|Year : 2020 | Volume
| Issue : 10 | Page : 5136-5141
Incidence and clinical features of viral sore throat among children in rural Haryana, India
Raghavan Parthasarathy1, Rakesh Kumar1, Giridara Gopal1, Ritvik Amarchand1, Shobha Broor2, Avinash Choudekar1, Debjani Ram Purakayastha3, Abhishek Wahi1, Venkatesh Vinayak Narayan1, Anand Krishnan1
1 Centre for Community Medicine, All India Institute of Medical Sciences, New Delhi, India
2 Centre for Chronic Diseases Control, Gurugram, Haryana, India
3 Translational Health Science and Technology Institute, Faridabad, Haryana, India
|Date of Submission||03-May-2020|
|Date of Decision||11-Jun-2020|
|Date of Acceptance||11-Jul-2020|
|Date of Web Publication||30-Oct-2020|
Dr. Anand Krishnan
Centre for Community Medicine, All India Institute of Medical Sciences, New Delhi
Source of Support: None, Conflict of Interest: None
Background: Sore throat is one of the commonest symptoms that patients present to a primary care physician. We describe the epidemiology of sore throat and performance of an algorithm to predict viral sore throat in a part of India. Methods: Children below 10 years of age were followed in 4 villages of Haryana, India from Aug 2012 to Aug 2014 through weekly domiciliary visits by trained field workers who screened for symptoms of acute respiratory infection (ARI) including sore throat. Nasal and throat swabs were obtained from a random sample of sore throat cases by nurses and sent in appropriate transport media for real-time polymerase chain reaction for detection of viral nucleic acid. Incidence of sore throat and viral sore throat are reported as number of sore throat episodes per 1000 child-years (EPTCY) with 95% confidence-interval (CI). Symptoms, associated with viral sore throat were identified by logistic regression, combined into a clinical score and Receiver Operating Characteristic curve was plotted. Results: Over a two-year period, 3765 children were followed up for 5578 child years. 1069 episodes of sore throat were reported, and swabs were collected from 8% of the cases randomly. The incidence of sore throat and viral sore throat was 191.7 (95%CI: 180.5-203.6) and 60.1 (95%CI: 55.1-68.2) EPTCY, respectively. Fever (aOR 5.40,95%CI: 1.16-25.18) and running nose (aOR 10.16,95%CI: 1.01-102.42) was significantly associated with viral sore throat. The clinical score (fever, running nose, and headache) had an overall sensitivity of 86.2% (68.3-96.1%), specificity of 62% (47.2-75.3%) and AUC of 0.78 (0.67-0.87) in predicting viral sore throat. Conclusion: Viruses contributed to one-third of burden of sore throat and clinical score can be used in primary care settings to aid antibiotic prescription by physicians.
Keywords: ARI, Children, viral sore throat
|How to cite this article:|
Parthasarathy R, Kumar R, Gopal G, Amarchand R, Broor S, Choudekar A, Purakayastha DR, Wahi A, Narayan VV, Krishnan A. Incidence and clinical features of viral sore throat among children in rural Haryana, India. J Family Med Prim Care 2020;9:5136-41
|How to cite this URL:|
Parthasarathy R, Kumar R, Gopal G, Amarchand R, Broor S, Choudekar A, Purakayastha DR, Wahi A, Narayan VV, Krishnan A. Incidence and clinical features of viral sore throat among children in rural Haryana, India. J Family Med Prim Care [serial online] 2020 [cited 2020 Nov 30];9:5136-41. Available from: https://www.jfmpc.com/text.asp?2020/9/10/5136/299392
| Introduction|| |
Sore throat among children is one of the most common health condition that primary health care physicians deal with. Viruses are reported to be the most common etiology for sore throat, common among them are Respiratory Syncytial Virus (RSV), Para-Influenza Virus- (PIV), Human Rhino Virus (HRV), Human Metapneumo virus (hMPV), and Influenza virus., Bacterial sore throats comprise of only 5–15% of sore throat cases, though antibiotic prescription is common in the cases of sore throat.
Since majority of the sore throats are viral in origin, unnecessary prescription of antibiotics to prevent the bacteriological complications could lead to side-effects, out-of-pocket expenditures, and development of antibiotic resistance in the micro-organisms. Over-prescription of antibiotics and development of antibiotic resistance in micro-organisms is an escalating problem in the country and programs have been formulated recently to curb its rise. The knowledge about the epidemiology of viral sore throat and symptom complex algorithm for prediction of viral sore throat would help in understanding the burden as well aid policy makers in making policy decisions. The main objective of the current study was to describe the epidemiology of viral sore throat among a cohort of children under 10 years of age in rural north India. Also, we evaluated the performance of a clinical score for predicting viral etiology based on symptoms which were significantly different between viral and non-viral sore throats.
| Methods|| |
This study was conducted in the platform established for community-based surveillance of Acute Respiratory Infections (ARI) among children in rural, Haryana. The characteristics of the cohort are published previously in another paper. Children aged <10 years were followed in 4 villages from Aug 2012 to Aug 2014 through weekly domiciliary visits. A written informed consent was obtained from the either parent of the children for children under 7 years of age and from both parents and children for children aged 7 or more years. Socio-economic status of all households in the study area were assessed based on the possession of various consumer items and based on wealth index used in the National Family Health Survey (NFHS). The Institutional Ethics Committee approved the study. Ethical approval was obtained from the institute's ethics committee (AIIMS, New Delhi) and is mentioned at the last as a separate section in Page no 6 (Approval no: IEC /NP- 27/2012 & RP-05/2012).
Trained field workers screened all enrolled children weekly for any of the five ARI symptoms (cough, sore throat, nasal congestion, earache/discharge, breathing difficulty). Anyone with throat pain or discomfort in the throat were considered to have sore throat. Detailed clinical history and examination was done for all identified cases. Child was deemed to have sore throat if the mother/care giver reported that the child have “pain in throat” or “difficulty in swallowing”. Nasal and throat swabs were obtained from a random sample of 10% of ARI cases and then sent in viral transport media to department of Microbiology for real-time polymerase chain reaction (RT-PCR). RT-PCR was performed for the detection of following viruses: influenza virus, rhinovirus, para-influenza viruses 1-3, human meta-pneumo virus, and respiratory syncytial virus.
Data analysis was done using STATA 13.0 (StataCorp, 2011). Incidence of sore throat was reported as number of sore throat episodes per 1000 child-years with the 95% confidence interval (CI) using normal approximation method for gender and various age groups. The incidence of viral sore throat in the cohort was estimated by applying the quarterly sample positivity rate (SPR) of viruses among the sore throat cases to the quarterly sore throat rates which were summed and then divided by the overall follow-up years to estimate the overall incidence of viral sore throat [Table 1]. Incidence of sore throat and viral sore throat was calculated within various wealth quintiles of the cohort and reported with 95%CI.
|Table 1: Incidence of sore throat and viral sore throat according to socio-demographic features|
Click here to view
The association of various associated signs and symptoms with viral sore throat were calculated as odds ratios (OR) and reported with 95% CI [Table 2]. In calculating the association, cases were viral sore throat (sore throat cases wherein a virus was isolated) and controls were non-viral sore throat cases (sore throat cases with no virus isolates on testing). Variables with P value of less than 0.4 in the bivariate analysis were fitted in the multivariable logistic regression model and their corresponding adjusted odds ratios (aOR) were calculated with 95%CI and the goodness of fit was reported using pseudo-R2.
|Table 2: Bivariate and multi-variable analysis for symptom association with viral sore throat|
Click here to view
The symptoms were combined to calculate their corresponding sensitivity and specificity. Each symptom was given a score depending on their aOR and the total score was summed. Receiver Operating Characteristic (ROC) curve was plotted for the proposed score for screening viral sore throat and its sensitivity, specificity and Area Under the Curve (AUC) was calculated with 95%CI.
| Results|| |
A total 3765 children were followed up for 2 years for an overall 5578 child years. The mean age of the study cohort was 4.07 years (SD - 1.51 years). The overall incidence of sore throat was 191.7 (95%CI: 180.5-203.6) episodes per 1000 child years. Specimen for virus testing were obtained from 79 (8%) episodes of sore throat out of the total 1069 episodes reported. A virus was isolated from 29 (36.7%) specimens. The estimated incidence of viral sore throat was 60.1 (95%CI: 55.1-68.2) episodes per 1000 child years. Viral nucleic acid was detected from specimens of one third (31.3%) of the incident sore throat cases. Among the specimens in which viruses were detected, 68.9% of the specimens were positive for one virus and 31.1% reported co-infection with other viruses. The various viruses detected were as follows; RSV (15.4%), HRV (53.8%), PIV (15.4%), hMPV (11.5%), and influenza (27.6%).
There was no significant difference in incidence of sore throat between boys (184.5 EPTCY; 95%CI: 169.9-200.3) and girls (180.6 EPTCY; 95%CI: 165.4-197.2); however, the incidence of viral sore throat was significantly higher among boys (92.4 EPTCY; 95%CI: 62,4-138.1) [Table 1]. There was an increase in the incidence of sore throat with age and was higher in children above 5 years of age (aOR-2.70, 95%CI: 2.20-3.33), in the contrary to viral sore throat, which decreased with age [Table 1]. Also, the incidence of viral sore throat was lesser in the wealthier quintiles.
Among the symptoms, after adjustment [Table 2], the following were significantly associated with viral sore throat: fever (aOR 5.40, 95%CI: 1.16-25.18) and running nose (aOR 10.16, 95%CI: 1.01-102.42).
The clinical score was designed by giving scores to the following variables approximating to their adjusted odds ratios as follows: headache, 3; fever, 5; running nose, 10. Combining the symptoms into a clinical score yielded an overall sensitivity of 86.2% (95%CI: 68.3-96.1%), specificity of 62% (95%CI: 47.2-75.3%), and AUC of 0.78 (95%CI: 0.67-0.87) for a cut-off of 13 [Table 2] and [Table 3].
| Discussion|| |
This is one of the first studies to report incidence of sore throat and viral sore throat in India. The study clearly demonstrates sore throat to be a significant problem among children in the community. The incidence of sore throat in the study was 191.7 (95%CI: 180.5-203.6) episodes per 1000 child years. The reported incidence was lower as compared to other studies reporting the incidence of URTI.,, URTI is a broad category of diseases, with sore throat as one of its components. Since burden of overall spectrum of URTI was not the primary objective in this study, the reported incidence would have been lower as compared to other studies reporting overall URTI. The incidence of sore throat among children was found to increase with age in the contrary to viral sore throat [Table 1]. Few studies, conducted worldwide have reported inverse relationship between age and incidence of sore throat among children, with higher rates in children less than five years. However, majority of these studies focused on children under five years of age, whereas in the current study, children upto the age of 10 years was included and thus could have resulted in the shift. Also, it is reported that bacterial pharyngitis is more common in children above 5 years age group, supporting the decreasing incidence of viral sore throat with age in the current study. The incidence of viral sore throat was higher among the poorer quintiles (1st, 2nd, and 3rd) in this study corroborating with other studies. This could have been due to poor housing conditions or over-crowding in the households. However, the study was not powered enough to study the association of socio-economic risk factors with viral sore throat.
The estimated incidence of viral sore throats in the current study was 60.1 (95%CI: 55.1-68.2) episodes per thousand child years [Table 1], which was one-third of the overall sore throat incidence estimated. There are very few community-based studies on epidemiology of viral sore throats. One study conducted among children visiting a family-medicine center in Turkey reported a slightly higher contribution of sore throats by viruses among the sore throat cases visiting the center. The age-groups included in the study were different, as the above-mentioned study included adults and was done in a hospital setting. Similar to the current study, other studies have reported viral etiology among one-third to half of the URTI cases.,, In this study, the most commonly found virus in the isolate was HRV. Globally, Rhinovirus is reported to be the most common causative organism for URTI.,,,, Also, many Indian studies have reported Rhinovirus to be most common etiology for URTI.,, Certain studies also reported influenza group of viruses to be the common etiology,[25.26] however, the above studies could not be compared with the current study, as the setting (community vs. hospital), demographic profile of participants (geography, age group, occupation etc.) and methodology were different. In the current study, influenza viruses were also found to be of significant concern, as they contributed a significant proportion. Similar to other studies, parainfluenza group of viruses and HMPV were also detected. Co-infection with other viruses have been reported in the study. In studies done globally, most of the co-infections were due to adenovirus as they continue to shed from the nasopharyngeal mucosa for a longer duration as compared to other viruses, thereby increasing their probability of concomitant infections. However, in the current study RSV was the commonly associated co-infection, as the swabs were not tested for adenovirus.
The following symptoms were found to be significantly associated with viral sore throat: running nose, fever, and headache. Though, very few studies have focused on the association of signs and symptoms with viral URI/sore throat, a large number of studies have studied the associations with specific viral infections, affecting the lower respiratory tract and bacterial sore throat. Sentinel surveillance of febrile respiratory illness patients who sought primary health care in Singapore reported that symptoms such as fever and running nose were more common among those diagnosed with viral as compared to bacterial infections. Also, a recent systematic review and meta-analysis reported significant association between influenza infection and fever or headache, as well as between RSV infection and cough. However, similar association of symptom complex with specific viruses could not be estimated in the current study as it was not the study objective.
Rational usage of antibiotics and explicit mentioning on optimal prescription antibiotics for conditions such as common cold and other non-specific upper respiratory tract infections are given by the national guidelines. However, studies indicate a higher proportion of antibiotic prescription for such infections, especially in the primary care settings (both public and private). In low-resource primary care settings, microbiological or rapid diagnosis for bacteriological and viral etiology of sore throat is not an economically feasible option. There are many clinical prediction models for diagnosing bacterial sore throat such as: McIsaac score and Centor score, etc., However, similar algorithms for prediction of viral sore throat is scarce. The current study validated a clinical algorithm with three-symptom complex predicting the probability of viral sore throat. In comparison, study by Mistik et al., included other symptoms in addition such as sneezing, stuffy nose and absence of tonsillar hypertrophy in the scoring for diagnosing viral sore throat. Also, Mistik et al., documented reduction in antibiotic prescription by combined usage of viral prediction scores along with bacterial prediction scores. However in our study, scores for bacterial sore throat could not be validated as the swabs were not tested for bacterial culture and it was primarily a study on epidemiology of viral-ARI. In both the studies presence of headache was associated with viral sore throat, however specificity was higher in the current study. The current study reports a good sensitivity and moderate specificity as compared to the study by Mistik et al. This could be due to higher proportion of sore throats contributed by viruses in the current study. The clinical scores need further validation for checking their applicability in Indian settings.
This is one of the first community-based studies on epidemiology of viral sore throat and a clinical prediction model for viral sore throat in India. Robust techniques were employed in data collection, handling the specimens and identification of organisms. Another strength was that the association was estimated with laboratory proven infections and not with presumptive viral sore throats. One of the limitations in the study was the small sample size of viral sore throat testing due to high-cost of conducting RT-PCR. Other limitation was both throat and nasal swab were obtained from a given case from which RNA was extracted for PCR testing. However, it is assumed that virus is implicated in sore throat even if shedding is only from nose. We did viral testing only for four viral pathogens. If we had we tested for more viral pathogens, proportion of viral sore throat among all sore throat cases was likely to be higher. Further studies need to be conducted to assess the distribution and burden in other parts of the country to come to a consensus on the epidemiology of viral sore throat.
| Conclusion|| |
Viral sore throat contributes to a significant problem in the community. This study adds to the information and knowledge about epidemiology of viral sore throats in India and also emphasizes on symptom attributes of URIs due to viral etiology. Such, clinical scores could be utilized in primary care settings for predicting viral URI, thereby guiding antibiotic prescription. These algorithms will be cost-effective, less time consuming and have a greater impact in aiding primary care physicians for optimal utilization of antibiotics.
What is already known?
Upper respiratory infections are the most common reason for consulting a doctor and are prescribed the maximum percentage of antibiotics.
What this study adds?
Viral sore throat contributes a significant burden in the community. Clinical scores could help in predicting viral sore throat thereby reducing the amount of prescribed antibiotics for sore throat.
The Institutional Ethics Committee of the AIIMS, New Delhi approved the study, with an institutional reliance by the United States Centers for Disease Control and Prevention (CDC) Institutional Review Board.
Financial support and sponsorship
The study is funded by a co-operative agreement between the United States Centers for Disease Control and Prevention (CDC) and the All India Institute of Medical Sciences (AIIMS), New Delhi. This work was supported by the United States Centers for Disease Control and Prevention [U01 IP000492].
Conflicts of interest
The authors do not have a commercial or other association that might pose a conflict of interest with respect to this study.
| References|| |
Mehta N, Schilder A, Fragaszy E, Evans HER, Dukes O, Manikam L, et al
. Antibiotic prescribing in patients with self-reported sore throat. J Antimicrob Chemother 2017;72:914-22.
Kakkar M, Walia K, Vong S, Chatterjee P, Sharma A. Antibiotic resistance and its containment in India. BMJ 2017;358:j2687.
Krishnan A, Amarchand R, Gupta V, Lafond KE, Suliankatchi RA, Saha S, et al
. Epidemiology of acute respiratory infections in children-preliminary results of a cohort in a rural north Indian community. BMC Infect Dis 2015;15:462.
International Institute for Population Sciences (IIPS) and Macro International. National Family Health Survey (NFHS-3), 2005–06: India: Volume I. Mumbai: IIPS; 2007. http://rchiips.org/nfhs/NFHS-4Reports/India.pdf
. [Last accessed on 2019 Nov].
Acharya D, Prasanna KS, Nair S, Rao RS. Acute respiratory infections in children: A community based longitudinal study in south India. Indian J Public Health 2003;47:7-13.
Walke SP, Das R, Acharya AS, Pemde HK. Incidence, pattern, and severity of acute respiratory infections among infants and toddlers of a peri-urban area of Delhi: A 12-month prospective study. Int Sch Res 2014:1-6. doi: 10.1155/2014/165152.
Zaman K. Acute respiratory infections in children: A community-based longitudinal study in rural Bangladesh. J Trop Pediatr 1997;43:133-7.
Kahbazi M, Fahmizad A, Armin S, Ghanaee RM, Fallah F, Shiva F, et al
. Aetiology of upper respiratory tract infections in children in Arak city: A community based study. Acta Microbiol Immunol Hung 2011;58:289-96.
Cauwenberge PBV, Mijnsbrugge AV. Pharyngitis: A survey of the microbiologic etiology. Pediatr Infect Dis J 1991;10:S39-42.
Ramani VK, Pattankar J, Puttahonnappa SK. Acute respiratory infections among under-five age group children at urban slums of Gulbarga city: A longitudinal study. J Clin Diagn Res 2016;10:LC08-13.
Mistik S, Gokahmetoglu S, Balci E, Onuk FA. Sore throat in primary care project: A clinical score to diagnose viral sore throat. Fam Pract 2015;32:263-8.
Tsai H-P, Kuo P-H, Liu C-C, Wang J-R. Respiratory viral infections among pediatric inpatients and outpatients in Taiwan from 1997 to 1999. J Clin Microbiol 2001;39:111-8.
Peng D, Zhao D, Liu J, Wang X, Yang K, Xicheng H, et al
. Multi-pathogen infections in hospitalized children with acute respiratory infections. Virol J 2009;6:155.
Lin TY, Huang YC, Ning HC, Tsao KC. Surveillance of respiratory viral infections among pediatric outpatients in northern Taiwan. J Clin Virol 2004;30:81-5.
Monto AS, Cavallaro JJ. The Tecumseh study of respiratory illness: II. Patterns of occurrence of infection with respiratory pathogens, 1965–1969. Am J Epidemiol 1971;94:280-9.
Arruda E, Hayden FG, McAuliffe JF, de Souza MA, Mota SB, McAuliffe MI, et al
. Acute respiratory viral infections in ambulatory children of urban northeast Brazil. J Infect Dis 1991;164:252-8.
Miser WF. Sinusitis and pharyngitis. In: Family Medicine: Principles and Practice. 6th
ed.. New York: Springer-Verlag; 2003.
Ruohola A, Waris M, Allander T, Ziegler T, Heikkinen T, Ruuskanen O. Viral etiology of common cold in children, Finland. Emerg Infect Dis 2009;15:344-6.
Manjarrez ME, Rosete DP, Rincón M, Villalba J, Cravioto A, Cabrera R. Comparative viral frequency in Mexican children under 5 years of age with and without upper respiratory symptoms. J Med Microbiol 2003;52:579-83.
Swamy Ma, Malhotra B, Janardhan Reddy P, Tiwari J. Profile of respiratory pathogens causing acute respiratory infections in hospitalised children at Rajasthan a 4 year's study. Indian J Med Microbiol 2018;36:163-71.
] [Full text]
Mishra P, Nayak L, Das RR, Dwibedi B, Singh A. Viral agents causing acute respiratory infections in children under five: A study from Eastern India. Int J Pediatr 2016;2016:1-8. doi: 10.1155/2016/7235482.
Broor S, Parveen S, Bharaj P, Prasad VS, Srinivasulu KN, Sumanth KM, et al.
A Prospective Three-Year Cohort Study of the Epidemiology and Virology of Acute Respiratory Infections of Children in Rural India. Poeta MD, editor. PLoS ONE. 2007 Jun 6;2(6):e491.
Laguna-Torres VA, Gómez J, Ocaña V, Aguilar P, Saldarriaga T, Chavez E, et al
. Influenza-like illness sentinel surveillance in Peru. PLoS One 2009;4:e6118.
Weigl JA, Puppe W, Gröndahl B, Schmitt HJ. Epidemiological investigation of nine respiratory pathogens in hospitalized children in Germany using multiplex reverse-transcriptase polymerase chain reaction. Eur J Clin Microbiol Infect Dis 2000;19:336-43.
Ho ZJM, Zhao X, Cook AR, Loh JP, Ng SH, Tan BH, et al
. Clinical differences between respiratory viral and bacterial mono- and dual pathogen detected among Singapore military servicemen with febrile respiratory illness. Influenza Other Respir Viruses 2015;9:200-8.
Ma X, Conrad T, Alchikh M, Reiche J, Schweiger B, Rath B. Can we distinguish respiratory viral infections based on clinical features? A prospective pediatric cohort compared to systematic literature review. Rev Med Virol 2018;28:e1997.
NCDC. National Treatment Guidelines for Antimicrobial Use in Infectious Diseases. New Delhi: National Center for Diease Control; 2016.
Kotwani A, Holloway K. Antibiotic prescribing practice for acute, uncomplicated respiratory tract infections in primary care settings in New Delhi, India. Trop Med Int Health 2014;19:761-8.
McIsaac WJ, Goel V, To T, Low DE. The validity of a sore throat score in family practice. CMAJ 2000;163:811-5.
Centor RM, Witherspoon JM, Dalton HP, Brody CE, Link K. The diagnosis of strep throat in adults in the emergency room. Med Decis Making 1981;1:239-46.
[Table 1], [Table 2], [Table 3]