standard as it was most widely used [Table 2] and [Figure 4]. The diamond was plotted in the left side of the 'no effect' axis. Similar to Meta-analysis A, the diamond does not touch the 'no-effect' axis, thus indicating the difference between the standard and other diagnostic approaches to be statistically significant with the P < 0.05 at 95% CI. Thus, AMPLICOR was shown to give a higher positive value than other tests of NAATs. This shows higher sensitivity but low specificity. NAATs like 16s rRNA assay and BD ProbeTec were shown to have a higher specificity than AMPLICOR. So even though the AMPLICOR system shows a better outcome, their accuracy is still under debate. In addition to N. gonorrhoeae, the test also reacts with Neisseria subflava and Neisseria cinerea, leading to false-positives. Adding to this issue, the COBAS AMPLICOR system is only effective in the case of endocervical specimens, male urethral and urine specimens from symptomatic patients, which further limits its effectiveness.[47]


 ~ Conclusions Top


In a resource-limited scenario like ours, the syndromic management of STIs is considered to be the norm. A positive diagnosis is only given if the tests are confirmed by Culture, as it is still considered to be the gold standard of diagnosis. It has high specificity, high sensitivity in case of acute infections and sufficient sensitivity to detect 50% infections for asymptomatic patients. However, in many cases, due to suboptimal transportation and lack of proper handling, culture is unable to grow even if the patient is infected. In such cases, Nucleic Acid Tests should be able to detect an infection. However, due to high expenses setting up, potential false-positives and limitations of sample types, they are not considered to be feasible in district-level hospitals. In certain areas, inadequate staff expertise may also be an issue. This is the norm still followed by the NACO guidelines for the detection of STIs. However, the time has come to review the guidelines still practised by different laboratories undertaking testing of STI control program initiated by the Government of India. Thus in spite of certain setbacks, culture is considered to be the preferred and most cost-effective method of diagnosis. However, suboptimal transportation and fastidious property of the organism limits the effectiveness of culture. On the other hand, NAATs can detect minute traces of the genetic material of the organism, which enhances its ability to diagnose a patient even from a non-viable sample, unlike culture. Hence, it should be noted that if it is possible to provide a significant start-up cost, NAATs should be the best approach for the diagnosis of N. gonorrhoea infections.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]
 
 
    Tables

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



 

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2004 - Indian Journal of Medical Microbiology
Published by Wolters Kluwer - Medknow

Online since April 2001, new site since 1st August '04